EFECTOS DE LA ALTERACIÓN ANTRÓPICA EN BOSQUES TROPICALES SOBRE LA DIVERSIDAD DE ORGANISMOS EPÍFITOS (LÍQUENES Y BRIÓFITOS)

Transcripción

1 EFECTOS DE LA ALTERACIÓN ANTRÓPICA EN BOSQUES TROPICALES SOBRE LA DIVERSIDAD DE ORGANISMOS EPÍFITOS (LÍQUENES Y BRIÓFITOS) Angel Benitez Chavez-Tesis Doctoral 2016 Universidad Rey Juan Carlos EFECTOS DE LA ALTERACIÓN ANTRÓPICA EN BOSQUES TROPICALES SOBRE LA DIVERSIDAD DE ORGANISMOS EPÍFITOS (LÍQUENES Y BRIÓFITOS) Angel Raimundo Benitez Chavez: Tesis Doctoral 2016 Universidad Rey Juan Carlos Directores: María Prieto Álvaro y Gregorio Aragón Rubio Departamento de Biología y Geología, Física y Química Inorgánica

2 TESIS DOCTORAL EFECTOS DE LA ALTERACIÓN ANTRÓPICA EN BOSQUES TROPICALES SOBRE LA DIVERSIDAD DE ORGANISMOS EPÍFITOS (LÍQUENES Y BRIÓFITOS) EFFECTS OF TROPICAL FORESTS DISTURBANCE ON EPIPHYTE DIVERSITY (LICHENS AND BRYOPHYTES) ANGEL RAIMUNDO BENITEZ CHAVEZ Directores: María Prieto Álvaro Gregorio Aragón Rubio Área de Biodiversidad y Conservación Departamento de Biología y Geología, Física y Química Inorgánica UNIVERSIDAD REY JUAN CARLOS Octubre de 2016 i

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4 La Dra. María Prieto Álvaro y el Dr. Gregorio Aragón Rubio, profesores visitante y titular del Departamento de Biología y Geología, Física y Química Inorgánica de la Universidad Rey Juan Carlos, Certifican: Que los trabajos de investigaciones desarrollados en la memoria de tesis doctoral Efectos de la alteración antrópica en bosques tropicales sobre la diversidad de organismos epífitos (líquenes y briófitos) son aptos para ser presentados por Angel Raimundo Benitez Chavez ante el tribunal que en su día se consigne, para aspirar al Grado de Doctor en Conservación de Recursos Naturales por la Universidad Rey Juan Carlos de Madrid. V B Directora de Tesis Dra. María Prieto Álvaro V B Director de Tesis Dr. Gregorio Aragón Rubio iii

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6 A mis padres Gregorio y Esperanza v

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8 ÍNDICE Agradecimientos 1 Resumen 3 Antecedentes 6 Objetivos 16 Metodología general 17 Discusión general 23 Conclusiones 32 Lista de manuscritos 34 Afiliación de coautores 35 Bibliografía 36 CAPÍTULOS/CHAPTERS Capítulo I / Chapter I 53 Effects of tropical montane forest disturbance on epiphytic macrolichens Capítulo II / Chapter II 75 Large trees and dense canopies: key factors for maintaining high epiphytic diversity on trunk bases (bryophytes and lichens) in tropical montane forests Capítulo III / Chapter III 105 Functional traits of epiphytic lichens as indicators of forest disturbance level and predictors of total richness and diversity Capítulo IV / Chapter IV 147 Lichen diversity in tropical dry forests is highly influenced by the host tree traits including tree species Capítulo V / Chapter V 175 Additions to the bryophyte flora of Ecuador 2 / Adiciones a la Flora de Briófitas del Ecuador 2 Capítulo VI / Chapter VI 195 More than one hundred new records of lichens from Ecuador vii

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12 AGRADECIMIENTOS Agradezco a la Universidad Técnica Particular de Loja (UTPL), Secretaria Nacional de Educación Superior, Ciencia, Tecnología e Innovación (SENESCYT) y la Universidad Rey Juan Carlos por brindar las herramientas y los recursos necesarios para el desarrollo de este trabajo de investigación. A todos los integrantes del departamento de Ciencias Naturales de la UTPL de la ciudad de Loja, de manera especial a Ana Arévalo, Yadira González, Gabriela Cevallos, Geovanny Cango, Fernando Gaona y Elizabeth Guzmán por su colaboración en el trabajo de campo. Mil gracias a la desaparecida sección de sistemática de la UTPL conformada por Carlos Naranjo, Fani Tinitana, Omar Cabrera, Nixon Cumbicus y Diego Marín por su apoyo y colaboración durante el desarrollo de este trabajo de investigación, es muy grato seguir contando con su amistad y apoyo, mil gracias amigos. Al Dr. Adrián Escudero, Dra. Isabel Martínez, Dr. José María Iriondo, Dr. Marcos Méndez y Dr. Luis Cayuela de la Universidad Rey Juan Carlos, por su disposición y colaboración desinteresada durante el desarrollo de este trabajo. Adicionalmente agradezco a Silvia Santamaría, Sonia Merinero, Jesús López y Samuel por su colaboración y apoyo durante las diferentes estancias doctorales. Bueno para mis directores de tesis, empezando con el Dr. Gregorio Aragón solo tengo tres palabras respeto, admiración y sobre todo agradecimiento ya que gracias a su calidad profesional y personal he podido empezar el duro pero gratificante camino de la investigación. Mil Gracias Goyo por el tiempo y dedicación que le pusiste a este trabajo y por darme la oportunidad de hacer investigación en tu campo de estudio. Sin sentimentalismos que yo no soy muy bueno para eso, pero la verdad tengo una gran admiración por el gran trabajo que realizas y la visión que tienes para hacer investigación. A la Dra. María Prieto Álvaro, por todo su apoyo incondicional durante el desarrollo de este trabajo, gracias por seguir confiando en mis capacidades a pesar que muchas de las veces ya sobrepasaba tu gran paciencia. Gracias por enseñarme a determinar los líquenes, sobre todo los costrosos, que ahora ya los llamo crustáceos. Mil gracias a los dos por confiar en mí y darme esta gran oportunidad de que hayan sido mi guía durante este largo camino. 1

13 Así mismo quiero agradecer infinitamente al Profesor Robbert Gradstein por su calidad personal y profesional en los diferentes momentos que compartimos durante diferentes salidas de campo e investigaciones que hemos desarrollado en el campo de la briología. Mil gracias profesor por darme la oportunidad y sobre todo por confiar en mis capacidades. Mil gracias a mi amada familia de España, la familia de Robert, Francisca y Gregorio. De manera especial a Fátima y Johnny por su gran hospitalidad y por hacerme sentir como en casa y sobre todo por apoyarme en los momentos más difíciles durante mis estancias en España. Especialmente quiero agradecer a mi querido y amado sobrino Ismael siempre serás como el hijo que sueño tener, gracias por esperarme siempre con la comida en la mesa y en las mañanas compartir los desayunos sin importarte la hora que sea. Mil gracias Isma por todos los momentos compartidos que han sido geniales. A mis padres que se han convertido en los promotores y sobre todo los impulsores para poder llegar a cumplir con esta meta. Además a toda mi familia y sobrinos que gracias a su alegría he podido seguir adelante. Finalmente a la persona que se ha convertido en la alegría y paz que encontraba en los momentos más difíciles de mi vida (Anita), ya que gracias a su apoyo incondicional en las etapas de campo, de laboratorio e investigación he podido cumplir con esta etapa de mi vida, mil gracias por estar siempre para mí y esperarme aunque no haya estado cuando tú me necesitabas debido a mis estancias en España. 2

14 RESUMEN La alteración de los bosques es una de las principales causas de la pérdida de biodiversidad en los ecosistemas tropicales a nivel global. Los bosques húmedos montanos y estacionalmente secos tropicales están desapareciendo a ritmos alarmantes por lo que han sido catalogados como los más amenazados y de prioridad para la conservación. Estos ecosistemas se caracterizan por sus altos niveles de diversidad y endemismos de flora y fauna, donde los epífitos constituyen un grupo importante. Dentro de los epífitos, una fracción significativa está representada por líquenes y briófitos que, por sus características fisiológicas relacionadas con la disponibilidad de agua y luz, se han convertido en organismos modelo para evaluar cambios en el ambiente. A pesar de ello, los estudios centrados en analizar los efectos de la transformación de estos ecosistemas sobre los epífitos no vasculares son muy limitados y, de manera especial en los bosques estacionalmente secos. Por estos motivos, el objetivo general de esta tesis doctoral se centra en analizar los efectos de la alteración de los bosques tropicales sobre la diversidad de los organismos epífitos (líquenes y briófitos). Para ello, estudiamos conjuntamente la diversidad taxonómica (riqueza y composición) de epífitos no vasculares y la diversidad funcional de líquenes. La tesis se centra en Ecuador, considerado en las últimas décadas como uno de los países con mayor tasa de deforestación (1,8 %) de América Latina. Las zonas de estudio se localizaron específicamente en la región sur de Ecuador donde el 46% de los bosques originales se han reducido y la tasa de deforestación es alarmante con una tasa del 2,86 %. En los dos ecosistemas estudiados (bosques húmedos montanos y estacionalmente secos), se identificaron manchas de bosques con diferentes tipos de manejo. Se definieron tres categorías de manejo para los bosques montanos, constituidas por dos manchas de bosques primarios, dos de bosques secundarios y dos de bosques monoespecíficos de Alnus acuminata. Para los bosques estacionalmente secos se identificaron cuatro manchas de bosques correspondientes a dos categorías de manejo (bosques no alterados y bosques alterados). En cada bosque se analizaron los cambios en la diversidad de epífitos no vasculares a nivel de árbol y parcela; y se identificaron los factores ambientales (altitud, pendiente y orientación) y de estructura forestal (cobertura del dosel arbóreo, diámetro de los árboles, especie del árbol y características de la corteza), podrían limitar estas comunidades. Además, se analizaron los efectos de la alteración de los bosques montanos sobre la diversidad funcional de líquenes epífitos y se analizaron las formas de crecimiento como posibles indicadores de la riqueza total de líquenes epífitos. 3

15 Los resultados mostraron que la deforestación disminuye drásticamente la riqueza de epífitos no vasculares en bosques montanos y estacionalmente secos tropicales, donde los bosques no alterados (bosques primarios) mantienen una mayor diversidad en comparación con los bosques secundarios. En los bosques montanos la diversidad de macrolíquenes denominados epífitos de sombra (e.g. Leptogium, Lobaria, Pannaria, Plagiochila o Sticta), adaptados a condiciones de alta humedad fueron más afectadas por la pérdida de la cobertura arbolada, debido a cambios microclimáticos relacionados con la disponibilidad de humedad. Por el contrario, los epífitos de sol (e.g. Frullania, Graphis, Heterodermia o Usnea) estuvieron mejor representados en los bosques secundarios, debido a que están mejor adaptadas a condiciones con mayor intensidad lumínica. La estructura del bosque relacionada con la cobertura del dosel y el diámetro de los árboles, fueron los factores más influyentes en las comunidades de los epífitos no vasculares. Particularmente, líquenes y briófitos estuvieron directamente afectados por el diámetro de los árboles, relacionado con el área disponible para su establecimiento y desarrollo, mientras que los briófitos estuvieron también limitados por la apertura del dosel arbóreo, que conlleva cambios en el microclima (luz y humedad). La diversidad funcional de líquenes epífitos fue también afectada por la deforestación, condicionada por la cobertura del dosel y el diámetro de los árboles. Algunos rasgos funcionales (e.g. cianolíquenes) estuvieron relacionadas con el grado de alteración de estos bosques, por lo que pueden ser indicadoras del estado de conservación de estos bosques. Las formas de crecimiento (e.g. especies con talo gelatinoso, filamentoso y foliáceo placodioide) se relacionan con la riqueza total de líquenes en los bosques montanos, y se proponen, por tanto, como herramienta para realizar inventarios rápidos de biodiversidad y predecir la riqueza total de líquenes. La riqueza en los bosques estacionalmente secos fue limitada principalmente por el grosor de los árboles, la cobertura arbolada y por las características del forófito. A pesar de la aceptada asunción de que en los bosques tropicales la especificidad del forófito y las especies epífitas es nula, en los bosques estacionalmente secos las comunidades de líquenes fueron condicionadas por la especie del árbol hospedador (forófito). En los muestreos realizados se han encontrado un total de 374 especies epífitas no vasculares en los bosques montanos (307 líquenes y 67 briófitos), mientras que en los bosques estacionalmente secos se registraron 123 especies (122 líquenes 4

16 y un briófito). Debido al escaso conocimiento de las criptógamas de Ecuador, paralelamente a los estudios realizados se han encontrado nuevas citas regionales, nacionales y provinciales de líquenes y briófitos para Ecuador y Suramérica. Así, se han encontrado aproximadamente 200 nuevos registros, lo que demuestra la gran diversidad y el escaso conocimiento de los líquenes y briófitos en los bosques tropicales de Ecuador. 5

17 ANTECEDENTES Los principales conductores de la pérdida de biodiversidad en bosques tropicales incluyen los efectos directos de las actividades antrópicas como la destrucción de hábitat y la fragmentación, las especies invasoras o la sobreexplotación, así como los efectos indirectos de las actividades humanas como el cambio climático (Morris 2010). La deforestación y fragmentación se proponen como los factores que tienen un mayor impacto en la biodiversidad de bosques tropicales (Sala et al., 2000), siendo los principales responsables de cambios en la estructura y función de los ecosistemas (Saunders et al., 1991; Debinski & Holt 2001). Así, estas alteraciones implican la reducción de la superficie, pérdida de la calidad del hábitat y cambios en las condiciones bióticas y abióticas de los ecosistemas (Forman 1995), y tienen además efectos negativos para la biodiversidad (Vitousek 1994). En la actualidad, la deforestación en los trópicos constituye uno de los problemas ambientales más importantes con serias consecuencias económicas y sociales (Laurance 1999). A pesar de que los bosques tropicales albergan el 70% de las especies de animales y plantas del mundo, y de que influyen en el clima a escala local y mundial (Malhi & Phillips 2004), han sufrido una acelerada pérdida de su superficie original (Houghton 1994; Kammesheidt 2002; Tejedor Garavito et al., 2012; Tapia-Armijos et al., 2015). Así, la extracción de madera y las actividades agrícolas y ganaderas son las principales amenazas sobre los bosques húmedos montanos y los bosques estacionalmente secos (Henderson et al., 1991; Gentry 1995; Churchill et al., 1995; Gibbs et al., 2010; Fajardo et al., 2005; Miles et al., 2006). Numerosos estudios han evaluado las consecuencias de las rápidas transformaciones de los bosques originales, que han provocado una reducción de la diversidad de varios organismos de animales y vegetales, como en árboles (Fujisaka et al., 1998; Kessler et al., 2005; Espinosa et al., 2011), epífitos (Barthlott et al., 2001; Nöske et al., 2008; Werner & Gradstein 2009), aves (Sodhi 2002; Gray et al., 2007), mariposas (Barlow et al., 2007), escarabajos (Nichols et al., 2007; Gardner et al., 2008), polillas (Beck et al., 2002; Brehm & Fiedler 2005), hormigas y termitas (Lawton et al.,1998). Dentro de la variedad de organismos, uno de los más afectados por la deforestación son los epífitos no vasculares (líquenes y briófitos), debido a su sensibilidad a cambios en el ambiente (Gradstein 2008; Nöske et al., 2008; Werner & Gradstein 2009). 6

18 Bosques húmedos montanos tropicales Los bosques húmedos montanos tropicales o bosques nublados, ocupan alrededor de 48 millones de hectáreas y aproximadamente el 50% se encuentran en América Latina (Kapos et al., 2000). La extensión geográfica de los bosques húmedos montanos se ha establecido en la región comprendida entre los 20º S y 20º N de latitud y por encima de los 1000 m de altitud (Stadtmüller 1987; Churchill et al., 1995; Webster 1995). De manera general, estos bosques se distribuyen en las regiones montañosas y sub-montañosas entre los m de altitud, sin embargo en la parte insular y las costas de diferentes regiones donde el nivel de condensación de la neblina se produce a una menor altitud, estos bosques aparecen entre los m (Hamilton et al., 1995). Los bosques húmedos montanos aquí estudiados, presentan un dosel irregular con varios estratos de vegetación y árboles que pueden llegar hasta los 40 m de altura, un sotobosque relativamente denso, altas precipitaciones durante todo el año, con una gran influencia de nieblas y con ausencia de marcadas estaciones climáticas (Bruijnzeel 2005; Richter 2008). Los suelos mantienen gran humedad con alta presencia de materia orgánica, debido a que albergan una elevada proporción de biomasa relacionada principalmente con la gran diversidad de organismos epífitos (Hamilton et al., 1995; Brown & Kappelle 2001; Hamilton 2001). La alta diversidad de especies es una de las características de estos bosques, hecho que le confiere el reconocimiento de ser uno de los puntos calientes de biodiversidad y de prioridad para la conservación (Myers et al., 2000; Jørgensen et al., 2011). Ecuador es el segundo país de América Central y América del Sur con mayor superficie de este tipo de bosque ( hectáreas), de las cuales tan solo están protegidas (Brown & Kappelle 2001). En Ecuador este tipo de bosque se distribuye a ambos lados de la cordillera andina, entre los m de altitud, y presenta una rica vegetación dominada por epífitos (Sierra 1999). Las diferentes actividades antrópicas afectan a los bosques húmedos montanos, originando pequeños fragmentos aislados producto de la regeneración natural (vegetación secundaria) dentro de una matriz agrícola y de pastoreo (Gibson et al., 2011; Tabarelli et al., 2010). En consecuencia, la destrucción de los bosques primarios viene acompañada por la expansión de los bosques secundarios de diferentes tamaños y edades en la mayor parte de las zonas tropicales. Ecuador presenta la tasa más alta de deforestación en América Latina, con una disminución del 1,8% anual de bosques primarios (FAO 2011). Un patrón similar se observa en la región sur de Ecuador con una tasa anual de deforestación del 2,86% entre los años 1989 y 2008, donde el área 7

19 de vegetación nativa se redujo cerca del 49%, debido a que solo el 9,8 % de esta superficie se encuentra protegida (Tapia-Armijos et al., 2015). Los bosques primarios se definen como bosques maduros o antiguos que han experimentado poca o ninguna perturbación humana (Gibson et al., 2011). Estos bosques presentan coberturas arboladas superiores al 80%; se caracterizan por presentar diferentes estratos, definidos por una vegetación arbustiva, un sotobosque denso, y un dosel arbóreo que alcanza los m de altura dominados principalmente por especies de la familia Podocarpaceae (Decussocarpus y Podocarpus) y algunas especies del género Clusia, Cinchona y Weinmannia (Barthlott et al., 2001; Sporn et al., 2009; Benitez et al., 2012). Los bosques secundarios de definen como aquellos ecosistemas que se han originado como consecuencia del impacto humano en los sistemas naturales forestales, excluyendo las plantaciones (Brown & Lugo 1990). Estos bosques pueden aparecer después de los procesos de deforestación y un posterior abandono de actividades relacionadas con la agricultura y ganadería (Brown & Lugo 1990; Gardner et al., 2008; Lugo 2009). Es decir, resultan de la regeneración después de un moderado uso antrópico relacionado con la tala selectiva, pastoreo, recolección de leña, y pequeñas quemas para tierras de cultivos (Brown & Lugo 1990; Holz 2003). Los bosques estudiados provienen de talas selectivas de los bosques primarios de hace años, por lo que presentan un dosel arbustivo bien desarrollado; sin embargo, el dosel arbóreo está compuesto de árboles aislados de hasta 30 m de altura que dan como resultado un dosel más abierto (50-75%). Están caracterizados por especies de la familia Melastomataceae y Lauraceae (Barthlott et al., 2001; Nöske et al., 2008; Benitez et al., 2012). Otra categoría de vegetación secundaria es producida por la total eliminación de los bosques originales, que dan como resultado bosques secundarios monoespecíficos de Alnus acuminata Kunth. Estos bosques están dominados por arboles jóvenes (10-20 años) de una especie pionera y nativa de los Andes, que gracias a la rápida germinación y crecimiento coloniza eficazmente áreas abiertas como son los pastizales y tierras de cultivo que han sido abandonadas. Estructuralmente se caracterizan por presentar un único estrato arbóreo, cobertura de dosel inferior al 50% con árboles de hasta 20 m de altura (Hofstede et al., 1999; Fehse et al., 2001). La estructura de los bosques monoespecíficos de A. acuminata es muy similar a las plantaciones (e.g. Cedrela y Pinus), muy uniforme debido a la ausencia de 8

20 un sotobosque (Barthlott et al., 2001), con la diferencia de que éstos se originan por la regeneración natural del bosque. Bosques tropicales estacionalmente secos A nivel mundial, los bosques tropicales estacionalmente secos (BTES) ocupan el 42% de la superficie de los bosques tropicales (Miles et al., 2006), e incluyen bosques caducifolios y semicaducifolios que crecen en áreas tropicales sujetas a una severa estacionalidad climática (Murphy & Lugo 1986). En el Neotrópico se distribuyen desde el norte de México hasta el sur brasileño y representan el 66,7% de la superficie de bosques estacionalmente secos del mundo (Miles et al., 2006). De manera particular, en la región biogeográfica Tumbesina de Ecuador y Perú, presentan la mayor superficie, con km 2, y se caracterizan por elevado número de endemismos (Dinerstein et al., 1995). Al mismo tiempo, comprenden una de las zonas más amenazadas por las actividades antrópicas (Best & Kessler 1995). Los bosques estacionalmente secos se caracterizan por una marcada estacionalidad climática, precipitación anual inferior a 1600 mm y un marcado período de sequía que se prolonga hasta 5 o 6 meses al año con una precipitación total menor a 100 mm (Pennington et al., 2000). Una particularidad especial de estos bosques es la pérdida estacional de las hojas (75% de las especies) durante la estación seca, mientras que durante la estación lluviosa presentan una estructura de bosque siempre verde (Aguirre et al., 2006). En la época seca se produce una acumulación de hojarasca debido a la baja humedad durante esta estación, que se descompone cuando llega la época de lluvias (Pennington et al., 2000), por lo tanto presentan una productividad primaria neta baja (Aguirre et al., 2006). Un factor clave en estos bosques es la disponibilidad de agua, convirtiéndose en un factor limitante para el establecimiento, supervivencia y desarrollo de las plantas (Ruthemberg 1980). Estos ecosistemas tienen una menor diversidad de especies (Gentry 1995), menor área basal y altura de los árboles que los bosques montanos tropicales (Murphy & Lugo 1986; Moony et al., 1995; Linares-Palomino 2004). Así mismo, la diversidad de epífitos es más baja, debido al incremento de la incidencia lumínica y a la disminución de la humedad (Gentry & Dodson 1987; Werner & Gradstein 2009). Sin embargo, están caracterizados por un alto número de especies endémicas (Trejo & Dirzo 2002; Fajardo et al., 2005). En cuanto a los efectos antrópicos, estos ecosistemas tienen los mismos problemas que los bosques húmedos montanos: talas selectivas, extracción 9

21 de madera y actividades agrícolas o ganaderas (Fajardo et al., 2005; Miles et al., 2006; Espinosa et al., 2011) que provocan pérdida de biodiversidad. Los bosques tropicales estacionalmente secos de Ecuador se localizan en las provincias de Manabí, Guayas, El Oro y Loja, entre los 0 y los 700 m de altitud. Estos bosques están caracterizados por especies representativas como Ceiba trichistandra (A. Gray) Bakh., especies de la familia Malvaceae como Eriotheca ruizii (K. Schum.) A. Robyns y especies del género Tabebuia (T. chrysantha y T. billbergii) que son muy importantes recursos maderables (Aguirre et al., 2006). Otras especies del estrato arbóreo son Bursera graveolens (Kunth) Triana & Planch., Cochlospermum vitifolium (Willd.) Spreng., Cynophalla mollis (Kunth) J. Presl, junto con vegetación arbustiva (Malpighia emarginata L. y diferentes especies del género Croton). La estructura forestal presenta una densa cobertura entre el 85-90%, con un estrato superior de m de altura y un estrato denso de arbustos (Werner & Gradstein 2009). En la actualidad la mayor parte de estos bosques se han convertido en fragmentos de vegetación secundaria de diferentes tamaños inmersos en un paisaje de cultivos y pastos, dado que muchas de estas zonas poseen excelentes suelos para la agricultura y desarrollo de la ganadería (Kalacska et al., 2005). Además otros tipos de transformaciones se deben a los recursos madereros que ofrecen, dando como resultado la pérdida de cobertura forestal a causa de la extracción de algunas especies arbóreas características de estos bosques (Sanchez-Azofeifa et al., 2005; Sanchez-Azofeifa & Portillo-Quintero 2011). Generalmente, los bosques secundarios son el producto de la regeneración natural ligado al abandono de actividades ganaderas, agrícolas, tala selectiva para madera y la recolección de leña (Werner & Gradstein 2009). La cobertura del dosel arbóreo de estos bosques secundarios está comprendida entre el 40-70% (Werner & Gradstein 2009), y su estructura forestal se caracteriza por la presencia de antiguos árboles dispersos (B. graveolens, C. mollis, E. ruizii, T. chrysantha, y Ziziphus thyrsiflora Benth.) con ausencia, generalmente, del estrato arbustivo. Epífitos como organismos indicadores de cambios en el ambiente Los organismos epífitos comprenden una importante fracción de la diversidad, representando entre el 25-50% de las especies en los bosques tropicales (Gentry & Dodson 1987; Benzing 1995, 2004). Específicamente para Ecuador, los epífitos abarcan más del 25% de la riqueza de especies de plantas vasculares (Küper et al., 10

22 2004). Los epífitos están bien representados por orquídeas, bromelias, helechos, briófitos y líquenes (Gradstein 2008). Los líquenes y briófitos constituyen un importante componente de la biodiversidad (Pharo & Beattie 1997), representando una parte integral de los ecosistemas forestales (Lesica et al., 1991) donde cumplen funciones importantes relacionadas con la diversidad, biomasa y funcionamiento (e.g. ciclos hidrológicos y minerales) de estos ecosistemas (Holz & Gradstein 2005; Gradstein 2008). Además, brindan refugio y alimento a una variedad de insectos, microrganismos, pequeños reptiles, anfibios y ciertos grupos de aves (Nadkarni & Matelson 1989; Nadkarni & Longino 1990; Yanoviak et al., 2007). Los epífitos en los bosques húmedos montanos tropicales son muy diversos, debido a la constante humedad de estos ecosistemas (Barthlott et al., 2001; Nadkarni et al., 2001; Gradstein 2008; Mandl et al., 2010); sin embargo, un patrón diferente se observa en los bosques estacionalmente secos, donde su diversidad desciende debido al incremento de la intensidad lumínica y a una menor disponibilidad hídrica (Yeaton & Gladstone 1982; Gentry & Dodson 1987; Werner & Gradstein 2009; Higuera & Wolf 2010; Vergara-Torres et al., 2010; de Rosa-Manzano et al., 2014). A pesar de ello en los bosques estacionalmente secos pueden aparecer altos niveles de endemicidad (Werner 2008). Estos organismos se han definido como elementos característicos de los bosques húmedos montanos y estacionalmente secos tropicales (Mondragón et al., 2004; Gradstein 2008). Además, se han convertido en un grupo modelo para evaluar cambios en el ambiente relacionado con alteraciones antrópicas (Acebey et al., 2003; Holz & Gradstein 2005; Gradstein 2008; Nöske et al., 2008; Aragón et al., 2010; Benitez et al., 2012), contaminación del aire (Käffer et al., 2011; Ochoa-Jimenez et al., 2015) y calentamiento global (Gignac 2001; Hauck 2009). Factores que limitan la diversidad y composición de las comunidades epífitas Los organismos epífitos están condicionados por variables macro y microambientales que afectan su diversidad y distribución a escala local y regional (McCune et al., 1997; Will-Wolf et al., 2002; Sillet & Antoine 2004; Perhans et al., 2007; Gradstein 2008). Las variables orográficas y climáticas (precipitación, temperatura, altitud) condicionan la diversidad de especies (Hauck & Spribille 2005, Marini et al., 2011), mientras que a nivel local son la estructura del bosque y el microclima los principales conductores de la diversidad (Sipman & Harris 1989; Wolseley & Aguirre- Hudson 1997; Holz & Gradstein 2005; Sporn et al., 2009; Norman et al., 2010; Mandl et al., 2010). 11

23 La humedad es un factor clave para los epífitos, y especialmente para los organismos poiquilohídricos como los líquenes y briófitos, que se distribuyen de manera diferente a lo largo de un gradiente de humedad (Sillet & Antoine 2004; Gradstein 2008). Por ejemplo, los líquenes que tienen alga verde como fotobionte son más tolerantes a la desecación que los cianolíquenes, que requieren niveles de hidratación del talo superiores al 80% para poder obtener óptimos fotosintéticos (Nash 1996); así mismo, los briófitos (incluidas hepáticas) son menos tolerantes a la desecación que los líquenes (Proctor et al., 2007). Por lo tanto, la diversidad y biomasa de briófitos y cianolíquenes es alta en bosques húmedos, mientras que los clorolíquenes son más abundantes en ambientes con menor humedad (Sillet & Antoine 2004). La luz también influye sobre la diversidad y distribución de las comunidades epífitas (Sillet & Antoine 2004; Hauck 2011). Algunas especies (especialmente las de borde de bosque, o las que viven en zonas más elevadas de los troncos) están adaptadas a una alta luminosidad, con saturación fotosintética por encima de los 500 µmolm -2 s -1 PFD (Photon Flux Density), mientras que otras que viven en el interior de bosques, y en zonas de la base de los troncos pueden saturarse por encima 150 µmolm -2 s -1 PFD (e.g. Pseudocyphellaria, Green et al., 1997). Los árboles del sotobosque reciben una cantidad de luz menor en comparación con el dosel superior (Hauck et al., 2011), lo que implica una estratificación de las comunidades epífitas en función de estos factores (Sillet & Antoine 2004; Gradstein 2008). La temperatura también puede tener efectos directos en la diversidad de briófitos y líquenes epífitos (Sillet & Antoine 2004). Así, los cianolíquenes están adaptados a temperaturas elevadas con puntos de compensación altos (e.g. Leptogium phyllocarpum), por lo tanto bajas temperaturas podrían afectar las tasas de colonización de las especies de cianolíquenes (Sillet & Antoine 2004). A nivel local, las diferentes transformaciones de los ecosistemas originales tienen consecuencias directas en los organismos epífitos, relacionadas principalmente con los cambios en los siguientes factores: 1. La alteración de la estructura forestal (cobertura arbolada) implicaría un aumento en la incidencia lumínica y humedad (microclima), que se traduce en un descenso de la disponibilidad hídrica respecto a las condiciones originales (Hedenås & Ericson 2003; Sillet & Antoine 2004; Gradstein 2008). Bajo esta premisa se ha determinado una 12

24 relación negativa entre la disminución de la cobertura arbolada y la diversidad de epífitos (Gradstein 2008; Werner & Gradstein 2009; Benitez et al., 2012, 2015). 2. La tala selectiva implicaría la pérdida del forófito (hospedador) para las especies epífitas, que se traduce en la pérdida de hábitat para su establecimiento y desarrollo. Por ello, la diversidad de forófitos se ha determinado como un factor limitante en la diversidad de las comunidades epífitas en diferentes bosques (McGee & Kimmerer 2002; Hauck 2011; Nascimbene et al., 2009; Király et al., 2013), muy relacionado con la especificidad del hospedador. El debate sobre la relación entre el hospedador y las comunidades epífitas pone de relieve dos visiones opuestas. La primera visión detalla la relación directa entre los epífitos y el árbol, con una especificidad entre el epífito y su hospedador (Berg et al., 2002; García-Suárez et al., 2003; Szövényi et al., 2004; Löbel et al., 2006; Hirata et al., 2009; Vergara-Torres et al., 2010; Király et al., 2013). Por el contrario, la visión alternativa detalla poca o ninguna relación entre el árbol huésped y los epífitos (Cornelissen & ter Steege 1989; Cáceres et al., 2007; Soto- Medina et al., 2012; Rosabal et al., 2013). 3. El tamaño y la edad del hospedador también se han identificado como factores determinantes de la diversidad de las comunidades epífitas, en respuesta al área y tiempo disponible para la colonización (Fritz et al., 2008; Ranius et al., 2008; Aragón et al., 2010; Benitez et al., 2012, 2015). 4. Finalmente, las características físicas y químicas de la corteza de los hospedadores, como la textura, profundidad, capacidad de retención de agua, estado de nutrientes y ph son otros factores que afectan a las comunidades epífitas (Callaway et al., 2001; Cáceres et al., 2007; Rosabal et al., 2013). En este contexto, se han definido dos visiones generales relacionadas con los efectos de la deforestación sobre los organismos epífitos en bosques montanos. La primera sostiene que la riqueza de especies disminuye conforme aumenta la alteración de los bosques (Barthlott et al., 2001; Acebey et al., 2003; Gradstein 2008; Gradstein & Sporn 2010), mientras que la otra corriente mantiene que no existen efectos negativos sobre el número de especies, aunque sí que existen cambios en la composición de las comunidades (Hietz-Seifert et al., 1996; Flores-Palacios & García-Franco 2006; Werner & Gradstein 2009; Larrea & Werner 2010). Esta variación en los patrones observados podría estar relacionado con las diferencias en la taxones estudiados, el nivel de perturbación, la diversidad de especies de árboles o incluso, la edad de la 13

25 vegetación secundaria (Heitz et al., 2006; Gradstein 2008). A diferencia, en los bosques tropicales secos, un estudio centrado en bosques monoespecíficos de Acacia macracantha, señala que la riqueza de epífitos disminuye significativamente al aumentar el grado de alteración, con un mayor efecto en los briófitos (Werner & Gradstein 2009). Las comunidades epífitas desde una perspectiva funcional Aunque de forma general, las especies se describen como entidades taxonómicas, también pueden clasificarse a través de sus rasgos funcionales (traits), que son características morfológicas, fisiológicas o fenológicas medibles a nivel de individuo y que afectan a su crecimiento, reproducción y desarrollo (Violle et al., 2007). Los rasgos funcionales se han determinado como una característica importante para entender el funcionamiento de los ecosistemas (Violle et al., 2007; Mokany et al., 2008), debido a que están directamente influenciados por factores bióticos y abióticos. Por ello, un enfoque alternativo o complementario es el uso de los rasgos funcionales de los organismos epífitos (líquenes y briófitos) como una herramienta que facilite el entendimiento de la estructura y funcionamiento de complejos ecosistemas como los bosques tropicales. La diversidad funcional puede proporcionar información útil sobre los procesos y servicios ecosistémicos (Mokany et al., 2008). La mayor parte de investigaciones relacionada con los efectos de la deforestación sobre los rasgos funcionales se han llevado a cabo en plantas vasculares (Díaz et al., 1999, 2002, 2007; Mabry & Fraterrigo 2009; Laliberte et al., 2010; Sabatini et al., 2014). Sin embargo, estos estudios son muy escasos en líquenes epífitos (Stofer et al., 2006; Giordani et al., 2012). Los rasgos funcionales de los organismos epífitos (líquenes y briófitos) relacionados con la forma de crecimiento, tipo de fotobionte, estrategia de reproducción y presencia de metabolitos secundarios se han utilizado como indicadores efectivos de cambios en el ambiente ligados a diferentes procesos: cambio climático (Ellis & Coppins 2006; Johansson et al., 2007; Marini et al., 2011; Giordani et al., 2012; Pinho et al., 2012; Li et al., 2013, Matos et al., 2015), contaminación del aire (Llop et al., 2012) o como indicadores de biodiversidad (Oishi 2009, Pardow et al., 2012; Aragón et al., 2016). Potencialmente los diferentes rasgos funcionales de líquenes epífitos pueden ser usados y se proponen como herramientas para establecer políticas de manejo y conservación (Stofer et al., 2006; Pinho et al., 2012; Li 14

26 et al., 2013). A pesar de ello, la mayor parte de estudios se han enfocado en ecosistemas templados y boreales, por lo que las medidas de conservación no pueden generalizarse a los ecosistemas tropicales donde los estudios son limitados (Koch et al., 2013). De esta forma, el uso combinado de la diversidad taxonómica y funcional puede convertirse en una alternativa eficaz para entender los efectos de la alteración de los bosques tropicales sobre la diversidad de líquenes y briófitos epífitos. 15

27 OBJETIVOS El objetivo principal de esta tesis es analizar los efectos de la alteración antrópica de los bosques tropicales sobre la diversidad (taxonómica y funcional) de organismos epífitos (líquenes y briófitos), y ampliar el estado de conocimiento relacionado con la diversidad de estos organismos que han sido poco estudiados en Ecuador. En una primera parte tratamos de evaluar los efectos de la alteración antrópica, concretamente la deforestación, sobre los macrolíquenes epífitos. Sin embargo, los macrolíquenes solo constituyen una pequeña fracción de la diversidad de los organismos epífitos. Por ello, en una segunda etapa nos centramos en evaluar la respuesta de epífitos no vasculares (macro y microlíquenes y briófitos) a la degradación de los bosques. Estos estudios se complementaron al analizar los efectos de la degradación de los bosques sobre los rasgos funcionales de líquenes epífitos. Posteriormente, nos centramos en analizar los efectos de la alteración de los bosques secos sobre la diversidad de líquenes y briófitos. Estos ecosistemas presentan marcadas diferencias con los bosques montanos relacionadas con la estacionalidad, diversidad y estructura forestal. De forma paralela a estos estudios, se ha recopilado toda la información relativa a la distribución de las especies identificadas, haciendo especial hincapié sobre aquellas que presentan hábitats novedosos o ampliaciones considerables en su área de distribución. Los objetivos específicos de esta tesis doctoral son los siguientes: 1. Analizar los efectos de la alteración de los bosques húmedos montanos y tropicales estacionalmente secos sobre la diversidad taxonómica (riqueza y composición) de epífitos no vasculares. 2. Evaluar los factores que condicionan la diversidad de líquenes y briófitos epífitos en los bosques húmedos montanos y tropicales estacionalmente secos bajo un gradiente de alteración. 3. Analizar los efectos de la alteración sobre los diferentes rasgos funcionales de líquenes epífitos como aproximación alternativa al estudio de la degradación de los bosques montanos tropicales. 4. Estudiar la diversidad, ecología y distribución de líquenes y briófitos en bosques montanos y estacionalmente secos del Sur de Ecuador. 16

28 METODOLOGÍA GENERAL En este apartado se describen el área de estudio, el diseño, la recolección de datos, así como los análisis estadísticos empleados de una forma general. Sin embargo en el apartado de Material y Métodos de cada capítulo se describen con detalle los métodos utilizados para alcanzar los objetivos planteados en cada uno de los capítulos. 1. Área de estudio Los muestreos se han realizado en remanentes de bosques húmedos montanos y bosques tropicales estacionalmente secos con diferentes grados de manejo. Los bosques se localizaron en las provincias de Loja y El Oro en la región sur de Ecuador (Figura 1). Figura 1. Área de estudio. Provincias de Loja y El Oro de la región del Sur de Ecuador. : localización de los bosques estudiados. Bosques húmedos montanos tropicales (Capítulos I, II, III, V y VI) El estudio se realizó en remanentes de bosques húmedos montanos situados entre los m de altitud en la provincia de Loja de la Región sur de Ecuador (Figura 1). La temperatura media anual es de 20º C, con precipitaciones anuales 17

29 comprendidas entre los mm y con un 80% de humedad relativa (Instituto Nacional de Meteorología en Hidrología INAMI). El trabajo de campo se realizó entre mayo y diciembre de Se seleccionaron tres categorías de manejo con dos remanentes de bosques para cada una de ellas: 1. Fragmentos de bosques primarios (PF, Figuras 2A y B): caracterizados por una densa cobertura, comprendida entre el 80-85%, y con grandes árboles de metros de altura (e.g. Podocarpus oleifolius D. Don). 2. Fragmentos de bosques secundarios (SF, Figura 2C): bosques que se han regenerado después de sufrir una tala selectiva de los bosques primarios hace 45 años (Brown & Lugo 1990; Holz 2003). La cobertura arbolada está comprendida entre el 60-70% con especies de la familia Melastomataceae y Lauraceae de hasta metros de altura. 3. Fragmentos de bosques monoespecíficos de Alnus acuminata Kunth (MF, Figura 2D): bosques jóvenes dominados por esta especie nativa y pionera de los Andes. Estos bosques se caracterizan por presentar una estructura uniforme y por la ausencia de sotobosque. La cobertura arbolada es inferior al 50% con árboles hasta los 20 metros de altura. Bosques tropicales estacionalmente secos (Capítulos IV, V y VI) Este estudio se realizó en la Reserva Ecológica Arenillas ubicada en la provincia de El Oro (Figura 1), con una superficie de 17 hectáreas, comprendida entre los m de altitud y una vegetación de bosque seco deciduo y matorral seco. El clima está caracterizado por una época seca y una lluviosa con una precipitación media de 152 y 515 mm respectivamente, y una temperatura máxima diaria de ca. 25 C (Espinosa et al., 2015). El trabajo de campo se realizó entre enero y diciembre de Se seleccionaron dos categorías de alteración con dos fragmentos de bosques para cada una de ellas: 1. Fragmentos de bosques secos no alterados (Figura 1E): bosques conservados con especies leñosas predominantes de Bursera graveolens (Kunth) Triana & Planch., Cochlospermum vitifolium (Willd.) Spreng., Cynophalla mollis (Kunth) J. Presl Eriotheca ruizii (K. Schum.) A. Robyns y Tabebuia chrysantha G. Nicholson. Las 18

30 especies características del sotobosque correspondieron a arbustos de Malpighia emarginata L. y especies del género Croton. 2. Remanentes de bosques secos alterados (Figura 1F): bosques alterados caracterizados por tener una menor densidad arbórea y escasa vegetación arbustiva. Presumiblemente se establecieron como árboles aislados luego de los diferentes usos del suelo. Las especies dominantes fueron Cynophalla mollis, Tabebuia chrysantha y Ziziphus thyrsiflora Benth. 2. Diseño de muestreo y recolección de datos Bosques húmedos montanos tropicales (Capítulos I, II, III, V y VI). Para cada una de las categorías de alteración (3 categorías) se seleccionaron dos fragmentos de bosque (6 bosques). En cada bosque se establecieron 10 parcelas de 5 x 5 m con una separación entre parcelas de más de 50 metros. En cada parcela se seleccionaron 4 árboles, donde se establecieron 6 cuadrantes de 20 cm x 30 cm en dos orientaciones (N y S) y a tres alturas en el tronco de el árbol: altura 1 (0-50 cm), altura 2 ( cm) y altura 3 ( cm). En los 240 árboles se tomaron medidas de presencia y cobertura de todas las especies. A nivel de parcela se tomaron medidas de la cobertura arbolada, inclinación, altitud, orientación, y a nivel de árbol, el diámetro (DBH). Bosques tropicales estacionalmente secos (Capítulo IV, V y VI) Para cada una de las categorías de alteración (2 categorías) se seleccionaron dos remanentes de bosque (4 bosques). En cada bosque se establecieron 4 parcelas de m con una separación entre parcelas de más de 100 metros. En cada parcela se identificaron todos los árboles y arbustos con un DBH > 5 cm. En cada árbol se establecieron 4 cuadrantes de cm y para los arbustos de cm en dos orientaciones (N y S) y a dos alturas en el tronco de el árbol: altura 1 (0-100 cm) y altura 2 ( cm). Se tomaron medidas de presencia y cobertura de todas las especies en un total de 513 árboles y arbustos. Para los capítulos I, II, III las condiciones de luz se estimaron mediante la medición de la cobertura arbolada (%) y para el capítulo IV se midió la apertura del dosel (%) usando fotografías hemisféricas digitales (Figuras 1G y H). Las fotografías fueron registradas siempre en días nublados y la altura del pecho (1,3 metros de altura), con una cámara digital nivelada horizontalmente y con una lente de ojo de pez. Las fotografías fueron analizados utilizando el programa Gap Light Analyzer (GLA) ver. 2.0 (Frazer et al., 1999). 19

31 A B C D E F G H Figura 2. Tipos de bosques estudiados. (A) y (B) Bosques primarios montanos; (C) Bosques secundarios montanos; (D) Bosques monoespecíficos de Alnus acuminata; (E) Bosque seco conservado; (F) Bosque seco alterado; (G) Foto hemisférica de un bosque seco no alterado; (H) Foto hemisférica de un bosque seco alterado. 20

32 3. Identificación de especies Para la identificación de especies se utilizaron claves taxonómicas generales (Brodo et al., 2001; Nash III et al., 2002, 2004, 2007) y claves específicas de las diferentes familias y géneros (e.g. Brako 1991; Egea & Torrente 1993; Tehler 1997; Gradstein et al., 2001; Gradstein & Costa 2003; Frisch et al., 2006; Rivas-Plata et al., 2006; Cáceres 2007; Aptroot et al., 2008, 2009; Brodo et al., 2008; Timdal 2008; Lücking et al., 2008, 2009; Aptroot 2012; Moncada et al., 2013; Aptroot et al., 2014). Se utilizaron técnicas de microscopía y pruebas químicas basadas en fluorescencia de luz ultravioleta (UV), reacción con K (10% de agua en solución de hidróxido de potasio), C (lejía comercial) y solución con Lugol (I) en las diferentes estructuras de las especies. La nomenclatura para briófitos sigue a Tropicos ( y para líquenes a MycoBank ( y LIAS (A Global Information System for Lichenized and Non-Lichenized Ascomycetes: Todas las muestras fueron depositadas en el Herbario HUTPL-Colección de briófitos y líquenes. 4. Análisis de datos En los capítulos I, II, III, y IV se analizaron los efectos de los factores ambientales (cobertura arbolada, altitud, inclinación, orientación y DBH) sobre la riqueza, diversidad y los rasgos funcionales de especies utilizando modelos mixtos lineales generalizados (GLMMS) (McCullagh & Nelder 1989). Dado que los análisis de datos se realizaron a escala de árbol y parcela se usaron los modelos mixtos, para incluir el efecto aleatorio de la parcela o bosque, dependiendo de la escala de trabajo. Todos los GLMMS se realizaron con el programa estadístico SAS (GLIMMIX ver. 8 for SAS/STAT). Adicionalmente, para el capítulo IV se utilizaron modelos lineales generalizados (GLM) para determinar los efectos de la especie de hospedador sobre la riqueza de líquenes. Los GLM fueron realizados en el programa estadístico R con el paquete nlme (Pinheiro et al., 2008). En los capítulos I, II, IV se analizaron los cambios en la composición de especies en función del grado de alteración mediante análisis multivariados basados en permutaciones (PERMANOVA) en el programa estadístico PRIMER (Anderson et al., 2008). Adicionalmente, se realizó un análisis de ordenación multidimensional NMDS con los valores de cobertura de las especies que fueron transformados a log10(x+1) y se utilizó la medida de distancia Bray Curtis para determinar la similitud en la composición de especies entre los diferentes niveles de 21

33 alteración. En el capítulo III se realizaron análisis de especies indicadoras (ISA, Dufrêne & Legendre 1997; Koch et al., 2013) para determinar qué grupo funcional es el mejor indicador de la alteración de los bosques y correlaciones lineales de Pearson para relacionar la riqueza total de especies de líquenes en función de las formas de crecimiento. En los capítulos II y IV, para identificar qué factores influyen en la composición de las comunidades epífitas, se realizó una correlación (r 2 ) entre los dos primeros ejes del NMDS y las variables ambientales con el paquete vegan (Oksanen et al., 2013). Los NMDS fueron realizados en el programa estadístico R (R Development Core Team 2011). 22

34 DISCUSIÓN GENERAL A pesar de los esfuerzos de la última década destinados a entender los efectos de la deforestación sobre la diversidad taxonómica (riqueza y composición) de los organismos epífitos en ecosistemas tropicales (bosques montanos y estacionalmente secos), sólo unos pocos estudios se han centrado en briófitos y líquenes (Gradstein 2008; Nöske et al., 2008; Werner & Gradstein 2009; Gradstein & Sporn 2010). De esta manera, los escasos y controvertidos resultados no han permitido definir un patrón general de la respuesta de estos organismos a los procesos de deforestación de los bosques. Por otro lado, un enfoque alternativo y complementario, que ha producido interesantes resultados en bosques templados y boreales es el uso de la diversidad funcional de líquenes epífitos en repuesta a los cambios ambientales derivados de la deforestación (Stofer et al., 2006; Girodani et al., 2012). El estudio de la diversidad funcional contribuye al entendimiento de los diferentes procesos involucrados en el funcionamiento en estos ecosistemas (Mokany et al., 2008). Por estos motivos, esta tesis se centra en el estudio de los efectos de la alteración de los bosques montanos y estacionalmente secos sobre la diversidad taxonómica (riqueza y composición) y funcional de las comunidades de epífitas no vasculares (líquenes y briófitos). Así mismo, también se pretende estudiar cuáles son los factores ambientales y de estructura del bosque que influyen sobre estas comunidades. De manera general, demostramos que la diversidad taxonómica de las comunidades epífitas no vasculares (macrolíquenes, microlíquenes y briófitos) fue drásticamente afectada por la deforestación, y por los cambios asociados a ella como cambios en la cobertura del dosel o en el tamaño de los árboles (diámetro) (capítulos I, II). Otros factores como la especie de hospedador y sus características también se han observado que afectan a las comunidades criptógamas, en este caso en los bosques estacionalmente secos (capítulo IV). En un primer estudio, se determinó que los macrolíquenes, y en especial los epífitos de sombra, que incluyen a las especies con cianobacteria (cianolíquenes) y aquellas que no sintentizan metabolitos secundarios en córtex o médula (e.g. Leptogiun, Lobaria, Sticta) fueron más abundantes en los bosques primarios y las más afectadas por la deforestación (Capítulo I). Muchos de estos cianolíquenes están restringidos a bosques maduros, con elevada cobertura arbolada y árboles de gran tamaño, que garantizan condiciones de alta humedad. Son especies con unos requerimientos hídricos muy elevados, ya que alcanzan óptimos fotosintéticos con 23

35 hidrataciones entre el % de su peso seco, y además sufren fotoinhibición con la excesiva radiación (Lange et al., 1993; Jovan & McCune 2004; Kranner et al., 2008; Marini et al., 2011). Por el contrario, las especies más fotófilas denominadas epífitos de sol (e.g. Heterodermia, Parmotrema, Usnea), que presentan adaptaciones morfológicas o anatómicas a los ambientes más secos y de mayor intensidad lumínica (presencia de metabolitos secundarios en córtex superior que permiten cierta protección a la irradiación, presencia de cristales de oxalato cálcico que reflejan la luz solar y algas verdes como fotobionte), estuvieron mejor representadas en los bosques secundarios, con un dosel más abierto (Capítulo I y II). A pesar de estos resultados, hay que tener en cuenta que los macrolíquenes representan menos de un tercio de todas las especies de epífitos de los bosques montanos tropicales. Por tanto, estos resultados no pueden generalizarse para toda la comunidad de epífitos no vasculares que son elementos característicos en términos de diversidad, biomasa y funcionamiento de estos ecosistemas. Por tanto, en un segundo estudio evaluamos los efectos de la deforestación sobre los epífitos no vasculares incluyendo macrolíquenes, microlíquenes y briófitos (Capítulo II). Los resultados señalaron un patrón similar a los del capítulo I. Así, la diversidad de epífitos no vasculares (líquenes y briófitos) mostró cambios relacionados con la alteración de los bosques y estuvieron condicionados principalmente por el diámetro de los árboles. Así, la riqueza fue mayor en bosques primarios que en bosques secundarios, y a su vez, éstos albergaron una mayor riqueza que los bosques monospecíficos de Alnus acuminata (Capítulo II). En este sentido, otros estudios ya habían encontrado que la estructura forestal de los bosques primarios, y en concreto el diámetro de los árboles garantizan una gran riqueza de criptógamas en los bosques montanos tropicales (Acebey et al., 2003; Gradstein 2008). En cuanto a la cobertura arbórea, ésta afectó de forma diferente a briófitos y líquenes. Así, la riqueza de briófitos disminuye con la alteración de la cobertura arbolada, que implica cambios ambientales drásticos como disminución de humedad y aumento de la incidencia lumínica. En general, los briófitos (hepáticas foliosas en este caso) dependen estrechamente de la humedad, necesaria para completar su ciclo vital, presentando altas demandas hídricas y con elevada sensibilidad a altos niveles de radiación solar (Sillett & Antoine 2004; Gradstein 2008; Gradstein & Sporn 2010; Pardow & Lakatos 2013). La riqueza de macrolíquenes y microlíquenes también disminuyó considerablemente conforme aumentó la alteración de los bosques, sin embargo, no estuvo ligada a los cambios en la cobertura arbolada. 24

36 La composición de especies en el gradiente de alteración mostró claras diferencias, en relación con el diámetro de los árboles y la cobertura arbórea. Al igual que observamos en el primer capítulo en macrolíquenes, parece que existe un remplazamiento de las especies de sombra por especies de sol, que suelen ser dominantes en bosques secundarios. Así, especies como Herbertus divergens, Coccocarpia filiformis y Coenogonium eximium, fueron exlcusivos para los bosques primarios, mientras Frullania brasiliensis, F. gibbosa, Graphis anfractuosa, G. cinerea y Heterodermia diademata estuvieron restringidos a bosques alterados. Como señala Nöske et al. (2008), la vegetación secundaria puede albergar una alta riqueza de líquenes epífitos, sin embargo la mayor parte de especies corresponden a los epífitos de sol que han reemplazado a los epífitos de sombra pobremente representadas en estos bosques. Además, la riqueza de líquenes se ve muy afecta por la eliminación de árboles de gran porte (talas selectivas), y la pérdida estuvo relacionada con líquenes especialistas de sustratos relacionados con la mayor edad de los árboles (fisuras, grietas, presencia de briófitos y humus) y al tiempo necesario para la colonización (e.g. Fritz et al., 2008; Johansson et al., 2007; Király et al., 2013). Por lo tanto, las comunidades de epífitos no vasculares estuvieron condicionadas por la disminución de potenciales hospedadores (árboles con mayor diámetro) y cambios microclimáticos a causa de la disminución de la cobertura arbolada (Capítulo II). Adicionalmente, algunos estudios han señalado que la composición de las comunidades epífitas es un indicador más sensible de la alteración de los bosques que la riqueza de especies (Nöske et al., 2008, Larrea & Werner 2010). El uso de la diversidad funcional constituye una aproximación complementaria que puede ayudar a comprender los procesos biológicos relacionados con el funcionamiento de los ecosistemas. En los líquenes, su fisiología está relacionada con su morfología y anatomía (caracteres funcionales) y con la respuesta a los cambios ambientales. Así, y con el objetivo de complementar nuestros estudios de diversidad taxonómica, en un tercer capítulo, nos centramos en analizar si la alteración de los bosques tiene efectos sobre la diversidad funcional de líquenes epífitos en los bosques montanos y si esta diversidad puede ser utilizada como indicadora del grado de alteración de los bosques montanos (Capítulo III). En el estudio realizado encontramos que muchos de los rasgos funcionales estudiados se relacionaban con la deforestación en los bosques montanos tropicales, y específicamente con la cobertura del dosel arbóreo y el diámetro de los árboles (Capítulo III). Así, la relación fue directa entre la cobertura arbórea y los cianolíquenes, 25

37 las especies crustáceas con protalo, foliáceas placodioides, filamentosas y gelationosas y aquellas sin metabolitos secundarios. Por el contrario, se encontró una relación inversa entre la cobertura y las especies foliáceas con lóbulos estrechos, especies con lirelas, con soredios y con ácidos como compuesto secundario. En cuanto al diámetro de los árboles la relación fue directa con los clorolíquenes, especies foliáceas con lóbulos anchos, fruticulosas y escuamulosas, con reproducción asexual, con isidios y soredios y especies con ácidos como compuesto secundario. También encontramos que los cianolíquenes, las especies filamentosas y escuamulosas y aquellas sin compuestos secundarios, son indicadoras de bosques primarios, mientras que las especies fruticulosas, foliáceas con lóbulos estrechos y con lirelas son las mejores indicadoras de bosques alterados (en este caso, monoespecíficos) (Capítulo III). Estos rasgos funcionales han sido documentados previamente como adecuados indicadores de cambios en el ambiente (Ellis & Coppins 2006; Stofer et al., 2006; Marini et al., 2011). La escases y ausencia de algunos rasgos funcionales relacionados con la forma de crecimiento (talos crustáceos con protalo, gelatinosos o placodioides) o tipo de alga (presencia de cianobacteria), en bosques secundarios, y especialmente en los monoespecíficos de Alnus acuminata, tiene que ver con los requerimientos hídricos e incluso con las adaptaciones del talo para liberar el exceso de agua. Las especies gelatinosas presentan talos muy finos, muy adaptados a la captación y pérdida de agua en muy poco tiempo, las especies placodioides, liberan agua através de las hifas del córtex inferior, que se estructuran en forma de canales y, las crustáceas con protalo, carecen de córtex superior, y la médula hidrófoba expuesta al medio ambiente repele el exceso de humedad (Pardow et al., 2012). Además, como ya se ha indicado con anteriordad, las especies con cianobacterias presentan unos requerimientos hídricos mayores que las especies que contienen alga verde, ligado a la hidratación del talo para alcanzar los óptimos fotosintéticos. Por esta razón, las especies con estos rasgos funcionales están restringidas a los bosques primarios (Capítulo III). Bajo esta visión algunos estudios han documentado que las especies de líquenes con características similares (e.g. especies con cianobacteria) están restringidos al ambiente forestal de bosques maduros y bien conservados (Belinchón et al., 2007; Kranner et al., 2008; Normann et al., 2010; Aragón et al., 2010; Marini et al., 2011). Por el contrario lo líquenes con talos foliáceos estrechos, con lirelas como estructura de reproducción y con presencia de metabolitos en córtex superior o médula 26

38 (e.g. ácido úsnico, vulpínico o lecanórico) fueron mejor representados en los bosques más alterados (Capítulo III). Estos rasgos funcionales se han identificado como adaptaciones de las especies de líquenes a mayores intensidades de luz (Lücking 1999; Koch et al., 2013). Por ejemplo, especies con atranorina, ácido úsnico, ácido vulpínico o parietina protegen al fotobionte de la excesiva irradiación absorbiendo luz incidente y además actúan como filtros frente a la radiación ultravioleta (Molnár & Farkas 2010). Así, la mayoría de las especies, y especialmente los macrolíquenes que viven en el interior de bosques primarios carecen de la protección que les confiere estos metabolitos secundarios. Adicionalmente, se evidenció que la riqueza de especies con formas de crecimiento gelatinosa, filamentosa y foliácea placodioide pueden ser utilizados para predecir la riqueza total de líquenes epífitos en los bosques montanos tropicales (Capítulo III). Hasta el momento pocos estudios han utilizado la riqueza de las diferentes formas de crecimiento o formas de vida de epífitos no vasculares (líquenes y briófitos) para predecir la riqueza total en ecosistemas con alta diversidad (Oishi 2009; Aragón et al., 2016). Esta aproximación se propone como una herramienta útil y complementaria a la hora de realizar inventarios de biodiversidad y de inferir la riqueza de los ecosistemas y que pueden ser aplicados por personas no especializadas en taxonomía de líquenes y briófitos (Capítulo III). Como comparativa del estudio de los bosques montanos y para detectar patrones generales, nos planteamos el estudio de los efectos de la deforestación sobre los epífitos no vasculares en bosques tropicales estacionalmente secos, que hasta la fecha constituye el primer estudio orientado en esta temática a nivel de país (Capítulo IV). Los bosques tropicales estacionalmente secos presentan una marcada estacionalidad, árboles deciduos y menor diversidad de especies en comparación con los bosques húmedos. A pesar de la baja diversidad de epífitos, pueden albergar altos grados de endemismo y cumplir importantes funciones en estos ecosistemas (Werner 2008). Estas características tan peculiares han generado una interrogante acerca de si los efectos de la deforestación sobre la diversidad de epífitos siguen el mismo patrón que en los bosques húmedos. Hasta la fecha, existe un único estudio sobre el efecto de la deforestación en los bosques secos (Werner & Gradstein 2009). En éste, se encuentra una disminución de la diversidad de epífitos (briófitos) determinada por la cobertura del dosel y el microclima. Sin embargo estos resultados se restringen a bosques monospecíficos de árboles de hoja perenne de Acacia macracantha, que no 27

39 presentan las mismas características estructurales y funcionales de los bosques estacionalmente secos. Los resultados aquí obtenidos señalan que la deforestación tiene efectos negativos en la diversidad de los organismos epífitos en los bosques estacionalmente secos, y que las características del hospedador (i.e. la especie de árbol, su diámetro, y la textura y profundidad de la corteza) junto con la cobertura arbórea constituyen factores limitantes de estas comunidades (Capítulo IV). La pérdida de diversidad forestal de estos bosques implica la disminución de la cobertura arbolada junto con la eliminación de hospedadores potenciales con consecuencias negativas para los epífitos. En otros ecosistemas (i.e. bosques templados y boreales), varios estudios han determinado que la diversidad de árboles constituye un factor limitante para la diversidad de epífitos no vasculares (Nascimbene et al., 2009; Király et al., 2013). En nuestra área de estudio los líquenes crustáceos fueron los elementos dominantes (90% de especies) y solamente se encontró una especie de briófito, debido a que estos últimos están restringidos a zonas con mayor humedad. En el estudio realizado, comprobamos que la mayor parte de las especies (líquenes crustáceos) presentaban especificidad por un pequeño grupo de potenciales hospedadores, como es el caso de Cochlospermum vitifolium y Eriotheca ruizii, caracterizados por un mayor tamaño y corteza más lisa respecto al resto de forófitos (Capítulo IV). En los bosques tropicales no se ha encontrado especificidad del hospedador por parte de las especies epífitas, explicado principalmente por la compleja estructura de estos ecosistemas, producida por la elevada diversidad de especies de árboles que forman diferentes estratos arbóreos y diversos hábitats para el establecimiento de las especies (Cáceres et al., 2007; Rosabal et al., 2013). Sin embargo estos resultados no pueden generalizarse para los bosques estacionalmente secos, ya que presentan una menor diversidad de especies arbóreas y con una marcada estacionalidad. En un trabajo previo, Vergara-Torres et al. (2010), evidenciaron un alto grado especificidad de epífitas vasculares y su hospedador en estos ecosistemas. En el estudio realizado, hemos encontrado que las características del forófito es un factor limitante en los bosques estacionalmente secos para las comunidades de líquenes epífitos en comparación con los bosques húmedos tropicales (Capítulo IV). 28

40 Cabe señalar, que los resultados obtenidos en los capítulos I, II, III y IV han supuesto importantes avances en el conocimiento de la ecología y distribución de las especies de líquenes y briófitos, generando además un incremento considerable de nuevos registros provinciales, nacionales y regionales (Capítulos V y VI). Ecuador se caracteriza por una alta diversidad de líquenes y briófitos, donde se han reportado 950 especies de musgos, 700 especies de hepáticas y antoceros (Churchill 1994; Churchill et al., 2000; León-Yánez et al., 2006) y cerca de 900 especies de líquenes (Cevallos 2012). A pesar de los avances en el área de la briología y liquenología en Ecuador, los estudios siguen siendo limitados y se han enfocado en área específicas; por ejemplo únicamente para las Islas Galápagos se han descrito 633 especies de líquenes y hongos liquenizados (Bungartz et al., 2016) y 253 especies de briófitos (Ziemmeck et al., 2011). Así, si comparamos el número de especies de líquenes entre las Islas Galápagos y Ecuador continental podemos observar que no distan mucho, a pesar de la gran diferencia en superficie y la diversidad de ambientes, lo que nos dá una idea de la falta de conocimiento de este grupo de organismos en Ecuador, uno de los países más diversos del mundo. Como resultado, por tanto, de los trabajos realizados, se han encontrado más de 200 nuevos registros regionales, nacionales y provinciales de briófitos y líquenes para Ecuador (Capítulos V y VI). En lo que respecta a registros para Sur América destacamos a Chapsa diploschistoides (Zahlbr.) Frisch, Fibrillithecis halei (Tuck. & Mont.) Mangold o Pyrenula psoriformis Zahlbr. (Capítulo VI). Dentro de los registros nacionales destacan Mazosia carnea (Eckfeldt) Aptroot & M. Cáceres, Notothylas vitalii Udar & D.K. Singh (Capítulo V) y Syncesia effusa (Fée) Tehler (Figura 3). Además, encontramos también nuevos registros para Ecuador continental como Ramonia valenzueliana (Mont.) Stizenb. y Trypethelium eluteriae Spreng., que previamente habían sido citados en las Islas Galápagos. Hemos detectado también numerosos registros provinciales, como por ejemplo, Diplolabia afzelii (Ach.) A. Massal. Por último, hemos encontrado posibles nuevas especies para la ciencia como algunos miembros de los géneros Fissurina, Graphis y Gyalidea (Figura 4), que más adelante podrán ser descritas. 29

41 A B C D E F Figura 3. Nuevas aportaciones provinciales, para el continente y para Ecuador. (A) Diplolabia afzelii (Ach.) A. Massal.; (B) Ramonia valenzueliana (Mont.) Stizenb.; (C) Trypethelium eluteriae Spreng.; (D) Mazosia carnea (Eckfeldt) Aptroot & M. Cáceres; (E) Notothylas vitalii Udar & D.K. Singh y (D) Syncesia effusa (Fée) Tehler. 30

42 A B C D E F Figura 4. Nuevas aportaciones de líquenes para Sur América y posibles especies nuevas para la ciencia. (A) Chapsa diploschistoides (Zahlbr.) Frisch; (B) Fibrillithecis halei (Tuck. & Mont.) Mangold; (C) Pyrenula psoriformis Zahlbr.; (D) Fissurina sp.; (E) Graphis sp. y (F) Gyalidea sp. 31

43 CONCLUSIONES Los resultados obtenidos en el presente trabajo, muestran diferentes patrones y procesos relacionados con la respuesta de las comunidades epífitas no vasculares (líquenes y briófitos) a la alteración de los bosques tropicales (bosques húmedos montanos y bosques estacionalmente secos), a partir de los cuales se extraen las siguientes conclusiones generales: 1. La riqueza de líquenes y briófitos epífitos se reduce considerablemente conforme aumenta la alteración de los bosques húmedos montanos y bosques tropicales estacionalmente secos. 2. Los cambios en la riqueza y composición de las comunidades de macrolíquenes epífitos en los bosques húmedos montanos, se atribuyeron a la pérdida severa de los epífitos de sombra debido a su intolerancia a la excesiva radiación, derivados de un aumento de la apertura del dosel arbóreo en los bosques secundarios y monospecíficos de Alnus acuminata. 3. La respuesta de líquenes (macrolíquenes y microlíquenes) y briófitos frente a la alteración de los bosques montanos tropicales estuvieron influenciados por variaciones en el tamaño (diámetro) de los árboles, sin embargo los briófitos también estuvieron condicionados por cambios en los factores microclimáticos relacionados con el incremento en la radiación y una disminución de la humedad, provocada por una mayor apertura del dosel. 4. En los boques montanos tropicales, tanto la cobertura arbórea como el diámetro de los árboles tuvieron efectos sobre las especies liquénicas en función de sus rasgos funcionales y sobre la media ponderada de cada rasgo en la comunidad (CWM). 5. Observamos que determinados rasgos funcionales relacionados con el tipo de fotobionte (cianobacterias), formas de crecimiento (gelatinosa, foliácea placodioidea, crustácea con protalo), estructura de reproducción y la presencia de metabolitos secundarios resultaron ser indicadores del estado de conservación de los bosques montanos. 6. Determinadas formas de crecimiento (e.g. gelatinosa, crustácea con protalo, foliácea placodioidea, filamentosa y escuamulosa) estuvieron fuertemente correlacionados con la riqueza total de líquenes en los bosques montanos. Por ello, se proponen como posibles indicadores para realizar inventarios rápidos de biodiversidad en estos ecosistemas, que han sido catalogados como uno de los más amenazados de todo el planeta. 32

44 7. A pesar de que la deforestación en los bosques estacionalmente secos relacionada con la apertura de dosel provocó una disminución en la diversidad de las comunidades epífitas, otros factores relacionados con las características del hospedador (i.e. especie de árbol, diámetro, textura y profundidad de la corteza) son también determinantes de las comunidades epífitas en estos bosques. 8. Los resultados de esta investigación han permitido resaltar la importancia de la conservación de los bosques montanos y bosques secos no alterados como prioritarios para mantener una alta diversidad de líquenes y briófitos, debido a la alta heterogeneidad de hábitats y estructura forestal que proporcionan estos ecosistemas. 9. Por último, mediante este estudio se pone de manifiesto el escaso conocimiento que se tiene de las criptógamas en Ecuador, ya que las ampliaciones de ecología y distribución de las especies de líquenes y briófitos identificadas son numerosas. 33

45 LISTA DE MANUSCRITOS La tesis incluye cinco capítulos en inglés y uno en español, cuyos títulos, lista de coautores y estado de publicación se detalla a continuación. Bosques húmedos montanos tropicales Capítulo I Capítulo II Capítulo III Benítez, Á., Prieto, M., González, Y. & Aragón, G Effects of tropical montane forest disturbance on epiphytic macrolichens. Science of the Total Environment, 441: Benítez, Á., Prieto, M. & Aragón, G Large trees and dense canopies: key factors for maintaining high epiphytic diversity on trunk bases (bryophytes and lichens) in tropical montane forests. Forestry, 88: Benítez, Á., Aragón, G., González, Y. & Prieto, M. Functional traits of epiphytic lichens as indicators of forest disturbance level and predictors of total richness and diversity. En revisión en la revista Ecological Indicators. Bosques Tropicales Estacionalmente Secos Capítulo IV Benítez, Á., Prieto, M., & Aragón, G. Lichen diversity in tropical dry forests is highly influenced by the host tree traits including tree species. Manuscrito inédito Aportaciones a la flora criptogámica de Ecuador Capítulo V Capítulo VI Benitez A., Gradstein S.R., Prieto M., Aragón G., León-Yánez S., Moscoso A. & Burghardt M Additions to the bryophyte flora of Ecuador 2. Adiciones a la Flora de Briófitas del Ecuador 2. Tropical bryology 34: Benítez, Á., Aragón, G., González, Y., & Prieto, M. New records of lichens from Ecuador. En revisión en la revista Polish Botanical Journal. 34

46 AFILIACIÓN DE COAUTORES María Prieto y Gregorio Aragón (Directores de tesis) Área de Biodiversidad y Conservación, Departamento de Biología y Geología, Física y Química Inorgánica, ESCET, Universidad Rey Juan Carlos, Móstoles, E-28933, Móstoles, España. Yadira González (Capítulos I, III y VI) Departamento de Ciencias Naturales, Sección de Ecología y Sistemática, Herbario HUTPL, Universidad Técnica Particular de Loja, San Cayetano s/n, Loja, Ecuador. Robbert Gradstein (Capítulos V) Muséum National d Histoire Naturelle, C.P. 39, 57 rue Cuvier, Paris cedex 05, France. Susana León-Yánez, Alejandra Moscoso y Michael Burghardt (Capítulo V) Escuela de Ciencias Biológicas, Pontificia Universidad Católica del Ecuador, Herbario QCA, Quito, Ecuador. 35

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62 CAPÍTULOS / CHAPTERS 51

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64 CAPÍTULO I / CHAPTER I Effects of tropical montane forest disturbance on epiphytic macrolichens Ángel Benítez a, María Prieto b, Yadira González a, Gregorio Aragón b a Instituto de Ecología, Herbario HUTPL, Universidad Técnica Particular de Loja, San Cayetano s/n, Loja, Ecuador b Área de Biodiversidad y Conservación, ESCET, Universidad Rey Juan Carlos, Móstoles, E-28933, Madrid, Spain Benítez, Á., Prieto, M., González, Y., & Aragón, G. (2012). Science of the Total Environment, 441, Pseudocyphellaria aurata (Ach.) Vain 53

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66 Abstract The high diversity of epiphytes typical of undisturbed montane tropical forests has been negatively affected by continuous deforestation and forest conversion to secondary vegetation. Macrolichens are an important component of these epiphytes. Because their physiology is strongly coupled to humidity and solar radiation, we hypothesized that microclimatic changes derived from forest clearing and logging can affect the diversity of these poikilohydric organisms. In southern Ecuador, we examined three types of forests according to a disturbance gradient (primary forests, secondary forests, and monospecific forests of Alnus acuminata) for the presence/absence and coverage of epiphytic macrolichens that we identified on 240 trees. We found that total richness tended to decrease when the range of the disturbance increased. The impoverishment was particularly drastic for shade-adapted lichens, while the richness of heliophytic lichens increased in the drier conditions of secondary growth. Epiphytic composition also differed significantly among the three types of forests, and the similarity decreased when the range of the disturbance was greater. We concluded that a span of 40 years of recovery by secondary vegetation was not enough to regenerate the diversity of epiphytic macrolichens that was lost due to forest disturbances. Keywords: Ecuador, diversity, epiphytic macrolichens, disturbance, tropical montane forest. 55

67 56

68 1. Introduction Montane tropical rain forests have been recognized as one of the most diverse ecosystems, being simultaneously one of the most threatened habitats in the world (Henderson et al., 1991; Gentry, 1995; Brummit and Nic Lughadha, 2003; Barthlott et al., 2005). Montane rain forests are disappearing at an incredibly high rate and currently cover a tiny fraction of their historical distributions (Henderson et al., 1991; Bruijnzeel and Hamilton, 2000; Wright, 2005; Laurance and Peres, 2006; Gibbs et al., 2010). Many natural forests have been reduced to small isolated remnants by deforestation and subsequent agricultural or livestock activities (Churchill et al., 1995; Asner et al., 2005; Gibbs et al., 2010). This scenario of forest alteration from logging and different land uses has serious consequences for epiphytes (Barthlott et al., 2001; Wolf., 2005; Nöske et al., 2008), which are important components of the diversity within montane rain forests (Barthlott et al., 2001; Nadkarni et al., 2001; Gradstein et al., 2003; Gradstein, 2008) and have important roles in the total biomass, water balance and nutrient cycling of the ecosystems (see Holz and Gradstein, 2005). As a general pattern, epiphyte diversity tends to be higher in primary than in secondary vegetation (Barthlott et al., 2001; Gradstein, 2008). This matter has been recently studied in montane forests, but the results have been rather controversial; some studies supported the higher diversity in primary vegetation (Kapelle et al., 1995; Nöske et al., 2008), while others have found no relationship (Hietz, 1998; Holz and Gradstein, 2005; Nöske et al., 2008). This variation in the patterns observed might be related to differences in the studied taxa, the level of disturbance, the diversity of the host tree species, or the age of the secondary vegetation (Hietz et al., 2006; Gradstein, 2008). In addition to the epiphytic richness, forest disturbance also affects species composition of the epiphytes (Hietz et al., 2006). For instance, epiphytes characteristic of a shaded understory declined in more open vegetation than in primary forests, whilst sun epiphytes were lacking from the shady canopy strata of natural forests (Hietz et al., 2006; Gradstein, 2008). Macrolichens (foliose and fruticose lichen species) are important epiphytic organisms in montane rain forest (Mandl et al., 2010), and the diversity and composition of the communities depend mainly on microclimatic factors associated with forest structure (tree age, canopy cover, management intensity, tree diversity) (Aragón et al., 2010). The physiology of macrolichens is strongly coupled to humidity, solar radiation and temperature conditions (Green et al., 2008), so their distributions at a local level are expected to be determined by changes in forest structure derived from 57

69 natural or human disturbance of the forests (Bergamini et al., 2005; Werth et al., 2005; Nascimbene et al., 2007; Aragón et al., 2010). Within macrolichens, certain groups without cortical pigments (e.g., peltigeralean species) are more sensitive to environmental changes, because they suffer photoinhibition in excessive radiation and are strongly dependent on atmospheric moisture (Lange at al., 2004; Kranner et al., 2008). In this sense, we expect drastic changes in macrolichen composition between the natural rain forest and the more disturbed environment of secondary vegetation. In addition to microclimatic changes caused by the reduction in canopy in disturbed forests, forest logging also causes a loss in diversity of host tree species. This fact may affect the epiphytic diversity and composition because the establishment of a particular species of lichens is determined by several factors related to the host tree species such as bark roughness and ph and tree size (Fritz et al., 2008; Ranius et al., 2008; Belinchón et al., 2009; Aragón et al., 2010). Thus, we expect to find a higher diversity of epiphytic macrolichens in primary forests than in the young secondary vegetation, where the diversity of host tree species is lower and trees are younger. Our main goal was to analyze differences in species richness and diversity of epiphytic macrolichens in relation with forest disturbance in tropical montane forests. The forest disturbance level considered included remnants of natural forests (primary forests), secondary forests that developed after selective logging of primary forest, and secondary vegetation that consisted of a monospecific forest of Alnus acuminata. We hypothesized that the reduction in canopy, the fewer species of host trees and the younger secondary vegetation with respect to primary forests would affect the diversity of the epiphytic macrolichens. Specifically, we addressed the following questions: Do the macrolichen communities suffer an impoverishment when forest disturbance is increased? Which species contribute most to differences among the three forests disturbance levels? 2. Materials and methods 2.1. Study area The study areas included six tropical montane forests located in southern Ecuador (Loja Province; m asl) (Fig. 1). The climate is humid tropical with a mean annual temperature of 20ºC, annual rainfall of ca mm, and relative humidity of ca. 80% (Instituto Nacional de Meteorología e Hidrología, INAMI). 58

70 In this study, we distinguished three types of vegetation according to a disturbance gradient: (1) Relicts of primary forest area (PF) of evergreen montane tropical vegetation. The PFs are characterized by a dense canopy layer (ca % coverage) with large trees (35-40 m tall). The upper canopy is composed of Cinchona macrocalyx Pav. ex DC., Clusia elliptica Kunth, Myrica pubescens Humb. and Bonpl. ex Willd, Podocarpus oleifolius D. Don and Weinmannia pubescens HBK. (2) Secondary forests (SF) that have regrown after selective or total logging events on primary vegetation that took place some 40 years ago (Brown and Lugo, 1990; Holz, 2003). The canopy layer is ca % in coverage, mainly composed of species in the Melastomataceae and Lauraceae, up to m tall. (3) Secondary vegetation dominated by young, monospecific forests (MF) of Alnus acuminata Kunth, a pioneer native species of the Andes. The MFs were characterized by a very uniform structure, absence of understorey, a canopy layer of ca. 50% coverage and trees up to 20 m tall. Fig. 1. Study area in Loja Province of southern Ecuador showing the location of the six tropical montane forest sites: 1 and 2, primary forests (PF); 3 and 4, secondary forests (SF); 5 and 6, monospecific forests of Alnus acuminata (MF). 59

71 2.2. Experimental design Six forests were selected to span the disturbance gradient considered (2 PFs, 2 SFs and 2 MFs) (Fig. 1). Ten plots (5 x 5 m) at different elevations and orientations were selected within each forest, and four trees were sampled within the 10 plots. The distance between plots within a forest was over 50 m. Trees with the greatest and the smallest diameter and two other trees with a diameter at breast height (dbh) that was closest to the mean dbh within the plot were selected for a reliable representation of the epiphytic macrolichens of the stand. Additionally, we measured the elevation (m asl), slope (º), aspect (cosine transformed), and the canopy cover (%) at plot level, and the dbh of all trees (cm) within each plot. These variables are summarized in Appendix B. We determined the species richness and composition of epiphytic macrolichens on 240 trees (40 in each forest). On the basis of our field experience in this type of community, we used 20 x 30 cm grids on the bark of each selected tree as monitoring units (Aragón et al., 2012). Six positions were chosen: three heights (0-50 cm, cm, cm) on the north and on the south aspects to obtain a good representation of the species growing in the different microenvironments of the tree trunks. We calculated the means of two data sets (macrolichen composition and species richness) for a given sample position. The total species richness was defined as the total number of species found in the six sites per tree. For the lichen composition, we calculated the mean estimated cover of each species (% of the site area) for the six sample sites. We calculated the total species cover per tree (as percentage of the grids) using the same methods Data analyses The effects of microclimatic variables (slope, aspect, elevation, canopy cover, dbh) on the epiphytic richness at the tree and plot level was modelled by fitting Generalised Linear Mixed Models (GLMMs) (McCullagh and Nelder, 1989). This modelling approach was chosen because our data had a hierarchical structure with trees nested within plots, plots nested within forests and forests nested within disturbance level. We analyzed the data using a multilevel approach and, when necessary, considered plots and forests as random factors and applied mixed modelling (Verbeke and Molenberghs, 1997). Disturbance level was also initially included in the models, but none of the response variables were significantly related to 60

72 it, so it was removed from the models to be as parsimonious as possible. Predictors were included as explanatory variables (fixed factors), and plot and forest were included as random sources of variation. Effects of random factors were tested using the Wald Z-statistic test. All GLMM computations were performed using SAS Macro program GLIMMIX, which iteratively calls SAS Procedure Mixed until convergence (GLIMMIX ver. 8 for SAS/STAT). To test whether the three levels of disturbance had significantly different compositions of epiphytic species and to detect the effects of forest and plot variability, we performed a three-factor permutational multivariate analysis of variance (PERMANOVA) on the cover data (Anderson et al., 2008). In this analysis, the experimental design included three factors: disturbance level (three levels, fixed factor), forest (two levels, random factor nested within disturbance) and plot (10 levels, random nested within forest), with four replicate trees for each plot. The cover data (percentage cover by each macrolichen per tree) were log 10 (x + 1)-transformed to account for contributions by both rare and abundant taxa. We used the Bray-Curtis distance measure. To assess species similarity among the different disturbance levels, we performed additional pairwise PERMANOVA tests (Anderson et al., 2008). We also computed a non-metric MDS (multidimensional scaling) ordination from the species cover values to reveal the degree of similarity among levels of disturbance. To identify the species that contributed most to the similarity and dissimilarity among the different disturbances levels, we used the SIMPER statistical routine (Clarke and Warwick, 1998). For all tests, we allowed 9999 random permutations under the reduced model. 3. Results 3.1 Species richness We recorded a total of 119 species of epiphytic macrolichens on 240 trees. Results showed that the total number of macrolichens increased when forest disturbance decreased (Fig. 2). A total of 82 species were found in primary forests (PF), 64 species in secondary forests (SF) and 49 species in monospecific forests of Alnus acuminata (MF) (Appendix A). Moreover, species richness of the Peltigerales decreased when forest disturbance was higher (Appendix A). We found 36 exclusive species in PFs, but only 8 and 17 exclusive species in SFs and MFs, respectively (Appendix A). 61

73 Results of the mixed models showed that the most relevant predictors of the epiphytic communities at plot and tree levels were canopy cover and tree diameter (Table 1). The random variable forest was not significant in any case (Table 1). 3.2 Species composition Multivariate statistical analyses showed that epiphytic composition was structured according to the different spatial scales, and a large component of variation was associated with the disturbance level (Table 2). The non-metric MDS ordination showed a clear separation between trees in the different disturbance levels (Fig. 3). The subsequent pairwise test revealed significant differences in epiphytic composition between all three disturbance levels (Table 3). Results of the PERMANOVA test showed that the highest similarity values for species composition within a disturbance level were associated with the highest disturbance: PF (29.35%), SF (35.44%) and MF (41.59%). The SIMPER routine revealed that not all species contribute equally to establish the differences in the disturbance gradient. We observed that the largest contributions are due to differences in species cover of the genus Sticta (S. aff. canariensis, S. tomentosa) (Table 4) PF SF MF Tree Plot Forest Fig. 2. Species richness of epiphytic macrolichens in the three types of vegetation (PF, SF and MF) at tree, plot and forest levels. Values represent means (±SD). 62

74 Table 1. Results of the Generalised Mixed Linear Models on some community traits. Coef.: coefficient of the variable in the model. S.E.: standard error. The random variable forest was non-significant in both cases, while plot variable at tree level was significant (Z-value=2.67, Prob. Z=0.0038). Tree diameter (cm) was at tree level, while elevation (masl), slope (º), aspect (cosine transformed), canopy cover (%) and mean tree diameter (cm) were at plot level. Richness Coef. (S.E.) F-value P-value Tree level Tree diameter 0.061(0.022) Elevation 0.002(0.001) Slope (0.019) Aspect 0.289(0.319) Canopy cover 0.052(0.017) Plot level Mean tree diameter 0.231(0.049) < Elevation 0.003(0.002) Slope (0.021) Aspect (0.371) Canopy cover 0.341(0.0472) < Discussion Our results demonstrated that deforestation in tropical montane rainforests resulted in major loss in the species diversity of epiphytic macrolichens. Secondary forests (SF and MF) had on average 25-45% fewer species than in the neighboring primary forests (PF). Similarly, Gradstein (2008) pointed out that deforestation is a major cause in the loss of all epiphytic species, especially those of the shaded understory of the forest, the so-called "shade epiphytes". In our case, the impoverishment of epiphytic macrolichens in the more disturbed forests was mainly due to the severe loss of the more shade-adapted species (Peltigerales). The most plausible explanation could be related to the efficiency in the physiological activity and the degree of desiccation tolerance in the latter group (Lange et al., 1993; Jovan and McCune, 2004; Kranner et al., 2008). The Peltigerales is composed mainly of lichens without cortical pigments that protect the thallus when is exposed to excessive irradiation, and many of them possess cyanobacteria as the photobiont, which are strongly dependent on the amount of atmospheric moisture (Lange et al., 1993; Jovan and McCune, 2004; Kranner et al., 2008; Marini et al., 2011) because they need liquid water to activate photosynthesis (Lange et al., 1993). Environmental conditions inside primary forests are optimal for the development of shade-adapted lichens because the high canopy cover favours the presence of more 63

75 light-sheltered sites in the understory layer and a permanently moist environment where the air is constantly saturated (Sipman and Harris, 1989; Gradstein, 2008). On the contrary, the open canopy and stronger radiation in disturbed forests (SF and MF) create a drier microclimate than in natural forests (PF) (Gradstein, 2008). The consequent lower humidity negatively affects the shade-adapted lichens. When desiccation stress was induced for some macrolichens species, photosynthesis, respiration, morphology and growth were negatively affected, and the effects were greater for shade species (included in Collema, Lobaria, Peltigera, Sticta) growing in moist habitats (tropical climate) than for species adapted to more exposed areas and drier environments (see Kranner et al., 2008). Table 2. Results of three-factor PERMANOVA analysis of species composition by disturbance gradient, forest and plot. Source df MS Pseudo-F P CV (%) Disturbance Forest (Disturbance) Plot (Forest (Disturbance)) Error However, heliophytic species (with green algae and cortical pigments, mainly included in Lecanorales, Caliciales and Teloschistales) were 13-16% more numerous in more disturbed forests than in the primary forests and were especially abundant in the monospecific forests of Alnus acuminata, representing 85% of the total species. The decrease in shade-adapted lichens vs. the increase in heliophytic lichens in the more disturbed forests provides a negative balance in the total number of the species and therefore an impoverishment of the macrolichen communities linked to the increased forest disturbance. Holz and Gradstein (2005) found a similar pattern in montane forests in Costa Rica, while Nöske et al. (2008) found that the number of epiphytic lichen species increased in secondary forests, suggesting that the number of species along a disturbance gradient does not follow a uniform pattern over time and that community composition might provide a more sensitive indicator of the human impact than species richness. In addition to the changes in microclimate caused by the more or less open canopy, the impoverishment of epiphytic macrolichens in more disturbed forests might be explained by several factors related to differences in forest structure among the three types of vegetation considered (Fritz et al., 2008; Aragón et al., 2010; Soto- 64

76 Medina et al., 2011). First, the larger tree size in primary forests involves more bark surface, formation of age-related specialized substrates and longer periods for colonization (Fritz et al., 2008; Ranius et al., 2008; Johansson et al., 2009). Second, since the establishment of lichens is linked to bark roughness and ph (e.g., Coppins and Wolseley, 2002; Rosabal et al., 2010), the species richness will decrease in secondary forests where trees have rather smooth bark and are more architecturally uniform than in primary forests (Gradstein, 2008). However, this trend might be mitigated by the high species diversity in the tropics, by the great water availability or by the interactions between other epiphytic organisms (angiosperms, mosses and ferns) (Cáceres et al., 2007; Soto-Medina et al., 2011). Third, the presence of a dense bryophyte cover provides a suitable substrate for the establishment of the biggest and the most shade macrolichens (several species of Lobaria and Sticta) (Kranner et al., 2008; Belinchón et al., 2009). Table 3. Results of pairwise PERMANOVA test between types of vegetation according to disturbance gradient to show dissimilarity (%, according to Bray-Curtis index) and level of significance. Source Dissimilarity (%) P PF vs SF PF vs MF SF vs MF Notes: PF: primary forests; SF: secondary forests; MF: monospecific forests of Alnus acuminata. Table 4. Results of the SIMPER analyses CA CA CA Species PF SF CD PF MF CD SF MF CD Bulbothrix coronata Coccocarpia palmicola Heterodermia aff. diademata Heterodermia aff. galactophylla Heterodermia galactophylla Heterodermia isidiophora Heterodermia japonica Heterodermia leucomela Heterodermia spathulifera Hypotrachyna revoluta Hypotrachyna rocky Leptogium azureum Leptogium cochleatum Lobaria subdissecta Parmeliella ecuadorense

77 Parmotrema aff. exquisitum Parmotrema aff. peralbidum Parmotrema arnodii Parmotrema rampoddense Parmotrema zollongeri Pseudocyphellaria aurata Punctelia aff. crispa Punctelia aff. reddenda Sticta aff. canariensis Sticta andensis Sticta ferax Sticta humboltii Sticta laciniata Sticta tomentosa Sticta sp Sticta sp Usnea sp Notes: CA: mean cover (%); CD: Contribution of each species to the dissimilarity (%). Differences among management types are also corroborated by results on species composition. However, a large part of the variability in species composition is associated with forest, plot and trees, indicating that local factors contribute to shape lichen communities, independently by management regime. The differences between primary forests and the rest of the disturbed forests (SF and MP) were mainly attributed to the coverage of more shaded-adapted species (e.g., Sticta spp.). These species drastically reduced their presence and coverage with disturbance level. Similarly, Rivas Plata et al. (2008) showed that some genera of microlichens had preferences for undisturbed primary forests, fully shaded microhabitat and bark of mature trees. However, in the absence of shade lichens in drier habitats, the increased coverage by the more heliophytic lichens (e.g., Heterodermia spp., Hypotrachyna spp.) will be responsible for the dissimilarity. The differences in species composition between the primary and secondary forests (SF and MF), which were not managed during the last 40 years since the last selective or total logging, might indicate that the epiphyte macrolichens had regenerated. Similarly, Gradstein (2008) found that the epiphytic composition in the natural forest was very different than in forests that had 50 years to recover, citing differences in the main variables that determine the response of the epiphytic organisms to habitat disturbance as possible causes: host tree characteristics, openness of the canopy and the microclimate in the forests (Gradstein, 2008; Nöske et al., 2008). In the same way, Holz and Gradstein (2005) suggested that at least 100 years are needed for the complete recovery of the floristic and community composition. 66

78 We therefore concluded that tropical forest disturbance significantly and drastically reduces macrolichen diversity. Disruption of the canopy leads to microclimatic changes that affect species richness of epiphytic macrolichens. Species loss is most severe for the shade-adapted lichens (included in Peltigerales) because in the disturbed habitats these epiphytes were not able to tolerate the high irradiation; therefore, these species may be useful indicators of forest conservation. In addition, change in the tree species composition and host tree characteristics play an important role. Actually, in this study there was evidence that in secondary forests lichen diversity of native forests was not regenerated; consequently, only the protection of remnants of primary tropical forest might help to preserve a rich and diverse community of epiphytic macrolichens. Acknowledgments Financial support for this study was received by the University Técnica Particular de Loja, Secretaria Nacional de Educación Superior, Ciencia, Tecnología e Innovación of Ecuador and the Ministerio de Ciencia e Innovación (proyect EPICON, CGL ) of Spain. We thank G. Cevallos for fieldwork help and C. Aguirre and A. Gonzaga, who kindly provided access to the study areas. References Anderson MJ, Gorley RN, Clarke KR. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. Plymouth, UK:PRIMER-E;2008. Aragón G, Martínez I, García A. loss of epiphytic diversity along a latitudinal gradient in southern Europe. Sci Total Environ 2012;426: Aragón G, Martínez I, Izquierdo P, Belinchón R, Escudero A. Effects of forestmanagement on epiphytic lichen diversity in Mediterranean forests. Appl Veg Sci 2010;13: Asner GP, Knapp D, Broadbent E, Oliveira P, Keller M, Silva J. Selective logging in the Brazilian Amazon. Science 2005;310: Barthlott W, Schmitt-Neuerburg V, Nieder J, Engwald S. Diversity and abundance of vascular epiphytes: a comparison of secondary vegetation and primary montane rain forest in the Venezuelan Andes. Plant Ecol 2001;152: Barthlott W, Mutke J, Rafiqpoor MD, Kier G, Kreft H. Global centres of vascular plant diversity. Nova Act Lc 2005;342:

79 Belinchón R, Martínez I, Otálora MAG, Aragón G, Dimas J, Escudero A. Fragment quality and matrix affect epiphytic performance in a Mediterranean forest landscape. Am J Bot 2009;96: Bergamini A, Scheidegger C, Stofer S, Carvalho P, Davey S, Dietrich M, et al. Performance of macrolichens and lichen genera as indicators of lichen species richness and composition. Conserv Biol 2005;19: Brown S, Lugo AE. Tropical secondary forests. J Trop Ecol 1990;6:1 32. Bruijnzeel LA, Hamilton LS. Decision time for cloud forests. IHP Humid Tropical Programme Series 2000;13:1 40. Brummit N, Nic Lughadha E. Biodiversity. Where s hot and where s not. Conserv Biol 2003;17: Cáceres MS, Lücking R, Rambold G. Phorophyte specificity and environmental parameters versus stochasticity as determinants for species composition of corticolous crustose lichen communities in the Atlantic rain forest of northeastern Brazil. Mycol Prog 2007;10: Churchill SP, Balslev H, Forero E, Luteyn JL. Biodiversity and Conservation of Neotropical Montane Forests. New York: New York Botanical Garden; Clarke KR, Warwick RM. Quantifying structural redundancy in ecological communities. Oecologia 1998;113: Coppins BJ, Wolseley P. Lichens of tropical forests. In: Watling R, Frankland JC, Ainsworth AM, Isaac S, Robinson CH, editors. Tropical Mycology: Micromycetes. Wallingford: CABI Publishing; p Fritz Ö, Niklasson M, Churski M. Tree age is a factor for the conservation of epiphytic lichens and bryophytes beech forest. Appl Veg Sci 2008;12: Gentry AH. Patterns of diversity and floristic composition in neotropical montane forests. In: Churchill SP, Balslev H, Forero E, Luteyn J L, editors. Biodiversity and conservation of neotropical montane forests. New York: New York Botanical Garden Bronx; p Gibbs HK, Reusch AS, Achard F, Clayton MK, Holmgren P, Ramankutty N, Foley JA. Tropical forests were the primary sources of new agricultural lands in the 1980s and 1990s. Proc Nat Acad Sci 2010;107: Gradstein SR, Nadkarni NM, Krömer T, Holz I, Nöske N. A protocol for rapid and representative sampling of epiphyte diversity of tropical rain forests. Selbyana 2003;24: Gradstein SR. Epiphytes of tropical montane forests impact of deforestation and climate change. In: Gradstein SR, Homeier J, Gansert, D, editors. The tropical 68

80 mountain forest. Patterns and Processes in a Biodiversity Hotspot. Göttingen: University Press; p Green TGA, Nash III TH, Lange OL. Physiological ecology of carbon dioxide exchange, In: Nash III, TH, editor. Lichen Biology. Cambridge: Cambridge University Press UK; p Henderson A, Churchill SP, Luteyn JL. Neotropical plant diversity. Nature 1991;351: Hietz P. Diversity and conservation of epiphytes in a changing environment. Pure Appl Chem 1998;70: Hietz P, Buchberger G, Winkler M. Effect of forest disturbance on abundance and distribution of epiphytic bromeliads and orchids. Ecotropica 2006;12: Holz I. Diversity and Ecology of Bryophytes and Macrolichens in Primary and Secondary Montane Quercus Forests, Cordillera de Talamanca, Costa Rica. Dissertation. Universität Göttingen; Holz I, Gradstein SR. Cryptogamic epiphytes in primary and recovering upper montane oak forests of Costa Rica, species richness, community composition and ecology. Plant Ecol 2005;178: Johansson V, Bergman KO, Lättman H, Milberg P. Tree and site quality preferences of six epiphytic lichens growing on oaks in southeastern Sweden. Ann Bot Fenn 2009;46: Jovan S, McCune B. Regional variation in epiphytic macrolichen communities in northern and central California forest. Bryologist 2004;104: Kappelle M, Kennis PAF, Vries RAJ. Changes in diversity along a successional gradient in a Costa Rica upper montane Quercus forest. J Trop Ecol 1995;12: Kranner I, Beckett R, Hochman A, Nash TH III. Desiccation-Tolerance in Lichens: A Review. Bryologist 2008;111: Lange O, Büdel A, Meyer A, Kilian E. Further evidence that activation of net photosynthesis by dry cyanobacterial lichens requires liquid water. Lichenologist 1993;25: Lange OL, Burkhard B, Meyer A, Zellner H, Zotz G. Lichen carbon gain under tropical conditions: water realtions and CO 2 exchange of Lobariaceae species of a lower montane rainforest in Panama. Lichenologist 2004;36: Laurance WF, Peres CA. Emerging Threats to Tropical Forests. Chicago: Chicago University Press;

81 Mandl N, Lehnert M, Kessler M, Gradstein SR. A comparison of alpha and beta diversity patterns of ferns, bryophytes and macrolichens in tropical montane forests of southern Ecuador. Biodivers Conserv 2010;19: Marini L, Nascimbene J, Nimis PL. Large-scale patterns of species richness of epiphytic lichens: exploring the role of human, climate, and forest structure. Sci Total Environ 2011;409: Nadkarni NM, Merwin MC, Nieder J. Forest canopies: plant diversity. In: Levin S, editor. Encyclopedia of Biodiversity. San Diego California USA: Academic Press; p Nascimbene J, Marini L, Nimis PL. Influence of forest management on epiphytic lichens in a temperate beech forest of northern Italy. Forest Ecol Manag 2007;247:43 7. Nöske N, Hilt N, Werner FA, Brehm G, Fiedler K, Sipman HJ, Gradstein SR. Disturbance effects on diversity of epiphytes and moths in a montane forest of Ecuador. Basic Appl Ecol 2008;9:4 12. Ranius T, Johansson P, Berg N, Niklasson M. The influence of tree age and microhabitat quality on the occurrence of crustose lichens associated with old oaks. J Veg Sci 2008;19: Rivas Plata E, Lücking R, Lumbsch HT. When family matters: na analysis of Thelotremataceae (Lichenized Ascomycota: Ostropales) a bioindicators of ecological continuity in tropical forests. Biovivers Conserv 2008;17: Rosabal D, Burgaz AR, De la Masa R. Diversity and distribution of epiphytic macroliches on tree trunks in two slopes of the montane rainforest of Gran Piedra, Santiago de Cuba. Bryologist 2010;113: Sipman HJM, Harris RC. Lichens. In: Lieth H, Werger MJA, editors. Tropical Rain Forest Ecosystems. Amsterdam: Elsevier; p Soto-Medina E, Lücking R, Bolaños-Rojas A. Especificidad de forófito y preferencias microambientales de los líquenes cortícolas en cinco especies de forófitos en el bosque premontano de la finca Zíngara (Cali, Colombia). Rev Biol Trop 2011;59(4). Verbeke G, Molenberghs G. Linear mixed models in practice. A SAS-oriented approach. Springer, New York; Werth S, Tømmervik H, Elvebakk A. Epiphytic macrolichen communities along regional gradients in northern Norway. J Veg Sci 2005;16: Wolf JHD. The response of epiphytes to anthropogenic disturbance of pine oak forests in the highlands of Chiapas, Mexico. Forest Ecol Manag 2005;212:

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83 Appendix A Number of trees on which each species appears in three types of vegetation according to a disturbance gradient. PF: primary forests, SF: secondary forests, MF: monospecific forests of Alnus acuminate Taxa PF SF MF Lecanorales Alectoria ochroleuca (Hoffm.) A. Massal. 9* Anzia parasitica (Fée) Zahlbr. 4* Bryoria sp. 1* Bulbothrix apophysata (Hale & Kurok.) Hale 6* Bulbothrix coronata (Fée) Hale 45* Bulbothrix isidiza (Nyl.) Hale 16* Bulbothrix suffixa (Stirton) Hale 14* Canomaculina cristobalii (L.I.Ferraro & Elix) Elix 3 14 Canomaculina pilosa (Stizenb.) Elix & Hale 1 1 Cladonia coniocraea (Flörke) Sprengel 7 13 Cladonia subradiata (Vainio) S&st Everniastrum cirrhatum (Fr.) Hale ex Sipman 7 2 Everniastrum vexans (Zahlbr. ex W.L. Culb. & C.F.Culb.) Hale ex Sipman Flavopunctelia flaventior (Stirt.) Hale 3* Hypotrachyna aff. degelii (Hale) Hale 16 1 Hypotrachyna bogotensis (Vain.) Hale 4* Hypotrachyna costaricensis (Nyl.) Hale Hypotrachyna densirhizinata (Kurok.) Hale 6* Hypotrachyna eitenii (Hale) Hale 8* Hypotrachyna rachista (Hale) Hale 4* Hypotrachyna revoluta (Flörke) Hale Hypotrachyna reducens (Nyl.) Hale 9* Hypotrachyna rockii (Zahlbr.) Hale Hypotrachyna sp. 28* Parmelinopsis miniarum (Vain.) Elix & Hale 5* Parmotrema aff. exquisitum (Kurok.) DePriest & B.W.Hale 8 31 Parmotrema aff. peralbidum (Hale) Hale Parmotrema arnoldii (Du Rietz) Hale Parmotrema austrosinense (Zahlbr.) Hale 9* Parmotrema cristiferum (Taylor) Hale 17* Parmotrema exquisitum (Kurok.) DePriest & B.W.Hale 12* Parmotrema internexum (Nyl.) Hale ex DePriest & B.W. Hale. 9 9 Parmotrema mellisii (Dodge) Hale. 8* Parmotrema rampoddense (Nyl.) Hale Parmotrema zollingeri (Hepp) Hale Punctelia aff. crispa Marcelli, Jungbluth & Elix Punctelia aff. reddenda (Stirt.) Krog Ramalina celastri (Spreng.) Krog & Swinscow 26* Ramalina cochlearis Zahlbr

84 Ramalina peruviana Ach. 2* Ramalina sp Relicina abstrusa (Vainio) Hale. 7* Rimelia subisidiosa (Müll. ARg.) Hale & A. Fletcher 2* Rimelia succinreticulata Eliasaro & Adler 5* Usnea sp Usnea sp Usnea sp. 3 3* Usnea sp Peltigerales Coccocapia dissecta Swinscow & Krog 4* Coccocarpia erythroxyli (Spreng.) Swinscow & Krog 6 6 Coccocarpia filiformis Arv. 4* Coccocarpia guimarana (Vain.) Swinscow & Krog 2* Coccocarpia microphyllina Lücking & Aptroot 7* Coccocarpia palmicola (Spreng.) Arv. & D.J. Galloway 8 39 Coccocarpia pellita (Ach.) Müll. Arg. 12* Coccocarpia prostrata Lücking, Aptroot & Sipman 7 5 Coccocarpia sp. 22* Coccocarpia stellata Tuck Leioderma glabrum D. J. Galloway & P. M. Jørg. 13* Leptogium austroamericanum (Malme) C. W. Dodge 6 4 Leptogium azureum (Sw.) Mont Leptogium burgesii (L.) Mont Leptogium burnetii Dodge 6* Leptogium chloromelum (Ach.) Nyl. 2 5 Leptogium cochleatum (Dicks.) P.M. Jørg. & P. James Leptogium coralloideum (Meyen & Flot.) Vain Leptogium corticola (Taylor) Tuck. 9 7 Leptogium cyanescens (Rabh.) Körb. 13* Leptogium diaphanum (Sw.) Nyl. 3* Leptogium laceroides B. de Lesd. 5 2 Leptogium marginellum (Sw.) Gray 4* Leptogium millegranum Sierk 6* Leptogium olivaceum (Hook.) Zahlbr. 8* Leptogium phyllocarpum (Pers.) Mont Lobaria dissecta (Sw.) Raeusch. 8* Lobaria erosa (Eschw.) Nyl. 3 4 Lobaria subdissecta (Nyl.) Vain Lobaria tenuis Vain. 1* Lobariella crenulata (Hook. in Kunth) Yoshim Lobariella exornata (Zahlbr.) Yoshim. 3* Lobariella pallida (Hook.) Yoshim. 6 7 Pannaria conoplea (Ach.) Bory 9 24 Pannaria mosenii C.W. Dodge 6* Pannaria prolificans Vain. 1* Parmeliella andina P. M. Jorg. & Sipman 22* Parmeliella delicata P. M. Jørg. & Arv. 23* Parmeliella miradorensis Vain. 13* Parmeliella sp Peltigera sp. 1* 73

85 Pseudocyphellaria aurata (Ach.) Vain Pseudocyphellaria crocata (L.) Vain. 1 3 Sticta aff. canariensis (Ach.) Bory ex Delise Sticta andensis (Nyl.) Trevis Sticta ferax Müll. Arg. 5 7 Sticta fuliginosa (Dicks.) Ach. 7* Sticta humboltii Hook. f. 11* Sticta laciniata (Sw.) Ach. 12* Sticta tomentosa (Sw.) Ach Sticta sp.1 9* Sticta sp.2 13* Caliciales Heterodermia aff. diademata (Taylor) D.D. Awasthi 54* Heterodermia aff. galactophylla (Tuck.) W.L. Culb Heterodermia comosa (Eschw.) Follmann & Redón 1* Heterodermia corallophora (Taylor) Skorepa 9 11 Heterodermia galactophylla (Tuck.) W.L. Culb Heterodermia hypochraea (Vain.) Swinscow & Krog 9* Heterodermia hypoleuca (Mühl.) Trevis Heterodermia isidiophora (Nyl.) D.D. Awasthi Heterodermia japonica (M. Satô) Swinscow & Krog Heterodermia leucomela (L.) Poelt Heterodermia microphylla (Kurok.) Swins. & Krog 1* Heterodermia palpebrata (Taylor) Trass 2* Heterodermia sitchensis Goward & Noble 7* Heterodermia spathulifera Moberg & Purvis Heterodermia subcitrina Moberg 3* Heterodermia sp. 2 8* Phaeophyscia aff. limbata (Poelt) Kashiw. 12* Teloschistales Teloschistes flavicans (Sw.) Norman 41* 74

86 CAPÍTULO II / CHAPTER II Large trees and dense canopies: key factorsformaintaininghigh epiphytic diversity on trunk bases (bryophytes and lichens) in tropical montane forests Ángel Benítez 1, María Prieto 2 and Gregorio Aragón 2 1 Sección de Sistemáticay Diversidad, Departamento de Ciencias Naturales, Universidad Técnica Particularde Loja, San Cayetano s/n, Loja, Ecuador 2 Área de Biodiversidad y Conservación, ESCET, Universidad Rey Juan Carlos, Móstoles, E-28933, Madrid, España. Benítez, Á., Prieto, M., & Aragón, G. (2015). Forestry, 88, Normandina pulchella (Borrer) Nyl. Radula javanica Gottsche 75

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88 Abstract The high richness of epiphytes in moist tropical montane forests is continuously decreasing due to deforestation and habitat loss. Lichens and bryophytes are important components of epiphyte diversity on trunk bases and play an important role in the water balance and nutrient cycling of tropical montane forests. As lichens and bryophytes are very sensitive to microclimatic changes, we hypothesized that their species richness and composition would change with forest alteration. We also expected their response patterns to be different given the capability of lichens to photosynthetize using water vapour. In this study, we assessed the richness and composition of epiphytes (lichens and bryophytes) on the trunk bases of 240 trees in primary and secondary forests of southern Ecuador. We found that diversity was higher in primary forests and lower in monospecific secondary forest stands. Total diversity was negatively affected by habitat loss and by the reduction of canopy cover for bryophytes. Shade epiphytes were replaced by sun epiphytes in open secondary forests. We conclude that lichen and bryophyte diversity of tropical montane forests are negatively affected by the removal of large trees and canopy disruption. The different species compositions of primary and secondary forests and the high number of species exclusive to primary forests indicate that secondary forests are of limited importance in compensating for the loss of non-vascular epiphyte species associated with primary forests. Keywords: non-vascular epiphytic communities, lichens, bryophytes, logging, secondary forests, tropical montane forest, Ecuador 77

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90 Introduction Neotropical montane rain forests are considered "hot spots" of global biodiversity and are a high conservation priority (Gentry, 1995; Myers et al., 2000; Dirzo and Raven, 2003). Epiphytes constitute an important floristic, structural and functional component in these forests (Barthlott et al., 2001; Gradstein, 2008; Köster et al., 2009); however, this exceptional diversity is threatened by continued deforestation and habitat loss (Churchill et al., 1995; Bruijnzeel and Hamilton, 2000; Gibbs et al., 2010). Forest conversion produces changes which directly influence epiphyte diversity: abiotic conditions are altered, habitat complexity (i.e. tree size, tree species and canopy structure) is reduced, and dispersal is constrained (Werner et al., 2005, 2011; Hietz et al., 2006). In fact, several authors have found a loss of epiphytic diversity (including vascular plants, bryophytes and lichens) in secondary forests and a higher diversity in primary forests (Barthlott et al., 2001; Acebey et al., 2003; Krömer and Gradstein 2003; Wolf, 2005; Gradstein 2008; Gradstein and Sporn, 2010). Non-vascular epiphytes (i.e. bryophytes and lichens) constitute an important fraction of epiphytic organisms in tropical montane forests in terms of diversity, biomass and nutrient cycling (Pócs, 1982; Sipman, 1995; Holz and Gradstein, 2005; Mandl et al., 2010; Gehrig-Downie et al., 2011). Due to their poikilohydric nature, these organisms are tolerant to desiccation (Pardow and Lakatos, 2013), even though their degree of desiccation tolerance varies greatly among species (Proctor et al., 2007; Kranner et al., 2008). In particular, lichens and bryophytes in humid sites in tropical forests, mainly the forest understory and inner parts of the canopy, are highly sensitive to desiccation (Kranner et al., 2008; Pardow and Lakatos, 2013) and may experience photoinhibition when exposed to a small rise in solar radiation (Sillett and Antoine, 2004; Green et al., 2008; Pardow and Lakatos, 2013). As the physiology of these organisms is strongly linked to ambient moisture, solar radiation and temperature (Gignac, 2001; Sillett and Antoine, 2004; Green et al., 2008), forest logging and land use may greatly affect the diversity of non-vascular epiphytic communities. The canopy disruption caused by forest logging can affect the humidity, temperature, and light conditions inside forests, making them unsuitable sites for shade-adapted species (Gradstein, 2008; Gradstein and Sporn, 2010; Norman et al., 2010; Benítez et al., 2012). Open forests are generally drier, warmer and windier compared to closed forests, where moisture content is higher and less variable (Gradstein, 2008). However, these microclimate changes do not necessarily involve a 79

91 decrease in species richness, but rather a replacement in community composition (Holz and Gradstein, 2005; Nöske et al., 2008). The more shade-adapted lichens and bryophytes that are intolerant to desiccation are often replaced by heliophytic species (Ariyanti et al., 2008; Gradstein, 2008; Gradstein and Sporn, 2010; Benítez et al., 2012). Forest logging may also have immediate negative effects on the persistence of bryophytes and lichens due to the removal of host tree species (Gradstein, 2008). Host tree characteristics, especially tree size, play an important role in lichen and bryophyte colonization (Benítez et al., 2012; Rosabal et al., 2013), probably due to greater bark surface available for colonization on large trees and the creation of additional microhabitats (Fritz et al., 2008; Ranius et al., 2008). Epiphytic diversity may also be influenced by bark roughness, humus and moss cover on the bark surface, stochastic effects of species dispersion, and to lesser extent, bark ph (Sipman and Harris, 1989; Cáceres et al., 2007; Gradstein and Culmsee, 2010; Soto et al., 2012). As a result of human activities in Ecuador, primary forests have often been replaced by secondary vegetation, creating forests with a less developed canopy structure, smaller trees, and less tree diversity. Benítez et al. (2012) found that the diversity of shade epiphytes decreased drastically as a result of such forest disturbance. This could be due to the high percentage of the macrolichen species belonging to the order Peltigerales (ca. 50%), as these species are adapted to within forest conditions, have high water demands and are sensitive to high solar radiation. However, as macrolichens represent less than one-third of all poikilohydric epiphytic species in tropical montane forests, these results should be interpreted with caution when considering epiphytic communities as a whole (bryophytes and lichens). Knowledge of the differences in epiphytic diversity in primary and secondary forests is crucial to evaluate the conservation status of these forests and to design conservation strategies. The goal of this study was to explore the response of the non-vascular epiphytic community to forest logging in tropical montane rain forests. We hypothesized that differences in species diversity and community composition would be related to differences in forest structure and microclimate caused by the intensity of forest logging. Another objective was to compare the response patterns between bryophytes and lichens, as lichens prefer relatively high light levels (excluding some cyanolichens) 80

92 (Sillett and Antoine, 2004; Green et al., 2008; Normann et al., 2010) and are generally less negatively affected by drought than bryophytes (Perhans et al., 2009). Materials and methods Study area This study was carried out at two sites in southern Ecuador and included six remnants of tropical montane forests along a disturbance gradient (Table 1). The climate is humid tropical with a mean annual temperature of 20 C, an annual rainfall of approximately 1900 mm and a relative humidity of approximately 80% (National Institute of Meteorology and Hydrology, INAMI). The altitude of the studied plots ranged from 2200 to 2800 m a.s.l. Field work was carried out in three types of forest vegetation varying in age, species composition and tree cover: (1) Remnant primary forest fragments (PF) of evergreen tropical montane forests characterized by a dense canopy layer (ca % cover) and large trees (35-40 m tall). The main canopy trees were Cinchona macrocalyx Pav. ex DC., Clusia elliptica Kunth, Myrica pubescens Humb. & Bonpl. ex Willd., Podocarpus oleifolius D. Don ex Lamb. and Weinmannia pubescens Kunth. (2) Secondary mixed forest fragments (SF) regrown after selective logging events which took place ca. 40 years earlier (Brown and Lugo, 1990; Holz, 2003). Canopy cover was ca %, and the main canopy trees were Melastomataceae and Lauraceae species (25-30 m tall). (3) Secondary monospecific forests of Alnus acuminata Kunth (MF; y old) regrown by natural regeneration after forest clearing (Hofstede and Aguirre, 1999). This tree is a pioneer and native species of the Andes. Monospecific forests are characterized by their uniform structure, absence of understory plants, approximately 50% canopy cover and trees up to 20 m tall. Logging and firewood extraction were the main contemporary human activities in MF, while there were no human activities in PF and SF. Species identification For species identification we used more than 200 taxonomic and floristic papers (e.g. Gradstein et al., 2001; Gradstein and Costa, 2003; Frisch et al., 2006; Cáceres, 2007; Aptroot et al., 2008; Timdal, 2008; Lücking, 2009; Moncada et al., 2013). For 81

93 species nomenclature we followed mainly Tropicos.org for bryophytes and MycoBank for lichens. Experimental design We sampled two stands of each forest type (PF, SF and MF). We established ten 5 5 m plots in each stand for a total of 60 plots. The distance between the plots in each forest stand was >50 m. In each plot, epiphytic lichens and bryophytes were sampled on the bases of 4 mature trees (240 trees total) using cm grids. Samples were taken on each tree at three different heights (0 50, , cm) on the northern and southern exposure for a total of six samples per tree. Species richness was defined as the total number of species found in each plot. For epiphytic composition, we estimated the mean cover of each species (% of grid area) per tree and per plot (as the percentage of four trees). We also measured the following variables at the plot level: canopy cover (%), elevation (m a.s.l.), slope (º), aspect (cosine transformed) and mean tree DBH (cm) of the 4 trees analyzed per plot as a proxy for stand structure. Table 1 Means of the environmental variables in the studied primary and secondary montane forests (2 stands of each forest type) in Ecuador. PF, primary forest; SF, mixed secondary forest; MF, monospecific secondary forest of Alnus acuminata. Fores t PF1 PF2 SF1 SF2 MF1 MF2 Location S, W S, W S, W S, W S, W S, W Canopy cover (%) Tree diameter (cm) Elevation (masl) Slope (º) Aspect E-SW SW-N NW-NE E-SW E-SW NE-SW 82

94 Data analyses Richness and diversity We determined the effect of the environmental variables (canopy cover, mean DBH, elevation, aspect and slope) on the following community traits: total species richness, lichen richness, bryophyte richness and species diversity (Simpson inverse and Shannon indices). The Simpson and Shannon indices allow data on species richness and relative abundance to be combined (Gorelick, 2006). The Simpson index was determined by the predominant species, and the Shannon index was based on the assumption that individuals were randomly selected and that all species were represented in the sample (Magurran, 2004). Although host trees have a great influence on epiphyte diversity in temperate regions, the effect of host tree was not explored, as host-specificity does not seem to play an important role in tropical forests with a relatively high diversity of tree species (Sipman & Harris, 1989; Cáceres et al., 2007; Rosabal et al., 2013). The effects of slope, aspect, elevation, canopy cover and mean tree diameter on species richness, the Shannon index and Simpson inverse index were analyzed at the plot level using generalized linear mixed models (GLMMs) (McCullagh and Nelder, 1989; Verbeke and Molenberghs, 1997). Because forest stands were quite far apart (Benítez et al., 2012), stand distance was initially included in the models, but it was later removed as no significant differences were detected. Predictors were included as explanatory variables (fixed factors), and forest and plot were included as random sources of variation. Effects of random factors were tested using the Wald Z-statistic test. We fitted the mixed models using a normal distribution with an identity link function. All GLMM computations were performed using SAS (GLIMMIX ver. 8 for SAS/STAT). We measured total species richness, lichen richness and bryophyte richness at the forest level, as the total species identified on 40 trees in each forest. Sampling completeness at the forest level was estimated with Chao2 species richness estimator, using EstimateS (Colwell, 2013). Species composition and community structure Non-metric multidimensional scaling (NMDS) ordination was performed to detect the main factors influencing epiphytic composition. NMDS analyses were carried out using CRAN software R (R Core Team 2013) with vegan package (Oksanen et al., 83

95 2013). For the NMDS analyses, the Bray-Curtis distance was used, as it is one of the most effective measures for community data (McCune et al., 2002). The coefficients of determination (r 2 ) for the predictor variables were calculated with ordination axes to interpret the relationships between the variables and community composition (1000 permutations). Bray-Curtis dissimilarity between plots within a forest was calculated as a measure of species replacement. A pairwise PERMANOVA test using Bray-Curtis distance was also performed to assess species similarity among the three types of forest vegetation. Statistical analysis was performed using version of PRIMER multivariate statistical analysis software (Anderson et al., 2008), allowing 9999 random permutations under the reduced model. Results Richness and diversity A total of 374 epiphytic species (307 lichens, 67 bryophytes) were collected in the 60 plots (Supplementary data). The highest number of species was observed in primary forests (PF) with 234 species, followed by secondary mixed forests (SF) with 191 species and monospecific secondary forests with 134 species (Figure 1; Table 2). Figure 1 Species richness of epiphytic lichens and bryophytes in primary and secondary montane forests in Ecuador. PF, primary forest; SF, Mixed secondary forest; MF, monospecific secondary forest of Alnus acuminata. Axis X, epiphytic species richness; Axis Y, forest types. A similar pattern was observed for the richness estimator (Chao 2), confirming the occurrence of the highest species richness in PF (Table 2). Fifty-four species were exclusive to PF, exceeding the number of species exclusive to SF (Supplementary 84

96 data). Species replacement (as a measure of dissimilarity) was also higher in PF for both lichens and bryophytes (Table 2). Analysis of environmental variables showed that tree diameter was the most relevant predictor of species richness at the plot level (Table 3). Canopy cover had a significant effect on bryophyte richness. The random variable forest was non-significant in all cases. Table 2 Species richness and dissimilarity of bryophytes and lichens at the forest level. Chao2 estimates of total richness are shown in brackets. SE: standard error. PF, primary forest; SF, Mixed secondary forest; MF, monospecific secondary forest of Alnus acuminata. Observed species (Chao 2; SE) Bryophytes Bray Curtis Dissimilarity (%) Observed species (Chao 2; SE) Lichens PF1 44 (46; 3.42 ) (173; 9.25) PF2 42 (44; 2.53 ) (157; 5.16) SF1 35 (36; 1.17) (128; 5.05) SF2 31 (32; 2.13) (132; 7.71) MF1 23 (23: 0.04) (93: 2.06) MF2 26 (27; 2.04) (92; 3.86) Bray Curtis Dissimilarity (%) Table 3 Results of the Generalized Mixed Linear Models on community traits at the plot level including beta coefficients (Coef) and associated standard errors (SE). Plot level Coef. (SE) F-value P-value Total Richness Mean tree diameter 0.009(0.002) Canopy cover 0.002(0.002) Elevation 0.032(0.016) Slope <-0.001(0.001) Aspect <0.001 (0.000) Bryophytes Richness Mean tree diameter 0.208(0.070) Canopy cover 0.146(0.062) Elevation 0.121(0.501) Slope 0.018(0.027) Aspect 0.002(0.004) Lichen Richness Mean tree diameter 0.430(0.137) Canopy cover (0.113) Elevation 0.061(0.053) Slope (0.051) Aspect 0.005(0.004) Shannon index Mean tree diameter 0.017(0.006) Canopy cover <-0.001(0.005) Elevation 0.046(0.042) Slope <0.001(0.002) Aspect <-0.001(0.000) Simpson inverse index Mean tree diameter 0.445(0.173) Canopy cover 0.008(0.151)

97 Elevation 1.252(1.230) Slope 0.027(0.067) Aspect (0.008) Species composition and community structure NMDS ordination resulted in a two-dimensional pattern with an average stress of and showed a clear separation of the three different forest types. Most of the variability was explained by axis 1 (r 2 =0.69), followed by axis 2 (r 2 =0.12, Fig. 2). Axis 1 was associated with changes in canopy cover (Axis 1=-0.926, Axes 2=+0.378, r 2 =0.712, p=0.001) and tree diameter (Axis 1= , Axis 3=+0.553, r 2 =0.539, p=0.001). The pairwise test revealed significant differences in epiphytic composition between the three types of forest vegetation: PF vs SF (66.40% dissimilarity, p=0.025), SF vs MF (75.00% diss., p=0.034) and PF vs MF (84.18% diss., p=0.015). Herbertus divergens, Coccocarpia filiformis, C. pellita, Coenogonium eximium and Cryptothecia exilis correlated with a dense canopy and large trees as found in PF, whereas Frullania brasiliensis, F. gibbosa, Metzgeria lechleri, Graphis anfractuosa, G. cinerea, Heterodermia diademata and H. hypochraea correlated with a more open canopy and smaller trees, characteristic of SF and MF (Supplementary data). Figure 2 Non-metric multidimensional scaling (NMDS) analysis of species composition for the samples (plots) in the studied primary and secondary montane forests (2 stands of each forest type) in Ecuador. PF, primary forest (circle); SF, Mixed secondary forest (square); MF, monospecific secondary forest of Alnus acuminate (triangle). 86

98 Discussion Our results showed significant changes in non-vascular epiphytic diversity (lichens and bryophytes) related to forest alteration in montane tropical forests. Major shifts in species diversity were caused by changes in canopy cover and tree size. Thus, epiphytic diversity was higher in primary forests (PF) than in the forests with more altered vegetation. In these two forest types, diversity was higher in mixed (SF) than in monospecific (MF) secondary forests. These results are consistent with other studies on epiphyte diversity in tropical montane forests (e.g. Acebey et al., 2003; Wolf, 2005; Werner and Gradstein, 2009) and support the notion that forest alteration leads to species loss in these communities. These data further indicate that species loss is related to the degree of forest alteration (i.e. selective logging, clear-cut, plantation) (Ariyanti et al., 2008; Sporn et al., 2009; Gradstein and Sporn, 2010) and the time since disturbance (Holz and Gradstein, 2005; Gradstein, 2008). As at least one hundred years are needed for the complete recovery of epiphyte diversity in montane forests (Holz and Gradstein, 2005), the maintenance of primary forests is crucial in the conservation of tropical rain forest biodiversity (Gibson et al., 2011). We also found that lichens and bryophytes responded differently to forest disturbance. Species loss in lichens mainly correlated with reduced tree size, while species loss in bryophytes was also significantly related to climatic changes (i.e. increase in solar radiation, decrease in air humidity) induced by lower canopy cover in SF and MF. A high, dense canopy promotes optimal climatic conditions inside forests for the growth of shade epiphytes which have higher water demands and are very sensitive to solar radiation (Sillett and Antoine, 2004; Gradstein, 2008; Benítez et al., 2012; Pardow and Lakatos, 2013). The irradiation in closed forests is converted into heat at the interface of the atmosphere and the canopy, maintaining moist and cool conditions in the forest understory (Hohnwald, 1999, cited in Werner and Gradstein, 2009). Canopy disruption caused by selective logging produces small openings in the canopy (5-10%), which can significantly affect ambient moisture (Zimmerman and Kormos, 2012) and lead to a decrease in the diversity of shade epiphytes, adapted to the moist, shaded interior of the forest (Sipman and Harris, 1989; Acebey et al., 2003; Gradstein, 2008; Gradstein and Sporn, 2010). However, while bryophytes experienced species loss due to high irradiation and evaporation stress in more open habitats (Perhans et al., 2009), total lichen richness was not reduced by these factors. This may be because some of the more shade-adapted species (shade epiphytes) were replaced by light-demanding species (sun epiphytes) especially in MF where canopy openness 87

99 was the highest (ca. 50%). Thus, open secondary montane forests can support a high richness of epiphytic lichens, even though there are fewer shade epiphytes (Hietz et al., 2006; Nöske et al., 2008). Species composition of both bryophytes and lichens was severely altered by the increase in canopy openness, indicating that community composition is a more sensitive indicator of human impact than species richness (Nöske et al., 2008). In general, shade epiphytes are more sensitive to environmental changes, because they are strongly dependent on atmospheric moisture and experience photoinhibition when exposed to greater sunlight than in their normal environment (Gauslaa et al., 2001; Green et al., 2008; Kranner et al., 2008). Ariyanti et al. (2008) found that microclimatic changes related to the loss of shaded cover were responsible for shifts in bryophyte composition. In our study, differences in species composition between the three forest types were particularly noticeable in the higher number of species of the liverwort genus Plagiochila and the lichen genera Coccocarpia, Coenogonium, Herpothallon, Leptogium and Sticta in primary forests versus species of the lichen genera Graphis, Heterodermia or Parmotrema in secondary forests. Biological characteristics of lichens exclusive to primary forests are the predominance of the photobiont with a reduction of the mycobiont (Coenogonium) or the presence of cyanobacteria as photobionts, constituting the so-called cyanolichens (Leptogium, Coccocarpia, Sticta) (Green et al., 2008; Benítez et al., 2012). However, some cyanolichen species (e.g. Coccocarpia stellata, Leptogium azureum, L. chloromelum, Sticta weigelii) may also occur in open, relatively dry habitats (Normann et al., 2010; Rosabal et al., 2010). In this sense, and focusing on these cyanolichens, we observed a contrasted vertical and horizontal zonation along the trunks. In the drier and more open sites along our gradient (Alnus acuminata forests), these species were more common on tree bases (below 50 cm) and on northern exposures where light incidence was lower. However, these species in primary forests were located at higher elevations ( cm) on both exposures (north and south). One of the major problems faced by tropical forests is the harvesting of large, long-lived and slow-growing trees (Zimmerman and Kormos, 2012), as they have the greatest bark surface area and the greatest formation of specialized aged bark substrates (e.g. Fritz et al., 2008; Johansson et al., 2009; Király et al., 2013). We suggest that these features, which are absent on younger, smaller trees, are preferred by epiphyte species, which might explain the high species replacement (measured as dissimilarity) between PF and MF. 88

100 Conclusion Species diversity of non-vascular epiphytes (lichens and bryophytes) growing on the trunk bases of tropical montane forests is negatively affected by forest alteration in two ways: (1) removal of hosts, especially large trees and (2) environmental changes caused by canopy disruption. Opposite to Dent and Wright (2009), who pointed the importance of secondary forests in terms of supporting tropical biodiversity, our analyses showed different species composition of primary and secondary forests and a high number of species found exclusively in primary forests, thus suggesting that secondary forests are of limited importance in compensating for the loss of epiphytic species in primary forests. Although this study contributes to the knowledge of these organisms and their dynamics in tropical ecosystems, we should consider the constraints related to the number of replicates per forest type. Since the response of lichens and bryophytes to new environmental conditions caused by the increase in canopy openness is related to their morphological and anatomical characteristics (e.g. growth form, thallus thickness, type of photobiont, cortical pigments), more studies on the functional traits of epiphytes are needed to better understand their response to forest disturbance. Acknowledgments The authors thank X. Yadira González for field assistance, Dr. S. Robbert Gradstein, Dr. Chris Johnson and anonymous reviewers for their valuable comments, corrections and suggestions which help us to improve de manuscript, and Lori De Hond for English revision and comments. Funding Financial support for this study was received from the Universidad Técnica Particular de Loja, the Secretaria Nacional de Educación Superior, Ciencia, Tecnología e Innovación of Ecuador and the Ministerio de Ciencia e Innovación of Spain (project EPICON, CGL ). 89

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106 Supplementary data: Number of trees on which each species appears in the six forests. Primary forests (PF1 and PF2); Mixed secondary forest (SF1 and SF2); Monospecific secondary forest of Alnus acuminata (MF1 and MF2). *: The species only occurs in one forest. Axis coordinates from each species (NMDS). Taxa PF1 PF2 SF1 SF2 MF1 MF2 AXIS 1 AXIS 2 Bryophytes Adelanthus decipiens (Hook.) Mitt ,8806-0,1233 Adelothecium bogotense (Hampe) Mitt. 6* -0,6396-1,2754 Anoplolejeunea conferta (C. F. W. Meissn. ex Spreng.) A. Evans ,5922 0,1117 Bazzania falcata (Lindenb.) Trevis. 1* -0,3388-1,1763 Bazzania longistipula (Lindenb.) Trevis. 1* -1,2057 1,3783 Campylopus asperifolius Mitt ,5886-1,111 Cheilolejeunea aff. inflexa (Hampe ex Lehm. & Lindenb.) Grolle 3* -0,9523 0,3445 Cheilolejeunea rigidula (Mont.) R.M. Schust ,0725 0,1309 Cryphaea sp. 9* 1,636 0,26 Diplasiolejeunea pauckertii Steph ,2192 0,7959 Drepanolejeunea granatensis (J.B. Jack & Steph.) Bischl ,4291-0,3909 Frullania apiculata (Reinw., Blume & Nees) Dumort. 1* 0,0123-0,2796 Frullania brasiliensis Raddi ,4713 0,3144 Frullania convoluta Lindenb. & Hampe ,2687 0,26 Frullania ericoides (Nees) Mont ,3659 0,1361 Frullania gibbosa Nees ,5766 0,1331 Frullania kunzei Lehm. & Lindenb ,3944 0,0513 Frullania aff. convoluta Lindenb. & Hampe 2* -1,1658 1,0656 Frullania sp ,3785 0,2191 Groutiella apiculata (Hook.) H.A. Crum & Steere 3 1-1,6131-0,0775 Herbertus divergens (Steph.) Herzog 4 2-1,453 0,116 Lejeunea laetevirens Nees & Mont ,6847-1,4407 Lejeunea cerina (Lehm. & Lindenb.) Gottsche, Lindenb. & Nees 3* -1,024-0,1167 Lepicolea pruinosa (Taylor) Spruce 4* -0,4618-1,1732 Lepidozia incurvata Lindenb. 1* -1,6345-0,6363 Lepidozia sp ,5034-0,2125 Leucolejeunea xanthocarpa (Lehm. & Lindenb.) A. Evans 3 3 1,5313-0,1618 Leptotheca boliviana Herzog 8* -1,0157 0,2777 Leucobryum antillarum Schimp. ex Besch ,5925-0,1864 Lophocolea bidentata (L.) Dumort ,0118 0,8879 Lophocolea muricata (Lehm.) Nees ,7531-0,5369 Macromitrium podocarpi Müll. Hal ,0082-0,2191 Macromitrium sp ,5799 0,

107 Marchesinia brachiata (Sw.) Schiffner ,3575-0,0858 Mastigolejeunea auriculata (Wils. & Hook.) Schiffn ,4547 0,3706 Metzgeria lechleri Steph ,5485 0,2301 Metzgeria consanguinea Schiffner 3* -0,5035-0,8275 Metzgeria leptoneura Spruce ,2511 0,7176 Metzgeria polytricha Spruce ,4642-0,2919 Metzgeria sp. 1* -1,184 0,1744 Microlejeunea bullata (Taylor) Steph ,0726-0,3778 Neckera scabridens Müll. Hal ,6236-0,321 Omphalanthus filiformis (Sw.) Nees ,4513 0,2517 Plagiochila aerea Taylor ,6786-0,6061 Plagiochila bifaria (Sw.) Lindenb ,5775 0,1657 Plagiochila bryopterioides Spruce ,3885-0,356 Plagiochila cristata (Sw.) Dumort 5* -0,4141-1,0033 Plagiochila diversifolia Lindenb. & Gottsche ,5598-0,841 Plagiochila longispina Lindenb. & Gottsche 6* -0,547-1,2991 Plagiochila pachyloma Taylor 4 2-1,5531-0,4221 Plagiochila raddiana Lindenb ,8582-0,1441 Plagiochila sp. 9* -1,6774-0,318 Porella brachiata (Taylor) Spruce ,9673 0,2635 Porella swartziana (F. Weber) Trev ,7335-0,4148 Porotrichodendron superbum (Taylor) Broth ,5923-0,7584 Porotrichum longirostre (Hook.) Mitt ,8877-0,4846 Porotrichum sp ,8845 0,2942 Prionodon densus (Sw. ex Hedw.) Müll. Hal ,9516-0,032 Radula javanica Gottsche ,858-0,6694 Radula quadrata Gottsche 5 2-0,3612 0,0687 Radula voluta Taylor ex Gottsche, Lindenb. & Nees ,8225-0,2877 Rhizogonium novae-hollandiae (Brid.) Brid. 3* 0,1985-0,0533 Sematophyllum cuspidiferum Mitt ,8296 0,1853 Squamidium nigricans (Hook.) Broth ,4524-0,294 Syrrhopodon gaudichaudii Mont ,5329 0,0379 Trichocolea tomentosa (Sw.) Gottsche 2* -0,3388-1,1763 Thuidium tomentosum Schimp ,0315-0,5061 Lichens Agonimia sp. 1* -1,007 1,0341 Alectoria ochroleuca (Hoffm.) A. Massal ,0661 0,8524 Amandinea sp. 6* 1,4873-0,5609 Amandinea submontana Marbach 2 1-0,5563-0,9939 Anthracothecium macrosporum (Hepp) Müll. Arg. 1* -1,8372 0,666 Anzia parasitica (Fée) Zahlbr ,3543-0,0716 Arthonia cinnabarina (DC.) Wallr ,2159 0,2052 Arthonia sp.1 1* -1,1558-0,

108 Arthonia sp.2 2* -0,9316-1,1498 Arthonia sp.3 1* -0,6423-1,1003 Arthothelium sp. 1* -0,7022-1,5286 Bacidia sp ,3999 0,3915 Bacidia sp ,5742 0,3114 Bacidia sp ,2081-0,5939 Bacidia sp ,2692 0,4478 Bacidia sp ,0125 0,068 Bacidia sp ,1282-0,3867 Bacidia sp.7 4* 1,2931 0,3245 Baculifera remensa (Stirt.) Marbach 5* 1,5112-0,5295 Badimia sp ,2905-0,3788 Brigantiaea leucoxantha (Spreng.) R. Sant. & Hafellner ,868-0,2585 Bryoria sp. 1* -1,2057 1,3783 Buellia rhombispora Marbach ,7057 0,2325 Bulbothrix apophysata (Hale & Kurok.) Hale 3 3 1,5052 0,3666 Bulbothrix coronata (Fée) Hale ,6021 0,2371 Bulbothrix isidiza (Nyl.) Hale 1 6-0,249-0,6858 Bulbothrix suffixa (Stirton) Hale 1 4-0,4039-0,751 Byssoloma subdiscordans (Nyl.) P. James ,8092 0,4612 Canomaculina cristobalii (L.I. Ferraro & Elix) Elix ,3869 0,2056 Canomaculina pilosa (Stizenb.) Elix & Hale ,443-0,854 Chiodecton sphaerale Ach. 4* -1,0637 0,0808 Chrysothrix chrysophtalma (P. James) P. James & J. R. Laundon ,6105 0,2127 Cladonia coniocraea (Flörke) Sprengel ,4683 0,0071 Cladonia subradiata (Vainio) Sandst ,6137-0,2632 Coccocarpia dissecta Swinscow & Krog 1 3-1,4545 0,5895 Coccocarpia erythroxyli (Spreng.) Swinscow & Krog ,5518 0,0897 Coccocarpia filiformis Arv ,4627 0,0117 Coccocarpia guimarana (Vain.) Swinscow & Krog 2* -0,9731 0,4409 Coccocarpia microphyllina Lücking & Aptroot 2 5-1,3902 0,3248 Coccocarpia palmicola (Spreng.) Arv. & D.J. Galloway ,3463-0,5133 Coccocarpia pellita (Ach.) Müll. Arg ,3329 0,2654 Coccocarpia prostrata Lücking, Aptroot & Sipman ,8401-0,4684 Coccocarpia stellata Tuck ,4314-0,1792 Coccocarpia sp ,2153 0,6801 Coenogonium aff. frederici (Kalb) Kalb & Lücking ,4801-0,0627 Coenogonium aff. kawanae (H. Harada & Vezda) H. Harada & Lumbsch 2* -0,7834 0,511 Coenogonium bacilliferum (Malme) Lücking, Aptroot & Sipman 6* -1,2271 1,

109 Coenogonium epiphyllum Vain ,981-0,3999 Coenogonium eximium (Nyl.) Kalb & Lücking 2* -1,5293-0,1674 Coenogonium isidiosum (Breuss) Rivas Plata, Lücking, Umaña & Chavez 1* -1,3272-0,1434 Coenogonium kalbii Aptroot, Lücking & Umaña ,9037 0,7113 Coenogonium leprieurii (Mont.) Nyl ,956 0,4233 Coenogonium linkii Ehrenb. 2 0,7082 0,2875 Coenogonium luteolum (Kalb) Kalb & Lücking 5 5 1,5664 0,0334 Coenogonium lutescens (Vezda & Malcolm) Malcolm 1* -1,184 0,1744 Coenogonium magdalenae Rivas Plata, Lücking & Lizano ,541-0,2207 Coenogonium moniliforme Tuck. 2* -1,2319-0,0994 Coenogonium nepalense (G. Thor & Vezda) Lücking, Aptroot & Sipman ,1265 0,2659 Coenogonium pertenue (Stirt.) Kalb & Lücking ,517 0,0193 Coenogonium pineti (Ach.) Lücking & Lumbsch 5* -1,175 0,1835 Coenogonium roumeguerianum (Müll. Arg.) Kalb 8* -1,1939 1,1009 Coenogonium sp. 1* -1,0703 0,9772 Cresponea leprieurii (Mont.) Egea & Torrente ,5408-0,1737 Cresponea melanocheloides (Vain.) Egea & Torrente 1 9-1,314 0,8368 Cryptothecia effusa (Müll. Arg.) R. Sant. 3-1,3764 1,0547 Cryptothecia exilis G. Thor 1* -1,007 1,0341 Cryptothecia punctisorediata Sparrius & Saipunkaew 1 2-1,0045 0,6169 Cryptothecia striata Thor 2* -1,0145 1,0274 Dichosporidium boschianum (Mont.) G. Thor ,1013-0,2464 Diplolabia sp ,8179-0,3639 Echinoplaca sp. 1* -0,3533-0,9345 Everniastrum cirrhatum (Fr.) Hale ex Sipman 7 2-0,7383 0,3994 Everniastrum vexans (Zahlbr. ex W.L. Culb. & C.F. Culb.) Hale ex Sipman ,3775-0,1356 Fellhanera sp. 2* -1,2445 0,8858 Fissurina sp.1 2* -1,1558-0,0643 Fissurina sp.2 1* -0,0376-0,6453 Fissurina triticea (Nyl.) Staiger 4* -0,497-0,9976 Flakea papillata O. E. Erikss 2* 1,401 0,5822 Flavopunctelia flaventior (Stirt.) Hale 1 2 1,618 0,3208 Glyphis cicatricosa Ach ,5292 0,2996 Glyphis scyphulifera (Ach.) Staiger ,6771-1,3547 Graphis aff. bettinae Lücking, Umaña, Chaves & Sipman 11* 1,4247 0,4261 Graphis aff. striatula (Ach.) Spreng ,2337 0,058 Graphis anfractuosa (Eschw.) Eschw. 1* 1,7075 0,51 98

110 Graphis bettinae Lücking, Umaña, Chaves & Sipman 8 4 1,5424-0,0708 Graphis cinerea (Zahlbr.) M. Nakan. 1* 1,7075 0,51 Graphis conferta Zenker ,6723-0,5718 Graphis elixiana A.W. Archer 1* -0,0541-0,315 Graphis elongatoradians Fink. 2* 1,3517 0,2038 Graphis leptoclada Müll. Arg ,6171 0,1889 Graphis leptogramma Nyl. 2* 1,536-0,4967 Graphis myrtacea (Müll. Arg.) Lücking 1 1 1,3503 0,2594 Graphis pinicola Zahlbr ,4635 0,2551 Graphis ruiziana (Fée) A. Massal ,4229-0,3777 Graphis scaphella (Fée) A. Massal. 1* -1,0612 0,3792 Graphis sitiana Vain. 2* 1,5849-0,2582 Graphis streblocarpa (Bél.) Nyl ,5498 0,1027 Graphis subcontorta (Müll. Arg.) Lücking & Chaves 1* -0,0422-0,5722 Graphis subserpentina Nyl. 1* -0,9316-1,1498 Graphis sp ,4612 0,3829 Gyalecta sp. 1* -1,3 0,6871 Haematomma africanum (J. Steiner) C.W. Dodge 2* 1,6596 0,2471 Haematomma flexuosum Hillm. 3* -0,5915-0,7196 Herpothallon aff. roseocinctum (Fr.) Aptroot, Lücking & G. Thor ,769-0,4589 Herpothallon confusum G. Thor 1* -1,4671 0,7689 Herpothallon granulare (Sipman) Aptroot & Lücking ,6154-0,4568 Herpothallon hypoprotocetraricum G. Thor 4* -0,4746-1,1639 Herpothallon rubrocinctum (Ehrenb.) Aptroot & Lücking ,4285-0,0456 Herpothallon sp ,3725 0,871 Herpothallon sp ,1465 0,7531 Herpothallon sp.3 2* 1,3018 0,1484 Heterodermia aff. galactophylla (Tuck.) W.L. Culb ,0654-0,6285 Heterodermia comosa (Eschw.) Follmann & Redón 1* -0,6423-1,1003 Heterodermia corallophora (Taylor) Skorepa ,781-0,2206 Heterodermia diademata (Taylor) D.D. Awasthi ,5283 0,3 Heterodermia galactophylla (Tuck.) W.L. Culb ,7187 0,0015 Heterodermia hypochraea (Vain.) Swinscow & Krog 4 5 1,3343 0,2494 Heterodermia hypoleuca (Mühl.) Trevis ,494 0,4144 Heterodermia isidiophora (Nyl.) D.D. Awasthi ,3937 0,0589 Heterodermia japonica (M. Satô) Swinscow & Krog ,2681-0,0198 Heterodermia leucomela (L.) Poelt ,5412-0,1458 Heterodermia microphylla (Kurok.) Swinscow & Krog 1* 0,5862 0,

111 Heterodermia palpebrata (Taylor) Trass 2* -1,184 0,1744 Heterodermia sitchensis Goward & W.J.Noble 4 3-0,5865-1,028 Heterodermia spathulifera Moberg & Purvis ,3342-0,6207 Heterodermia subcitrina Moberg 2 1 1,2919-0,001 Heterodermia sp ,542 0,402 Hypoflavia velloziae (Kalb) Marbach 1 1-0,2796-0,7694 Hypotrachyna aff. degelii (Hale) Hale ,5369 0,4694 Hypotrachyna bogotensis (Vain.) Hale 1 3-0,6393 0,3855 Hypotrachyna costaricensis (Nyl.) Hale ,9266 0,8906 Hypotrachyna densirhizinata (Kurok.) Hale 5 1 0,1294-0,3628 Hypotrachyna eitenii (Hale) Hale 3 5-0,5114-1,0864 Hypotrachyna rachista (Hale) Hale 4* 1,5884-0,2125 Hypotrachyna reducens (Nyl.) Hale 9* -0,6167-0,9068 Hypotrachyna revoluta (Flörke) Hale ,8866 0,0306 Hypotrachyna rockii (Zahlbr.) Hale ,2943 0,0298 Hypotrachyna sp ,4744 0,3758 Lecanora caesiorubella Ach ,079-0,3585 Lecanora chlarothera Nyl. 1* 0,0123-0,2796 Lecanora flavidomarginata B. de Lesd ,498 0,0314 Lecanora helva Stizenb ,4972 0,2189 Lecanora neonashii Lumbsch 3* 1,82 0,2477 Lecanora varia (Hoffm.) Ach ,5102 0,0186 Lecanora sp. 1* -0,6423-1,1003 Leioderma glabrum D. J. Galloway & P. M. Jørg ,5149-0,4356 Leiorreuma exaltatum (Mont. & Bosch) Staiger 2* -1,6519-0,2581 Lepraria sp ,9357 0,7633 Lepraria sp ,1457 0,1321 Leptogium austroamericanum (Malme) C.W. Dodge ,634-0,1728 Leptogium azureum (Sw.) Mont ,5409-0,1842 Leptogium burgesii (L.) Mont ,309-0,1619 Leptogium burnetii Dodge 4 2-1,0501 0,7487 Leptogium chloromelum (Ach.) Nyl ,6812 0,5368 Leptogium cochleatum (Dicks.) P.M. Jørg. & P. James ,7821-0,0333 Leptogium coralloideum (Meyen & Flot.) Vain ,1646 0,0582 Leptogium corticola (Taylor) Tuck ,6028 0,5347 Leptogium cyanescens (Pers.) Körb ,2088 0,7393 Leptogium diaphanum (Sw.) Mont ,786 0,3105 Leptogium laceroides B. de Lesd ,7462 0,2195 Leptogium marginellum (Sw.) Gray 4* -1,2556-0,1122 Leptogium millegranum Sierk 4 2-1,1936 0,4798 Leptogium olivaceum (Hook.) Zahlbr ,5723 0,134 Leptogium phyllocarpum (Pers.) Mont ,2789 0,1754 Lithothelium sp.1 2* 1,7359 0,

112 Lithothelium sp.2 6* 1,336 0,5494 Lobaria erosa (Eschw.) Nyl ,787 0,236 Lobaria tenuis Vain ,2943 0,5182 Lobariella crenulata (Hook.) Yoshim ,2208-0,0127 Lobariella exornata (Zahlbr.) Yoshim. 3* -1,0712 1,3234 Lobariella pallida (Hook.) Yoshim ,8498 0,601 Lopezaria versicolor (Fée) Kalb & Hafellner 2* 0,2324-0,6873 Malcolmiella fuscella (Müll. Arg.) M. Cáceres & Lücking ,1519 0,1391 Malcolmiella gyalectoides (Vain.) Cáceres & Lücking 3* 1,5703 0,1335 Malcolmiella sp. 1* -1,6345-0,6363 Malmidea aff. rhodopis (Tuck.) Kalb, Rivas Plata & Lumbsch 1* -1,1558-0,0643 Maronea constans (Nyl.) Hepp 2 2-0,8666 0,8381 Maronina multifera (Nyl.) Hafellner & R. W. Rogers ,7004-0,146 Megalaria sp.1 3* -0,97 0,3554 Megalaria sp ,1695-0,0349 Megalospora admixta (Nyl.) Sipman 1* 0,0123-0,2796 Megalospora melanodermia (Müll. Arg.) Zahlbr. 3* -1,0923 1,2976 Megalospora sulphurata var. nigricans (Müll. Arg.) Riddle 5 4-0,8839 0,4491 Megalospora sulphurata var. sulphurata Meyen ,4594-0,7728 Megalospora tuberculosa (Fee) Sipman ,6039-0,1529 Megalospora sp. 1* -1,1486 0,0576 Micarea sp.1 2* -0,5368-0,7096 Micarea sp.2 1* -0,7335 1,2553 Micarea sp.3 3* -1,0807 1,0486 Mycomicrothelia subfallens (Mull. Arg.) D. Hawksw ,301 0,8097 Myeloconis sp ,0118 0,1335 Normandina pulchella (Borrer) Nyl. 1* -0,0422-0,5722 Ocellularia sp ,5481 0,6371 Ochrolechia pseudopallescens Brodo ,1984-0,5536 Ochrolechia sp. 2* -0,6118-1,1694 Opegrapha sp. 2* -0,9664 1,1009 Pannaria conoplea (Ach.) Bory ,7063-0,7166 Pannaria mosenii C.W. Dodge 1 5-1,0884 0,9477 Pannaria prolificans Vain ,2221 0,5428 Parmeliella andina P.M. Jørg. & Sipman ,3356 0,2264 Parmeliella delicata P.M. Jørg. & Arv ,2274 0,834 Parmeliella miradorensis Vain ,4304 0,2241 Parmeliella sp ,4191-0,2604 Parmelinopsis miniarum (Vain.) Elix & Hale 5* -1,062 1,0211 Parmotrema aff. exquisitum (Kurok.) DePriest & B.W. Hale ,3446 0,0975 Parmotrema arnoldii (Du Rietz) Hale ,3355-0,

113 Parmotrema austrosinense (Zahlbr.) Hale 9* 1,7904 0,2772 Parmotrema cristiferum (Taylor) Hale 7 1 1,5321-0,0827 Parmotrema exquisitum (Kurok.) DePriest & B.W. Hale 12* 1,3685 0,1334 Parmotrema internexum (Nyl.) Hale ex DePriest & B.W. Hale ,4636-0,3918 Parmotrema mellisii (Dodge) Hale 4 4-1,0672 0,5633 Parmotrema peralbidum (Hale) Hale ,2027-0,6252 Parmotrema rampoddense (Nyl.) Hale ,2701 0,3603 Parmotrema zollingeri (Hepp) Hale ,5037-0,5411 Peltigera sp. 1* -1,8372 0,666 Pertusaria aff. papillata (Ach.) Tuck 1 2-1,515 0,1989 Pertusaria excludens Nyl. 8* 1,3647 0,1468 Pertusaria hypothamnolica Dibben ,7168 0,1153 Pertusaria multipunctoides Dibben 2 6-0,9067-0,5836 Pertusaria ventosa Malme ,738-0,0391 Pertusaria sp ,0722 0,5085 Pertusaria sp ,5472-0,0897 Pertusaria sp.3 1* -1,3791 1,108 Pertusaria sp.4 2* -0,2558-0,6171 Phaeographis "scalpturatilla" 16* 1,4959 0,0916 Phaeographis brasiliensis (A. Massal.) Kalb & Matthes-Leicht 1* 1,4608-0,5959 Phaeographis brevinigra Sipman ,4793 0,1472 Phaeographis dendritica (Ach.) Müll. Arg. 16* 1,4318 0,247 Phaeographis inconspicua (Fée) Müll. Arg ,1246-0,1838 Phaeographis scalpturata (Ach.) Staiger 1 5 1,5351 0,0772 Phaeographis sp. 1* -0,2919-0,7499 Phaeophyscia aff. limbata (Poelt) Kashiw ,5567 0,2712 Phlyctella sp ,7646-0,0091 Phlyctella sp.2 2* -0,0404-0,1907 Phyllopsora chlorophaea (Müll. Arg.) Zahlbr ,1483 0,5473 Phyllopsora fendleri (Tuck. & Mont.) Müll. Arg. 2* -1,6345-0,6363 Phyllopsora furfuracea (Pers.) Zahlbr ,7688-0,4082 Phyllopsora glaucescens Timdal 3* -1,213 0,0762 Phyllopsora hispaniolae Timdal 12* -1,2439-0,0023 Phyllopsora isidiotyla (Vain.) Riddle ,8789 0,144 Phyllopsora parvifolia (Pers.) Mull. Arg ,0004 0,5831 Phyllopsora parvifoliella (Nyl.) Mull. Arg ,0343 0,3376 Phyllopsora santensis (Tuck.) Swinscow & Krog ,9029 0,555 Phyllopsora sp ,1977 0,4783 Porina aff. nucula Ach. 1* -1,1558-0,0643 Porina imitatrix Müll. Arg ,6997 0,1008 Porina internigrans (Nyl.) Müll. Arg ,1794 0,3026 Porina nucula Ach ,5258-0,1096 Porina sp. 1* 1,535 0,

114 Pseudocyphellaria aurata (Ach.) Vain ,2159-0,0709 Pseudocyphellaria crocata (L.) Vain ,8822 0,8298 Punctelia crispa Marcelli, Jungbluth & Elix ,4374-0,0934 Punctelia reddenda (Stirt.) Krog ,8994-0,1634 Pyrenula aff. falsaria (Zahlbr.) R. C. Harris 4* 1,4543 0,1358 Pyrenula aff. mamillana (Ach.) Trevisan 4* -1,2795-0,1625 Pyrenula andina Aptroot 4* 1,3907 0,1015 Pyrenula cf. nitidula (Bresadola) R. C. Harris 1* -0,4426-1,1124 Pyrenula macrocarpa A. Massal ,6039-0,1529 Pyrenula mastophoroides (Nyl.) Zahlbr. 2* -0,5168-0,6307 Pyrenula microcarpa Mull. Arg. 1* -1,1558-0,0643 Pyrenula microtheca R. C. Harris 2* 1,3514 0,5177 Pyrenula tenuisepta R. C. Harris ,0722-0,3004 Pyrenula sp ,3162 0,8481 Pyrenula sp.2 3* -0,5711-0,687 Pyrenula sp.3 2* -0,0934-0,4638 Pyrenula sp.4 2* -0,2919-0,7499 Pyrgillus sp. 2* -1,1418 0,2448 Ramalina celastri (Spreng.) Krog & Swinscow ,5686-0,2905 Ramalina cochlearis Zahlbr. 2* 1,536-0,4967 Ramalina peruviana Ach ,4106 0,1351 Ramalina sp ,3995-0,0279 Ramonia sp. 3* -1,1011 0,1681 Relicina abstrusa (Vain.) Hale 1 6-0,8971 0,7665 Rimelia subisidiosa (Müll. Arg.) Hale & A. Fletcher 2 2-1,3145 0,455 Rimelia succinreticulata Eliasaro & Adler 5* -0,92 1,1038 Rinodina sp.1 1* 1,4248 0,116 Rinodina sp.2 2* -0,7022-1,5286 Sarcographa fenicis (Vain.) Zahlbr. 2* -0,7022-1,5286 Squamacidia janeirensis (Müll. Arg.) Brako 2 1-0,9462 0,6957 Squamacidia sp. 2* -1,2633 0,0511 Sticta andensis (Nyl.) Trevis ,9478 0,6402 Sticta ferax Müll. Arg ,1416-0,1886 Sticta fuliginosa (Dicks.) Ach ,3363 0,8404 Sticta humboldtii Hook ,3583 0,4085 Sticta laciniata (Sw.) Ach ,4922 0,1865 Sticta lobarioides Moncada & Coca ,1698 0,0346 Sticta neolinita Gyeln ,2162 0,3314 Sticta neopulmonarioides Moncada & Coca 3 2-1,1825 0,5873 Sticta tomentosa (Sw.) Ach ,9183 0,1525 Sticta weigelii (Ach.) Vain ,3603-0,1973 Sticta sp ,1985 0,8257 Sticta sp ,1464 0,6384 Teloschistes flavicans (Sw.) Norman ,5933 0,

115 Tephromela atra (Hudson) Hafellner 1 9 1,5344 0,3259 Thelotrema aff. hawaiense (Hale) Hale 2* 0,1985-0,0533 Thelotrema hawaiense (Hale) Hale 1* -1,1977 1,1608 Thelotrema sp ,52 0,5488 Thelotrema sp ,5899 0,3467 Thelotrema sp ,067-0,012 Trichothelium horridulum (Mull. Arg.) R. Sant ,1325 1,1111 Trypethelium sp ,9668-0,061 Usnea sp ,3266-0,1165 Usnea sp ,4927 0,3923 Usnea sp ,271 0,5039 Usnea sp ,6119-0,3519 Yoshimuriella dissecta (Sw.)B. Moncada & Lücking 5 3-0,8001 0,2356 Yoshimuriella subdissecta (Nyl.)B. Moncada & Lücking ,3911 0,

116 CAPÍTULO III / CHAPTER III Functional traits of epiphytic lichens as indicators of forest disturbance level and predictors of total richness and diversity Benítez Angel a, Aragón Gregorio b, González Yadira a, Prieto Maria b a Sección de Sistemáticay Diversidad, Departamento de Ciencias Naturales, Universidad Técnica Particularde Loja, San Cayetano s/n, Loja, Ecuador. b Área de Biodiversidad y Conservación, ESCET, Universidad Rey Juan Carlos, Móstoles, E-28933, Madrid, Spain Benítez, Á., Aragón, G., González Y. & Prieto, M. Artículo en revisión en Ecological Indicators 105

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118 Abstract Epiphytic lichens are good ecological indicators due to their poikilohydric nature, which makes them sensitive to climatic and environmental changes. The physiology of lichens is related with their morphology and anatomy (traits) and thus the response to changes in the environment could be related with these traits. In this study we evaluate whether lichen functional traits are related with deforestation of tropical montane forests to be used as indicators of the disturbance level. We also evaluate the use of selected functional traits to infer total species richness and diversity of tropical montane forests. To do this, we assessed nine different traits related with photobiont type, growth form, reproductive strategy and chemistry of epiphytic lichens on the trunk bases of 240 trees in three types of forests according to a disturbance gradient (primary forests and secondary vegetation). Most functional traits of the lichen communities were related to structural changes (i.e canopy cover and tree diameter) along the forest disturbance gradient. Several trait categories are suitable to be used as indicators of forest disturbance level highlighting cyanolichens, filamentose and squamulose growth forms and species without secondary compounds as indicators of primary forests and fruticose, foliose species with narrow lobes, and with lirellae as the best indicators of disturbed forest. Growth forms are useful indicators for total lichen richness and diversity in montane tropical forests. Based on these results we recommend the use of lichen functional traits as a tool and a complement for conservation studies and forest management. Keywords: community weighted mean (CWM); conservation; Ecuador; growth forms; indicator species; tropical montane forests. 107

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120 1. Introduction Despite tropical montane rain forests are among the richest biologically and ecologically ecosystems in the world, they are disappearing at alarming rates due to anthropogenic threats (Myers et al., 2000; Laurance et al., 2006; Laurance, 2007; Gardner et al., 2009; Laurance et al., 2011; Gibson et al., 2011). A large proportion of the original landscapes of montane rain forests have been transformed into secondary vegetation, croplands or grasslands in order to satisfy human needs related with food, fiber, timber, and other goods (Dirzo and Raven, 2003; Foley et al., 2005; Wright, 2005; Chazdon et al., 2008; Gibbs et al., 2010; Gibson et al., 2011). Consequently, this scenario of rapid deforestation and forest conversion has caused the decline and disappearance of numerous species populating these habitats (Lawton et al., 1998; Sillet and Antoine, 2004; Kessler et al., 2005; Barlow et al., 2007; Gray et al., 2007; Nöske et al., 2008). Among them, lichens are a significant part in terms of diversity, biomass and its contribution to nutrient cycling (Holz and Gradstein, 2005), which are also affected by forest logging and deforestation (Gradstein, 2008; Nöske et al., 2008; Aragón et al., 2010; Benitez et al., 2012, 2015). Numerous studies have used the species richness and diversity to understand the impact of forest disturbance on communities, but sometimes these data are not sufficient to fully understand the ecological processes shaping these communities (Lawton et al., 1998; Schulze et al., 2004; Nöske et al., 2008; Larrea and Werner, 2010; Aragón et al., 2010; Gradstein and Sporn, 2010; Benitez et al., 2015). An alternative approximation to understand the mechanisms of community assembly and thus, how communities will respond to rapid environmental changes (e.g. forest disturbance) is to consider functional traits, as they are directly related to biotic and abiotic factors (Díaz et al., 2007; Webb et al., 2010; Pinho et al., 2012). In vascular plants, functional traits have been broadly used to study the response to forest disturbance, providing suitable information for biodiversity conservation and ecosystem functioning (Díaz et al., 1999, 2002, 2004; Mabry and Fraterrigo, 2009; Vandewalle et al., 2010; Laliberté et al., 2010; Sabatini et al., 2014; Carreño-Rocabado et al., 2016). Lichens are sensitive indicators of climatic conditions, because their poikilohydric physiology depends directly on water availability, surrounding temperature and light received (Nash, 1996; Green et al., 2008; Kranner et al., 2008). Forests conversion and logging alter microclimatic conditions related with moisture and light. Lichens present functional strategies related with photobiont, growth form, reproduction 109

121 strategy, presence of cortical pigments and secondary metabolites which depend on the environmental conditions and provide (dis)-advantages to them (Kranner et al., 2008; Marini et al., 2011; Giordani et al., 2012; Hauck et al., 2013). Previous studies have shown that several functional traits as photobiont type, growth form, reproductive structure and chemistry are directly related to microclimatic factors associated with forest structure (e.g. canopy cover, and tree age) and environmental conditions as humidity, temperature and light availability (Ellis and Coppins, 2006; Marini et al., 2011; Pinho et al., 2012; Li et al., 2013). In order to study the diversity of lichens it would be very useful to use indicator species instead of using species, genera or families due to the effort required for identification and sampling (Bergamini et al., 2005, 2007; Aragón et al., 2013). Several studies related with non-vascular epiphytes (bryophytes and lichens) suggest that the richness of growth forms is a robust estimator for detection of species richness of bryophytes and lichens in biodiversity hotspots as tropical forests and Mediterranean forests (Oishi, 2009; Pardow et al., 2012; Aragón et al., 2016). Therefore, from a conservation perspective, the use of easily recognizable growth forms in lichens could be used to detect areas of high lichen biodiversity. Our main goal was to evaluate changes in lichen functional traits in relation with the disturbance level of tropical montane rainforests. We hypothesized that forest structure, in particular, canopy cover and tree diameter, would affect the individual species traits and the community weighted mean (CWM). Second, we suspect that the richness of growth forms would be an indicator of total species richness and diversity of lichens. Specifically, we addressed the following questions: 1) how do the richness of each functional trait and the CWM respond to forests disturbance? 2) which lichen functional trait is the best indicator of forest disturbance?, and 3) could the total lichen species richness and diversity be predicted by the richness of growth forms alone?. 2. Methods 2.1. Study area Experimental design and details of the geographical location of the study is detailed in Benitez et al. (2012; 2015), and only a brief summary is included here. The survey was conducted in six remnants of tropical montane forests in southern Ecuador. The climate is humid tropical with a mean annual temperature of 20 C, annual rainfall 110

122 of ca mm and relative humidity of ca. 80% (data from the National Institute of Meteorology and Hydrology, INAMI). The altitude of the studied remnants ranged from 2200 to 2800 m a.s.l. These forests were chosen to cover a disturbance gradient, with the following three categories: (1) remnant primary forest fragments (PF) of evergreen montane tropical vegetation characterized by a dense canopy layer and large trees, (2) Secondary forest fragments (SF) that have regrown after selective logging events which took place some 40 years ago and (3) Secondary monospecific vegetation (MF) dominated by Alnus acuminata Kunth which have re-grown after a total logging of the original forest, and are characterized by a more open canopy cover and young trees Sampling design and data collection Two forests were studied per disturbance category. Within each forest, we established 10 plots, 5 m x 5 m each. In each plot, four trees were selected to estimate the occurrence of epiphytic lichens. For these trees, lichen frequency and coverage were visually estimated on six cm grids located at three heights (0 50 cm, cm, cm), and at the north and south aspects. In addition, the following variables were measured at plot level: canopy cover (%), elevation (m a.s.l.), slope (º), aspect (cosine transformed) and mean tree DBH (cm) of the 4 trees analyzed per plot. For species identification, we used general and specific taxonomic and floristic papers (e.g. Brako, 1991; Egea and Torrente, 1993; Brodo et al., 2001; Nash et al., 2002, 2004; Rivas-Plata et al., 2006; Nash et al., 2007; Lücking et al., 2008, 2009; Brodo et al., 2008; Timdal, 2008; Aptroot et al., 2008, 2009; Aptroot, 2012; Moncada et al., 2013) Functional traits For each lichen species found in the study area, nine traits were assessed to perform the functional analysis: (1) Photobiont type; (2) Growth form; (3) Size; (4) Reproduction type; (5) Type of reproductive structure; (6) Ascospores septation; (7) Ascospores size; (8) Thallus colour; and (9) Chemistry (Table 1). The information related to these traits was obtained from specific taxonomic literature (cited above), observed directly from the specimen collected and using the Database for the Rapid Identification of Lichens ( 111

123 Table 1. Functional traits categories and codes. Functional trait Categories Photobiont type C=Chlorococcoid; CY=Cyanobacteria; T=Trentepholia C= Crustose; CP=Crustose with prothallus; FB= Foliose with Growth form broad lobes; FN= Foliose with narrow lobes; FP= Foliose placodiod; FL=Filamentose; F=Fruticose, G=Gelatinose; S=Squamulose Size M=Macrolichens; MC=Microlichens Reproduction type A=Asexual; S=Sexual; AS=Asexual and sexual; N=None Reproductive structure A=Apothecia; I=Isidia; L=Lirellae; P=Perithecia; S=Soredia Ascospores septation S=Simple; S=Septate; M=Muriform Ascospores size* S=Small (<100 µm); M=Medium (>100 µm); L=Large ( >500 µm) Thallus colour D=Dark; L=Light Chemistry** A=Acids; O = Other compounds; N= No compounds *Ascospore size was calculated as the product of the length and width (µm 2 ). **Acids correspond to atranorin, parietin, furmarprotocetraric, stictic, norstictic and usnic. Other compounds refer to those that are exclusive in several species with and unknown function. The functional traits were selected based on previous studies, due to its relation with ecosystems functioning (Ellis and Coppins, 2006; Stofer et al., 2006, Johansson et al., 2006, 2007; Marini et al., 2011; Giordani et al., 2012; Pinho et al., 2012; Li et al., 2013). Specifically, photobiont type is related with light, temperature and water requirements for the photosynthesis and respiration processes (Lange et al., 1986; Lakatos et al., 2006; Marini et al., 2011). Growth form (thallus morphology) is related with water uptake and loss (Lakatos et al., 2006; Büdel and Scheidegger, 2008). Secondary metabolites (e.g. usnic acid) contribute to protect lichens from solar irradiation and herbivory (Cocchietto et al., 2002; Hauck et al., 2007, 2009). Finally, the reproductive strategy is related with dispersion ability and establishment (Stofer et al., 2006; Koch et al., 2013). Functional traits categories of each species are detailed in Appendix Data analysis We calculated species richness as the total number of different lichen species occurring in a plot. To analyze species diversity we calculated the Simpson s and Shannon s indices (Magurran, 2004) per plot with PRIMER v (Anderson et al., 2008). In addition, we calculated floristic similarities using Sørensen s and Bray-Curtis similarity indices (Chao et al., 2005), using EstimateS (Colwell, 2013). 112

124 To characterize the community structure from a functional perspective (Ricotta and Moretti, 2011) we used the community weighted mean (CWM), which describes the trait averages over a community (de Bello et al., 2007) and reflects the dominant trait in a given community (Garnier et al., 2004; Lepš et al., 2006; Violle et al., 2007; Lavorel et al., 2008). The total species richness of each functional trait category was calculated as the total number of species with each trait category found in the four trees per plot. Community weighted means, considering a continuous trait, represents the sum of each species trait value weighted by its relative abundance in the community (Lavorel et al., 2008). For multinomial traits, we have calculated it as the sum of the cover of all species sharing a trait divided by the total species cover, representing the proportion of each individual trait-category per community (i.e. mean trait values weighted with the abundance). The effect of environmental variables (canopy cover, elevation, slope, aspect and mean tree diameter per plot) on richness and CWM of the different lichen functional trait categories was modelled by fitting Generalized Linear Mixed Models (GLMMs) (McCullagh and Nelder, 1989). The richness and CWM models of each functional trait category were fitted with Poisson errors. Significance was estimated by means of deviance analysis (Guisan et al., 2002). All GLMMs computations were performed using SAS Macro program GLIMMIX, which iteratively calls SAS Procedure Mixed until convergence (GLIMMIX ver. 8 for SAS/STAT). To determine which lichen functional trait category was associated with the forest type, in order to identify it as indicator trait, we used the indicator species analysis developed by Dufrêne and Legendre (1997) and used by Koch et al. (2013). This analysis calculates an indicator value for each trait category based on the mean cover of each functional trait category per forest, which results from multiplying the relative abundance for each trait category by the frequency for each trait category in each forest. The indval function with the labdsv package was used for this purpose (Roberts, 2012), using R (R Development Core Team, 2015). The indicator value ranges from 0 (when one species trait was absent from one forest type) to 100 (when one species trait occurred in all plots of one forest type and was absent from other plots). The significance was tested using a Monte Carlo permutation with 1000 replicates. To determine whether a single functional category could be used as predictor for the total species richness of lichens, we used Pearson s linear correlation 113

125 coefficients to explore the relationships between the species richness per growth forms (pairwise tests) and the total species richness and diversity indices. When testing correlation, the number of species of each growth form was subtracted to the total richness of lichens to avoid biases produced by differences in species abundance. To keep a reasonable test-wide Type I error, the alpha values were divided by the number of correlations (nine correlations) (Sebastião and Grelle, 2009). Results A total of 307 epiphytic lichen species were recorded in 60 plots; for which nine functional traits were assessed. The richness of most functional trait categories decreased along the gradient of disturbance (Figs. 1-4). Thus, lichen species with Cyanobacteria and Trentepohlia decreased with increasing forest disturbance (Fig. 1). Figure 1. Richness of each photobiont type by type of forest (PF=primary forest; SF=mixed secondary forest; MF=monoespecific secondary forest of Alnus acuminata). C=Chlorococcoid. CY= Cyanobacteria. T=Trentepohlia. A similar pattern was found in the growth forms, with crustose species with prothallus, foliose broadly lobed, filamentose and gelatinose species decreasing in secondary forests (Fig. 2), and the disappearance of foliose placodiod and squamulose species in the monospecific forests of A. acuminata. 114

126 Figure 2. Richness of each growth form per type of forest (PF=primary forest; SF=mixed secondary forest; MF=monoespecific secondary forest of A. acuminata). C= Crustose; CP=Crustose with prothallus; FB= Foliose with broad lobes; FN= Foliose with narrow lobes; FP= Foliose placodiod; FL=Filamentose; F=Fruticose, G=Gelatinose; S=Squamulose. Species with apothecia and isidia also decreased in monospecific forests (Figs. 2 and 3). In contrast, foliose species with narrow lobes and those species with lirellate apothecia and soredia increased along the disturbance gradient (Figs. 2 and 3). Figure 3. Richness of reproductive structures per type of forest (PF=primary forest; SF=mixed secondary forest; MF=monoespecific secondary forest of A. acuminata). A=Apothecia; I=Isidia; L=Lirellae; P=Perithecia; S=Soredia. 115

127 In addition, lichens with acids as secondary compounds (atranorin, antrachinones, stictic and usnic acid) were more frequent in secondary forests, while lichens without acids (or with other compounds) increased in primary forests (Fig. 4). Figure 4. Richness of different secondary compounds per type of forest (PF=primary forest; SF=mixed secondary forest; MF=monoespecific secondary forest of A. acuminata). A=Acids; O = Other compounds; N= No compounds. The most relevant predictors for the richness of functional traits and CWM of epiphytic lichens were canopy cover and tree diameter, followed by altitude (Table 2). Aspect and slope had influence on very few traits (Table 2). Canopy cover had a positive and significant effect on cyanolichens, crustose species with prothallus, foliose placodioid, gelatinose species and lichens without secondary metabolites. Tree diameter had the same effect on lichens with Chroococcoid photobionts, foliose with broad lobes, fruticose, squamulose and isidiate species. On the other hand, canopy cover had a negative effect on the species with Trentepohlia, foliose lichens with narrow lobes, species with lirellae, with soredia and with acids as secondary metabolites (Table 2). 116

128 Table 2. Results of the Generalised Linear Mixed Models of plot-scale variables on the richness and CWM of the considered functional trait categories of epiphytic lichens. Coefficients of the variables in the model and P-value (between parentheses) are indicated. DBH=mean tree diameter, CWM= community weighted means of trait values. Photobiont Chlorococcoid Cyanobacteria Trentepholia Size Canopy cover (0.0080) Richness DBH Altitude Aspect Slope (0.0006) (0.0074) Canopy cover (0.0014) (0.0001) CWM DBH Altitude Aspect Slope (0.0456) Macrolichens Microlichens Growth form Crustose Crustose with prothallus Foliose with broad lobes Foliose with narrow lobes Foliose placodioid Filamentose Fruticose Gelatinose Squamulose Reproduction Asexual Sexual Asexual sexual None and (0.0013) (0.0037) (0.0010) Reproductive structure (0.0100) (0.0065) (0.0233) (<0.0001) (0.0110) (0.0155) (0.0456) (0.0417) (0.0473) (0.0075) (0.0177) (0.0378) (0.0317) (0.0037) (0.0444) (0.0009) (0.0165) Apothecia (0.0033) (0.0106) Isidia (<0.0001) Lirellae (0.0393) (0.0097) Perithecia (0.0146) Soredia (0.0434) (0.0311) 117

129 (0.0002) (0.0491) (0.0084) (0.0204) continued Ascospores septation Simples Canopy cover Richess DBH Altitude Aspect Slope (0.0235) (0.0381) Canopy cover CWM DBH Altitude Aspect Slope (0.478) Septated Muriform Ascospores size Small (0.0057) (0.0476) (0.0118) Medium Large Tallus colour Dark Light (0.0006) (0.0027) Chemistry Acids Other compounds No compounds (0.0025) (0.0007) (0.0343) (0.0079) (0.0044) Cyanolichens, species without secondary compounds, crustose with protallus, foliose placodiod, filamentose, gelatinose and squamulose growth forms, were the best indicators of sheltered habitats of montane undisturbed forests (PF), whereas, fruticose, foliose species with narrow lobes, lirellate and sorediate lichens and those species with light thallus colour and acids as secondary compounds were the best indicators of disturbed forest (Table 3). Table 3. Trait categories of epiphytic lichens with statistical significant values of indication for each forests type, following the indicator species analyses. P-values < 0.05 are considered significant. Trait categories with indicator value > 55% are considered as the best indicators. Functional group Forest type Indicator value P-value Photobiont Chlorococcoid MF Cyanobacteria PF Trentepohlia MF

130 Size Macrolichens PF Microlichens MF Growth form Crustose MF Crustose with prothallus PF Foliose with broad lobes PF Foliose with narrow lobes MF Foliose placodioid PF Filamentose PF Fruticose MF Gelatinose PF Squamulose PF Reproduction Asexual SF Sexual MF Asexual and sexual MF None MF Reproductive structure Apothecia PF Isidia SF Lirellae MF Perithecia SF Soredia MF Ascospores type Simple MF Septate PF Muriform PF Ascospores size Small MF Medium PF Large MF Thallus colour Dark PF Light MF Chemistry Acids MF Other compounds MF No compounds PF Several trait categories were correlated within the growth forms. Gelatinose forms were highly and positively correlated with foliose placodioid, crustose with prothallus and filamentose growth forms whereas foliose species with narrow lobes were negatively correlated with these previous four growth forms (Table 4). 119

131 Table 4. Pearson s correlation of species richness per growth forms of epiphytic lichens. P-value with asterisk is indicated. ns= Not significant. *= P < ** = P < ***= P < Richness CP S FI FN FB FP FR G C -0.55*** -0.31* -0.36** 0.47*** -0.59*** -0.51*** 0.34** -0.44*** CP 0.80*** 0.73*** -0.87*** 0.70*** 0.85*** -0.43*** 0.85*** S 0.72*** -0.82*** 0.55*** 0.83*** -0.37** 0.85*** FI -0.77*** 0.59*** 0.70*** -0.25ns 0.69*** FN -0.61*** -0.89*** 0.47*** -0.88*** FB 0.60*** -0.22ns 0.64*** FP -0.40** 0.85*** FR -0.40** Total species richness and diversity of epiphytic lichens were highly correlated with most growth form categories. The increase in the richness of gelatinose growth forms, filamentous, squamulose, foliose placodiod and crustose with prothallus was highly and significantly correlated with the increase in the total species richness. On the other hand, the richness of crustose and foliose species with narrow lobes were negatively correlated with the total richness of lichens (Table 5). Diversity was mainly related with gelatinose forms, crustose with prothallus and foliose species with broad lobes. Most growth forms were negatively correlated with Sørensen s and Bray-Curtis similarity indices except crustose, fruticulose and foliose species with narrow lobes (Table 5). Table 5. Pearson s correlation coefficients between the total lichen species richness and diversity and growth forms of epiphytic lichens. P-value is indicated as ns= Not significant. *= P < ** = P < ***= P < Traits richness Total Richness Shanno n index Simpso n inverse index Sorense n index Bray Curtis Crustose -0.61*** -0.19ns -0.13ns 0.54*** 0.53*** Crustose with prothallus 0.55*** 0.40** 0.15ns -0.77*** -0.73*** Foliose with broad lobes -0.02ns 0.70*** 0.53*** -0.68*** -0.78*** Foliose with narrow lobes -0.87*** -0.31* -0.04ns 0.78*** 0.67*** Foliose placodioid 0.56*** 0.30* 0.04ns -0.73*** -0.73*** Filamentose 0.70*** 0.30* 0.06ns -0.68*** -0.63*** Fruticulose -0.24ns -0.01ns 0.07ns 0.42*** 0.31* Gelatinose 0.74*** 0.44*** 0.17ns -0.73*** -0.76*** Squamulose 0.64*** 0.32* 0.02ns -0.68*** -0.63*** 120

132 Discussion Our results demonstrate that lichen traits and the CWM were related to the forest structural changes along a gradient of disturbance and were mainly controlled by factors related with the canopy cover and tree diameter. Several trait categories have high indicator values of the forest conservation status and growth forms are related with the total lichen species richness and diversity in tropical montane forests. The observed changes in functional groups (species with similar trait categories) in relation with the forest disturbance level may be caused by the similarity in the ecological and physiological requirements. Thus, the greater occurrence of three functional groups (i.e. Cyanolichens, gelatinose and crustose species or foliose species with placodiod thalli) on primary forests, was mainly due to the presence of a closed canopy, sheltered and humid with unaltered forest interior environments (Belinchón et al., 2007; Kranner et al., 2008; Aragón et al., 2010; Normann et al., 2010; Rosabal et al., 2010; Marini et al., 2011; Benitez et al., 2012; Li et al., 2013). This is due to that they are intolerant to excessive light and need liquid water to activate photosynthesis (Lange et al., 1986; Nash, 1996; Hedenås and Ericson, 2000; Sillet and Antoine, 2004). Crustose species with prothallus (e.g. Cryptothecia and Herpothallon) are more frequent in primary forests probably favoured by the hyphal projections from the medulla that create a hydrophobic layer and repels water excess as reported for Cryptothecia rubrocincta (Lakatos et al., 2006). Filamentose lichens (e.g. Coenogonium) are also related with old-growth and dense primary forests, and restricted to the low light environment of tropical shady understorey (Sipman and Harris, 1989; Lücking, 1999; Brodo et al., 2001). For them it has been reported high evaporation rates and rapid desiccation of the thallus (Lakatos et al., 2006). The decrease in squamulose and in foliose species with broad lobes in monospecific forests is related with the size of the trunks which may provide less available substrate for lichens, therefore limiting their abundance (Esseen et al., 1996; Lie et al., 2009). In contrast, fruticose, foliose species with narrow lobes, species with lirellate apothecia and those with acids as secondary metabolites were more abundant in secondary forests and negatively correlated with canopy cover. This is probably related to a higher luminosity and a lower humidity conditions promoted by canopy disruption. As a general pattern, foliose species with narrow lobes (e.g. Heterodermia and 121

133 Hypotrachyna) and fruticose lichens are more heliophytic, occupying sites with high irradiance levels and water stress (Aragón et al., 2010; Rosabal et al., 2010; Marini et al., 2011; Benitez et al., 2012; Giordani et al., 2012; Koch et al., 2013; Li et al., 2015). Lichens with lirellate ascoma (e.g. Graphis) are also more abundant in secondary forests. This is probably related with the tolerance to high light intensities and dry habitats conferred by the black and closed lirellae (Kappen, 1988; Lücking, 1999; Koch et al., 2013). Lichens producing acids as secondary compounds were more common in secondary forests, due to the protection against excessive radiation conferred by these compounds as it has been previously showed (Cocchietto et al., 2002; Hauck et al., 2007, 2009, 2013). With increasing disturbance intensity the importance of Chlorococcoid green algae and Trentepohlia as lichen photobionts increased, while it decreased for cyanobacteria. Stofer et al. (2006) found evidence showing that lichens with green algae are better adapted in open and intensively managed forests having a great capacity to avoid photoinhibition effects and being able to photosynthetize with minimum thallus water content and reactivate photosynthesis from air humidity (Lange et al., 1986; Demmig-Adams et al., 1990; Ellis and Coppins, 2006; Gauslaa and Solhaug, 2004; Hilmo et al., 2005). The analysis of indicator traits showed that photobiont type, growth forms, reproductive structure and secondary metabolites can be used as indicators of the conservation status (i.e. disturbance level) in tropical montane rainforests. Thus, crustose lichens with protallus, foliose placodiod, filamentose, gelatinose and squamulose growth forms can be used as indicators for primary forests, while foliose with narrow lobes and fruticose growth forms, lirellate and sorediate lichens were the best indicators of secondary forests. Other studies also found lichen traits as indicators for the forests disturbance level. Thus, fruticose and foliose species with narrow lobes have been proposed as indicators of open or disturbed forests (Giordani et al., 2012; Koch et al., 2013; Li et al., 2013) and cyanobacterial and gelatinose lichens as indicators of undisturbed or primary forests (Rosabal et al., 2010; Aragón et al., 2010, 2013; Benitez et al., 2012; Li et al., 2013). Morover, functional traits of epiphytic lichens have been used as indicators of air quality (Llop et al., 2012), effects of urbanization (Munzi et al., 2014; Pinho et al., 2016), and ecological conditions or climatic change (Giordani et al., 2012; Pinho et al., 2012; Matos et al., 2015). Based on these results and based on the fact that lichen species require considerable sampling effort and taxonomic expertise for 122

134 identification (Bergamini et al., 2005), we propose the use of indicator traits as a tool for studies of the conservation status of forests. Occasionally, the richness of genera, families and orders has been used to estimate total richness or diversity of several taxonomic groups (Beccaloni and Gaston, 1995; Balmford et al., 2000; Sebastião and Grelle, 2009). The great effort required for sampling and identification of lichens, especially the most inconspicuous species (e.g. crustose lichens), makes necessary to develop alternative ways for rapid diversity surveys (Giordani et al., 2009). Growth forms of lichens and bryophytes are easily identifiable traits, and they could be valuable indicators of diversity and thus previously used (Oishi, 2009; Pardow et al., 2012; Aragón et al., 2016) as a robust estimator for detection of total species richness. Following with this idea Aragon et al. (2016) showed that the diversity of growth forms was highly correlated with the overall lichen richness and can be used as a tool to the conservation of the high lichen diversity in the Mediterranean region. However, functional traits (e.g. growth forms) are poorly documented as indicators in tropical forests (Koch et al., 2013), hindering their use in environmental monitoring and conservation of lichens on these forests. Here, we contribute to this gap by studying growth forms of lichens as indicators of species richness and diversity in tropical montane forests. In conclusion, species traits and CWM of lichen communities responded significantly to structural forest changes along disturbance gradient as canopy cover and tree diameter. Photobiont type, growth form, reproductive structure and secondary compounds, are suitable functional traits to be used as indicators of disturbance level. Furthermore, we also found the richness of different growth forms as an indicator value to obtain information about the total epiphytic lichen species richness and diversity in montane tropical forests, which is crucial for forest monitoring and biodiversity conservation. This approximation will provide an important step for conservation studies as it constitute a feasible and promising alternative for evaluating and monitoring environmental changes in tropical montane forests that can be applied by non-specialists because the easiness to identify traits. Acknowledgments: Financial support for this study was granted by the Universidad Técnica Particular de Loja (PROJECT_CCNN_941), the Secretaría Nacional de Educación Superior, Ciencia, Tecnología e Innovación of Ecuador and the Ministerio de Ciencia e 123

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144 Species Appendix A. List of the lichens species with each trait categories. Codes for functional trait categories are described in Table 1. Photobio nt type Growth form Size Reprodu ction type Reprodu ctive structure Ascospore septation Ascopore size Thallus colour Agonimia sp. C C MC S P M - D N Alectoria ochroleuca (Hoffm.) A. Massal. C F M N D A Amandinea sp. C C MC S A SP - D N Amandinea submontana Marbach C C MC S A SP - D N Anthracothecium macrosporum (Hepp) Müll. Arg. C C MC S P SP L D N Anzia parasitica (Fée) Zahlbr. C FN M N D A Arthonia cinnabarina (DC.) Wallr. T C MC S A SP M L A Arthonia sp.1 Arthonia sp.2 Arthonia sp.3 Arthothelium sp. Bacidia sp.1 Bacidia sp.2 Bacidia sp.3 Bacidia sp.4 Bacidia sp.5 Bacidia sp.6 T C MC S A SP - L A T C MC S A SP - L A T C MC S A SP - L A T C MC S L M - L N C C MC S A SP - L A C C MC S A SP - L A C C MC S A SP - L A C C MC S A SP - L A C C MC S A SP - L A C C MC S A SP - L A Bacidia sp.7 C C MC S A SP - L A Baculifera remensa (Stirt.) Marbach C C MC S A SP M L A Badimia sp. C C MC S A SP - L A Brigantiaea leucoxantha (Spreng.) R. Sant. & Hafellner C C MC S A M L L A Bryoria sp. C F M N D A Buellia rhombispora Marbach C C MC S A SP M L A Bulbothrix apophysata (Hale & Kurok.) Hale C FN M A I - - L A Bulbothrix coronata (Fée) Hale C FN M S A S S L A Bulbothrix isidiza (Nyl.) Hale C FN M AS A,I S S L A Bulbothrix suffixa (Stirton) Hale C FN M S A S S L A Chemistry 133

145 Byssoloma subdiscordans (Nyl.) P. James C C MC S A SP S L N Canomaculina cristobalii (L.I. Ferraro & Elix) Elix C FB M A S - - L A Canomaculina pilosa (Stizenb.) Elix & Hale C FB M A S - - L A Chiodecton sphaerale Ach. T C MC S A SP - L N Chrysothrix chrysophtalma (P. James) P. James & J. R. Laundon C C MC S A SP M D O Cladonia coniocraea (Flörke) Sprengel C F M AS A,S S S D A Cladonia subradiata (Vainio) Sandst. C F M AS A,I,S S S L A Coccocapia dissecta Swinscow & Krog CY FB M AS A,I S S D N Coccocarpia erythroxyli (Spreng.) Swinscow & Krog CY FB M S A S S D N Coccocarpia filiformis Arv. CY FB M S A S S D N Coccocarpia guimarana (Vain.) Swinscow & Krog CY FB M A I - - D N Coccocarpia microphyllina Lücking & Aptroot CY FB M AS A,I S S D N Coccocarpia palmicola (Spreng.) Arv. & D.J. Galloway CY FB M AS A,I S S D N Coccocarpia pellita (Ach.) Müll. Arg. CY FB M AS A,I S S D N Coccocarpia prostrata Lücking, Aptroot & Sipman CY FB M S A S S D N Coccocarpia stellata Tuck. CY FB M S A S S D N Coccocarpia sp. CY FB M S A S - L N Coenogonium aff. frederici (Kalb) Kalb & Lücking T C MC S A SP - D N Coenogonium aff. kawanae (H. Harada & Vezda) H. Harada & Lumbsch T C MC S A SP - D N Coenogonium bacilliferum (Malme) Lücking, Aptroot & Sipman T C MC S A SP S D N Coenogonium epiphyllum Vain. T FL MC S A SP - D N Coenogonium eximium (Nyl.) Kalb & Lücking T FL MC S A SP S D N 134

146 Coenogonium isidiosum (Breuss) Rivas Plata, Lücking, Umaña & Chavez T C MC AS A,I SP S D N Coenogonium kalbii Aptroot, Lücking & Umaña T C MC S A SP S D N Coenogonium leprieurii (Mont.) Nyl. T FL MC S A SP S D N Coenogonium linkii Ehrenb. T FL MC S A SP S D N Coenogonium luteolum (Kalb) Kalb & Lücking T FL MC S A SP S D N Coenogonium lutescens (Vezda & Malcolm) Malcolm T C MC S A SP S D N Coenogonium magdalenae Rivas Plata, Lücking & Lizano T C MC S A SP S D N Coenogonium moniliforme Tuck. T FL MC S A SP S D N Coenogonium nepalense (G. Thor & Vezda) Lücking, Aptroot & Sipman T C MC S A SP - D N Coenogonium pertenue (Stirt.) Kalb & Lücking T C MC S A SP S D N Coenogonium pineti (Ach.) Lücking & Lumbsch T FL MC S A SP S D N Coenogonium roumeguerianum (Müll. Arg.) Kalb T C MC S A SP - D N Coenogonium sp. T C MC S A SP - D N Cresponea leprieurii (Mont.) Egea & Torrente T C MC S A SP M D N Cresponea melanocheloides (Vain.) Egea & Torrente T C MC S A SP M D N Cryptothecia effusa (Müll. Arg.) R. Sant. T CP MC S A M L L O Cryptothecia exilis G. Thor T CP MC S A M L D O Cryptothecia punctisorediata Sparrius & Saipunkaew T CP MC AS A,S M L D O Cryptothecia striata Thor T CP MC S A M L D A Dichosporidium boschianum (Mont.) G. Thor T CP MC S A SP - D N Diplolabia sp. Echinoplaca sp. T C MC S L SP - D O C C MC S A SP - L N 135

147 Everniastrum cirrhatum (Fr.) Hale ex Sipman C F M S A S M L A Everniastrum vexans (Zahlbr. ex W.L. Culb. & C.F. Culb.) Hale ex Sipman C F M AS A,I S S L A Fellhanera sp. Fissurina sp.1 C C MC S A SP - L O T C MC S L SP - D N Fissurina sp.2 T C MC S L SP - D N Fissurina triticea (Nyl.) Staiger T C MC S L SP M D O Flakea papillata O. E. Erikss C FN MC N D O Flavopunctelia flaventior (Stirt.) Hale C FB M AS A,S S M D A Glyphis cicatricosa Ach. T C MC S A SP M L N Glyphis scyphulifera (Ach.) Staiger T C MC S A M L L N Graphis aff. bettinae Lücking, Umaña, Chaves & Sipman T C MC S L SP L L N Graphis aff. striatula (Ach.) Spreng. T C MC S L SP M L N Graphis anfractuosa (Eschw.) Eschw. T C MC S L SP M L N Graphis bettinae Lücking, Umaña, Chaves & Sipman T C MC S L SP L L N Graphis cinerea (Zahlbr.) M. Nakan. T C MC S L SP L L N Graphis conferta Zenker T C MC S L SP M L N Graphis elixiana A.W. Archer T C MC S L M L D A Graphis elongatoradians Fink. T C MC S L - - L A Graphis leptoclada Müll. Arg. T C MC S L SP M L N Graphis leptogramma Nyl. T C MC S L SP M L N Graphis myrtacea (Müll. Arg.) Lücking T C MC S L M L L N Graphis pinicola Zahlbr. T C MC S L SP M L N Graphis ruiziana (Fée) A. Massal. T C MC S L M L L N Graphis scaphella (Fée) A. Massal. T C MC S L M L L N Graphis sitiana Vain. T C MC S L SP M L N Graphis streblocarpa (Bél.) Nyl. T C MC S L M L L A 136

148 Graphis subcontorta (Müll. Arg.) Lücking & Chaves T C MC S L M L L N Graphis subserpentina Nyl. T C MC S L M L L N Graphis sp. T C MC S L - - L N Gyalecta sp. T C MC S A SP - L N Haematomma africanum (J. Steiner) C.W. Dodge C C MC S A SP M L A Haematomma flexuosum Hillm. C C MC S A SP M L A Herpothallon aff. roseocinctum (Fr.) Aptroot, Lücking & G. Thor T CP MC A I - - D O Herpothallon confusum G. Thor T CP MC A I - - D O Herpothallon granulare (Sipman) Aptroot & Lücking T CP MC A I - - D O Herpothallon hypoprotocetraricu m G. Thor T CP MC A I - - D A Herpothallon rubrocinctum (Ehrenb.) Aptroot & Lücking T CP MC A I - - D O Herpothallon sp.1 Herpothallon sp.2 T CP MC A I - - D O T CP MC A I - - D O Herpothallon sp.3 T CP MC A I - - D O Heterodermia aff. galactophylla (Tuck.) W.L. Culb. C FN M A S - - L A Heterodermia comosa (Eschw.) Follmann & Redón C FN M S A SP L L A Heterodermia corallophora (Taylor) Skorepa C FN M AS A,I SP L L A Heterodermia diademata (Taylor) D.D. Awasthi C FN M S A SP M L A Heterodermia galactophylla (Tuck.) W.L. Culb. C FN M A S - - L A Heterodermia hypochraea (Vain.) Swinscow & Krog C FN M A I - - L A Heterodermia hypoleuca (Mühl.) Trevis. C FN M S A SP M L A Heterodermia isidiophora (Nyl.) D.D. Awasthi C FN M AS A,I SP M L A Heterodermia japonica (M. Satô) Swinscow & Krog C FN M AS A,S SP L L A Heterodermia leucomela (L.) Poelt C FN M AS A,S SP L L A 137

149 Heterodermia microphylla (Kurok.) Swinscow & Krog C FN M A S - - L A Heterodermia palpebrata (Taylor) Trass C FN M S A SP L L A Heterodermia sitchensis Goward & W.J.Noble C FN M AS A,S SP S L A Heterodermia spathulifera Moberg & Purvis C FN M AS A,S SP L L A Heterodermia subcitrina Moberg C FN M AS A,S SP M L A Heterodermia sp. C FN M A S - - L A Hypoflavia velloziae (Kalb) Marbach C C MC S A SP - L N Hypotrachyna aff. degelii (Hale) Hale C FN M A S - - L A Hypotrachyna bogotensis (Vain.) Hale C FN M AS A,I S S L A Hypotrachyna costaricensis (Nyl.) Hale C FN M AS A,I S S L A Hypotrachyna densirhizinata (Kurok.) Hale C FN M AS A,S S M L A Hypotrachyna eitenii (Hale) Hale C FN M S A S S L A Hypotrachyna rachista (Hale) Hale C FN M A I - - L A Hypotrachyna reducens (Nyl.) Hale C FN M S A S S D A Hypotrachyna revoluta (Flörke) Hale C FN M AS A,S S S L A Hypotrachyna rockii (Zahlbr.) Hale C FN M AS A,S S S L A Hypotrachyna sp. C FN M A S - - L A Lecanora caesiorubella Ach. C C MC S A S S L A Lecanora chlarothera Nyl. C C MC S A S S L A Lecanora flavidomarginata B. de Lesd. C C MC S A S S L A Lecanora helva Stizenb. C C MC S A S M L A Lecanora neonashii Lumbsch C C MC S A S S L A Lecanora varia (Hoffm.) Ach. C C MC S A S S L A Lecanora sp. C C MC S A S - L A Leioderma glabrum D. J. Galloway & P. M. Jørg. CY FB M S A S S L N Leiorreuma exaltatum (Mont. & Bosch) Staiger C C MC S A SP M D N 138

150 Lepraria sp.1 C C MC A S - - L A Lepraria sp.2 C C MC A S - - L A Leptogium austroamericanum (Malme) C.W. Dodge CY G M AS A,I SP M D N Leptogium azureum (Sw.) Mont. CY G M S A SP M D N Leptogium burgesii (L.) Mont. CY G M S A M M D N Leptogium burnetii Dodge CY G M A I - - D N Leptogium chloromelum (Ach.) Nyl. CY G M S A M M D N Leptogium cochleatum (Dicks.) P.M. Jørg. & P. James CY G M S A M M D N Leptogium coralloideum (Meyen & Flot.) Vain. CY G M AS A,I M M D N Leptogium corticola (Taylor) Tuck. CY G M S A M M D N Leptogium cyanescens (Pers.) Körb. CY G M AS A,I M M D N Leptogium diaphanum (Sw.) Mont. CY G M A I - D N Leptogium laceroides B. de Lesd. CY G M AS A,I M M D N Leptogium marginellum (Sw.) Gray CY G M AS A,I M M D N Leptogium millegranum Sierk CY G M A A,I SP M D N Leptogium olivaceum (Hook.) Zahlbr. CY G M A I - D N Leptogium phyllocarpum (Pers.) Mont. CY G M S A M L D N Lithothelium sp.1 T C MC S P SP - D N Lithothelium sp.2 T C MC S P SP - D N Lobaria erosa (Eschw.) Nyl. CY FB M S A SP - D N Lobaria tenuis Vain. C FB M AS A,I SP M D A Lobariella crenulata (Hook.) Yoshim. CY FB M S A SP M D O Lobariella exornata (Zahlbr.) Yoshim. CY FB M AS A,I SP L L O Lobariella pallida (Hook.) Yoshim. CY FB M S A SP - L O Lopezaria versicolor (Fée) Kalb & Hafellner C C MC S A SP L L 139

151 Malcolmiella fuscella (Müll. Arg.) M. Cáceres & Lücking C C MC S A S - L N Malcolmiella gyalectoides (Vain.) Cáceres & Lücking C C MC S A S - L N Malcolmiella sp. C C MC S A S - L N Malmidea aff. rhodopis (Tuck.) Kalb, Rivas Plata & Lumbsch C C MC S A S S D O Maronea constans (Nyl.) Hepp C C MC S A S S L O Maronina multifera (Nyl.) Hafellner & R. W. Rogers C C MC S A SP - L N Megalaria sp.1 C C MC S A SP - L N Megalaria sp.2 C C MC S A SP - L N Megalospora admixta (Nyl.) Sipman C C MC S A M L L O Megalospora melanodermia (Müll. Arg.) Zahlbr. C C MC S A SP L L A Megalospora sulphurata var. nigricans (Müll. Arg.) Riddle C C MC S A SP - L A Megalospora sulphurata var. sulphurata Meyen C C MC S A SP - L A Megalospora tuberculosa (Fee) Sipman C C MC S A SP L L A Megalospora sp. Micarea sp.1 Micarea sp.2 C C MC S A SP - L A C C MC S A SP - L N C C MC S A SP - L N Micarea sp.3 C C MC S A SP - L N Mycomicrothelia subfallens (Mull. Arg.) D. Hawksw. T C MC S P SP S L N Myeloconis sp. T C MC S P M - L N Normandina pulchella (Borrer) Nyl. C S MC AS P,S SP M L N Ocellularia sp. T C MC S A SP - L O Ochrolechia pseudopallescens Brodo C C MC S A S L L O Ochrolechia sp. C C MC S A S - L O Opegrapha sp. C C MC S L SP - L N Pannaria conoplea (Ach.) Bory CY FP M AS A,I S M D O Pannaria mosenii C.W. Dodge CY FP M AS A,I S M D N 140

152 Pannaria prolificans Vain. CY FP M AS A,I S - D N Parmeliella andina P.M. Jørg. & Sipman CY FP M S A S - D N Parmeliella delicata P.M. Jørg. & Arv. CY FP M S A S - D N Parmeliella miradorensis Vain. CY FP M S A S M D N Parmeliella sp. CY FP M S A - - D Parmelinopsis miniarum (Vain.) Elix & Hale C FP M AS A,I S M L A Parmotrema aff. exquisitum (Kurok.) DePriest & B.W. Hale C FB M A S - - L A Parmotrema arnoldii (Du Rietz) Hale C FB M AS A,S S M L A Parmotrema austrosinense (Zahlbr.) Hale C FB M AS A,S S M L A Parmotrema cristiferum (Taylor) Hale C FB M A A,S S M L A Parmotrema exquisitum (Kurok.) DePriest & B.W. Hale C FB M A S - - L A Parmotrema internexum (Nyl.) Hale ex DePriest & B.W. Hale C FB M AS A,I S S L A Parmotrema mellisii (Dodge) Hale C FB M AS A,I S M L A Parmotrema peralbidum (Hale) Hale C FB M AS A,I S S L A Parmotrema rampoddense (Nyl.) Hale C FB M AS A,S S S L A Parmotrema zollingeri (Hepp) Hale C FB M S A S M L A Peltigera sp. CY FB M N D N Pertusaria aff. papillata (Ach.) Tuck C C MC S A S - L A Pertusaria excludens Nyl. C C MC A A,S S - L A Pertusaria hypothamnolica Dibben C C MC S A S - L A Pertusaria multipunctoides Dibben C C MC S A S - L A Pertusaria ventosa Malme C C MC S A S - L A Pertusaria sp.1 Pertusaria sp.2 Pertusaria sp.3 C C MC S A S - L A C C MC S A S - L A C C MC S A S - L A 141

153 Pertusaria sp.4 C C MC S A S - L A Phaeographis "scalpturatilla" T C MC S L SP - L O Phaeographis brasiliensis (A. Massal.) Kalb & Matthes-Leicht T C MC S L SP M L A Phaeographis brevinigra Sipman T C MC S L SP - L O Phaeographis dendritica (Ach.) Müll. Arg. T C MC S L SP M L A Phaeographis inconspicua (Fée) Müll. Arg. T C MC S L SP S L A Phaeographis scalpturata (Ach.) Staiger T C MC S L M L L N Phaeographis sp. T C MC S L SP - L A Phaeophyscia aff. limbata (Poelt) Kashiw. C FN M N L A Phlyctella sp.1 C C MC S A M - D N Phlyctella sp.2 C C MC S A M - D N Phyllopsora chlorophaea (Müll. Arg.) Zahlbr. C S MC AS A,I S S D N Phyllopsora fendleri (Tuck. & Mont.) Müll. Arg. C S MC S A S S D N Phyllopsora furfuracea (Pers.) Zahlbr. C S MC AS A,I S S D O Phyllopsora glaucescens Timdal C S MC S A S S D O Phyllopsora hispaniolae Timdal C S MC AS A,I S S D O Phyllopsora isidiotyla (Vain.) Riddle C S MC AS A,I S S D A Phyllopsora parvifolia (Pers.) Mull. Arg. C S MC S A S S D N Phyllopsora parvifoliella (Nyl.) Mull. Arg. C S MC AS A,I S S D A Phyllopsora santensis (Tuck.) Swinscow & Krog C S MC AS A,I S S D A Phyllopsora sp. C S MC S A S - D O Porina aff. nucula Ach. T C MC S P SP L D N Porina imitatrix Müll. Arg. T C MC S P SP M D N Porina internigrans (Nyl.) Müll. Arg. T C MC S P SP M D N Porina nucula Ach. T C MC S P SP L D N Porina sp. T C MC S P SP - D N Pseudocyphellaria aurata (Ach.) Vain. C FB M AS A,S SP M D O 142

154 Pseudocyphellaria crocata (L.) Vain. CY FB M AS A,S SP M D O Punctelia crispa Marcelli, Jungbluth & Elix C FB M A I - - L A Punctelia reddenda (Stirt.) Krog C FB M A I - - L A Pyrenula aff. falsaria (Zahlbr.) R. C. Harris T C MC S P M L D N Pyrenula aff. mamillana (Ach.) Trevisan T C MC S P SP M D N Pyrenula andina Aptroot T C MC S P SP M D O Pyrenula cf. nitidula (Bresadola) R. C. Harris T C MC S P SP M D N Pyrenula macrocarpa A. Massal. T C MC S P SP M D N Pyrenula mastophoroides (Nyl.) Zahlbr. T C MC S P SP L D N Pyrenula microcarpa Mull. Arg. T C MC S P SP M D N Pyrenula microtheca R. C. Harris T C MC S P SP M D N Pyrenula tenuisepta R. C. Harris T C MC S P SP M D N Pyrenula sp.1 Pyrenula sp.2 Pyrenula sp.3 Pyrenula sp.4 T C MC S P SP - D N T C MC S P SP - D N T C MC S P SP - D N T C MC S P SP - D N Pyrgillus sp. T C MC S P SP - D N Ramalina celastri (Spreng.) Krog & Swinscow C F M S A SP S L A Ramalina cochlearis Zahlbr. C F M A S - - L A Ramalina peruviana Ach. C F M A S - - L A Ramalina sp. C F M S A - - L A Ramonia sp. T C MC S A S - L N Relicina abstrusa (Vain.) Hale C FN M AS A,I S S L A Rimelia subisidiosa (Müll. Arg.) Hale & A. Fletcher C FN M AS A,I S M L A Rimelia succinreticulata Eliasaro & Adler C FN M A S - - L A Rinodina sp.1 C C MC S A SP - L N Rinodina sp.2 C C MC S A SP - L N Sarcographa fenicis (Vain.) Zahlbr. T C MC S L SP M D A 143

155 Squamacidia janeirensis (Müll. Arg.) Brako C S MC S A S - D N Squamacidia sp. C S MC S A S - D N Sticta andensis (Nyl.) Trevis. CY FB M S A SP M D N Sticta ferax Müll. Arg. CY FB M S A SP - D N Sticta fuliginosa (Dicks.) Ach. CY FB M AS A,I SP M D N Sticta humboldtii Hook. CY FB M S A SP M D N Sticta laciniata (Sw.) Ach. CY FB M S A SP - D N Sticta lobarioides Moncada & Coca C FB M S A SP M D N Sticta neolinita Gyeln. C FB M S A SP M D N Sticta neopulmonarioides Moncada & Coca C FB M S A SP M D N Sticta tomentosa (Sw.) Ach. CY FB M S A SP M D N Sticta weigelii (Ach.) Vain. CY FB M A I - - D N Sticta sp. 1 CY FB M N D N Sticta sp. 2 CY FB M S A SP - D N Teloschistes flavicans (Sw.) Norman C F M AS A,S SP S D A Tephromela atra (Hudson) Hafellner C C MC S A S S L A Thelotrema aff. hawaiense (Hale) Hale T C MC S A M - L A Thelotrema hawaiense (Hale) Hale T C MC S A M - L A Thelotrema sp.1 Thelotrema sp.2 T C MC S A - - L A T C MC S A - - L A Thelotrema sp.3 T C MC S A - - L A Trichothelium horridulum (Mull. Arg.) R. Sant. T C MC S P M - D N Trypethelium sp. Usnea sp.1 Usnea sp.2 Usnea sp.3 T C MC S P SP - L N C F M N L A C F M N L A C F M N L A Usnea sp.4 C F M N L A Yoshimuriella dissecta (Sw.)B. Moncada & Lücking C FB M AS A,I SP - D N Yoshimuriella subdissecta (Nyl.)B. Moncada & Lücking C FB M AS A,I SP - D N 144

156 Photobiont type: C=Chlorococcoid; CY=Cyanobacteria; T=Trentepholia; Growth forms: C= Crustose; CP=Crustose with prothallus; FB= Foliose broad lobed; FN= Foliose narrow lobed; FP= Foliose placodiod; FL=Filamentose; F=Fruticose, G=Gelatinose; S=Squamulose; Size: M=Macrolichens; MC=Microlichens; Reproduction type: A=Asexual; S=Sexual; AS=Asexual and sexual; N=None; Reproductive structure: A=Apothecia; I=Isidia; L=Lirellae; P=Perithecia; S=Soredia; Ascospore septation: S=Simple; S=Septate; M=Muriform; Ascopore size: S=Small (<100 µm); M=Medium (>100 µm); L=Large ( >500 µm); Thallus colour: D=Dark; L=Light; Chemistry: A=Acids; O = Other compounds; N= No compounds. 145

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158 CAPÍTULO IV / CHAPTER IV Lichen diversity in tropical dry forest is highly influenced by the host tree traits including tree species Ángel Benítez 1, María Prieto 2 and Gregorio Aragón 2 1 Sección de Sistemáticay Diversidad, Departamento de Ciencias Naturales, Universidad Técnica Particularde Loja, San Cayetano s/n, Loja, Ecuador 2 Área de Biodiversidad y Conservación, ESCET, Universidad Rey Juan Carlos, Móstoles, E-28933, Madrid, España. Benítez, Á., Prieto, M., & Aragón, G. Manuscrito inédito 147

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160 Abstract Tropical dry forests have been recognized as one of the most threatened ecosystems in the world due to deforestation. These ecosystems, can harbor high levels of endemisms of epiphytes, which play a major role in the functioning of the forests. Bryophytes and lichens constitute an important fraction of the epiphytes. These poikilohydric organisms respond drastically to increasing disturbance that is strongly linked to humidity and light availability. We hypothesized that richness and species composition would be related to differences in forest structure (e.g. canopy openness) promoted by deforestation, and by host tree characteristics, due to the fact that dry forests generally have poor microclimatic stratification and low diversity of tree species. In this study, we assessed the composition and richness of epiphytes (lichens and bryophytes) on the trunks of 513 trees in undisturbed and disturbed forests of southern Ecuador. Diversity and richness were related whit canopy cover, mean tree diameter and richness of trees. Thus, epiphytic was highly correlated with characteristics of the host trees as bark texture, tree diameter and tree species. We concluded that epiphytic communities (lichens and bryophytes) in seasonal dry tropical forests of Ecuador are limited by host traits, and particularly by host tree species and substrate quality. Keywords: Diversity, dry forests, Ecuador, forest disturbance, host traits, bark texture, lichens. 149

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162 Introduction Despite tropical dry forests habours high levels of endemicity they are one of the most threatened ecosystems in the world (Janzen 1988; Dinerstein et al., 1995; Fajardo et al., 2005; Miles et al., 2006). These forests have been intensively deforested over time, and a large proportion of the original woodlands has been transformed into isolated fragments, pastures and croplands, due to timber or fuelwood extraction and cattle grazing (Kalacska et al., 2005; Fajardo et al., 2005; Leal-Pinedo & Linares- Palomino 2005). In Ecuador, dry forests are located in the Tumbesian region (Dinerstein et al., 1995) which is recognized as a hotspot (Janzen 1988; Linares- Palomino et al., 2010). At present, annual deforestation of these forests are near ca. 2% with only 5% of the 55,000 km 2 of the remaining dry forests being currently protected (Linares-Palomino et al., 2010; Sierra 2013). Dry forests have received little attention compared with other types of forests, and studies analyzing the disturbance effects are still scarce (Gillespie et al., 2000; Avila-Cabadilla et al., 2009; Espinosa et al., 2011; de la Rosa-Manzano et al., 2014). Although these forests have a lower vascular epiphytic diversity than tropical rain forests (Gentry & Dodson 1987; Werner & Gradstein 2009; Vergara-Torres et al., 2010; de la Rosa-Manzano et al., 2014) they can host hight levels of epiphytic endemisms (Werner 2008). Cryptogamic communities (i.e., lichens and bryophytes) are important components of the epiphytc diversity and they play important roles in the functioning of these ecosystems (Holz & Gradstein 2005; Mandl et al., 2010). Understanding how forest disturbance affect epiphytes is critical for the conservation of biodiversity in these threatened ecosystems. Several studies showed that forest disturbance greatly affects the diversity of epiphytic communities in tropical rain forests (Barthlott et al., 2001; Acebey et al., 2003; Wolf 2005; Gradstein 2008; Gradstein & Sporn, 2010), including non-vascular epiphytes (bryophytes and lichens) (Werner & Gradstein 2009; Benitez et al., 2015). However very little is known about the effects of disturbance on the epiphytic diversity in dry forests (Werner & Gradstein 2009). Bryophytes and lichens are strongly linked to humidity, solar irradiance and temperature conditions due to their physiology (Nash 1996; Green et al., 2008; Kranner et al., 2008). Therefore, changes in the microclimatic conditions produced by forest logging (e.g. humidity and light availability) affect the composition of lichens and 151

163 bryophytes (Nöske et al., 2008; Gradstein 2008; Gradstein & Sporn 2010; Normann et al., 2010; Benitez et al., 2015). In comparison with wet forests, dry forests are less complex in terms of tree diversity and structure (Murphy & Lugo 1986), with lower and more open canopies, resulting in poor microclimatic stratification (Graham & Andrade 2004). Thus, epiphytes generally show little or no vertical stratification due to the fact that the gradients in humidity and light are low (Benzing 1990; Graham & Andrade 2004). Because of this, it is expected that epiphytes in dry forests could be more tolerant to the microclimatic changes produced by canopy openness caused by disturbance than in more humid forests. Direct consequences of forest disturbance include the removal of host tree species which have immediate and negative effects on the persistence of bryophytes and lichens (Gradstein 2008). This process could affect more severely those species which grow speciphically in selected trees with particular traits (e.g. tree size, bark texture and depth, ph), which could limit the epiphytic diversity and species distribution (McGee & Kimmerer 2002; Cáceres et al., 2007; Fritz et al., 2008; Hirata et al., 2009; Nascimbene et al., 2009; Aragón et al., 2010; Király et al., 2013; Rosabal et al., 2013; Benitez et al., 2015; Li et al., 2015). Most studies have found little or no evidence between host trees and epiphytic diversity in tropical forests (Sipman & Harris 1989; Cornelissen & ter Steege 1989; Cáceres et al., 2007; Soto-Medina et al., 2012; Rosabal et al., 2013). However, the current knowledge cannot be extrapolated to those communities inhabiting dry forests, due to its peculiar characteristics: (1) strong seasonality of abiotic conditions related with water availability (Mooney et al., 1995), (2) forest structure with lower and more open canopies (Graham & Andrade 2004), and (3) low diversity of tree species (Murphy & Lugo 1986; Gentry 1995). In relation with these characteristics, host species and the associated traits may be important factors influencing epiphytic communities in tropical dry forests. Based on these premises, the goal of this study was to analyze which factors influence cryptogamic epiphytic communities under contrasting levels of disturbance in dry forests. Thus, we compared the composition and richness of epiphytic communities along a disturbance gradient in dry forests. We hypothesized that epiphytic diversity and composition would be affected by differences in forest structure (e.g., canopy openness) and microclimate caused by forest logging. We also studied the effects of the host traits including host tree species, tree size and bark texture on the diversity of epiphytic communities. 152

164 Methods Study area The study was conducted in the Ecological Reserve Arenillas (REA), located in El Oro province (southwest Ecuador, Figure 1). The Reserve comprises approximately 17 ha (Figure 1), with a transitional vegetation of dry deciduous forests and dry shrubs in the lowlands. The altitude ranged from m a.s.l., with average temperature between C with a maximum variation of 3.4 C between the coldest and warmest months (Espinosa et al., 2015). The climate is characterized by two distinct seasons, the rainy and dry seasons with an average precipitation of 515 mm and 152 mm, respectively (weather station Huaquillas for a recorded period of 45 years, ) Figure 1. Study area in Ecological Reserve Arenillas (REA) of southern Ecuador showing the location of the four tropical dry forest sites. DF1 and DF2=undisturbed forest; DF3 and DF4=disturbed forest. 153

165 Field work was carried out in four deciduous forests, at m a.s.l. We selected two well-preserved forests within a protected area and two disturbed forests in managed zones of the protected area. The establishment of military detachments, selective logging, timber extraction and livestock grazing has been the main human activities in these zones, although at present, only livestock grazing impacts have been observed in the managed forests. The most conspicuous tree species occurring in wellpreserved forests are Bursera graveolens (Kunth) Triana & Planch. (Burseraceae), Cochlospermum vitifolium (Willd.) Spreng. (Cochlospermaceae), Cynophalla mollis (Kunth) J. Presl (Capparaceae), Eriotheca ruizii (K. Schum.) A. Robyns (Malvaceae), and Tabebuia chrysantha G. Nicholson (Bignoniaceae), together with several shrubs as Malpighia emarginata L. (Malpighiaceae) and several Croton species. Disturbed forests are characterized by having less shrub vegetation and tree density than the well-preserved forests and by the presence of scattered trees which established as isolated trees prior to abandonment of use (e.g. selective logging or timber extraction), thus their architecture is resembled that of trees in undisturbed forest (Werner & Gradstein 2009). The dominant tree species here were C. mollis, T. chrysantha and Ziziphus thyrsiflora Benth. (Rhamnaceae). Sampling design and data collection Four plots of m (400 m 2 ) were randomly selected within each forest. The distance between plots within a forest was over 100 m. Within each plot, all trees and shrubs having a diameter above 5 cm were identified and the diameter at breast height (DBH) was measured. For these shrubs and trees, lichens and bryophytes were sampled using four cm and cm grids, respectively. Sampling cuadrats were established on each tree at two different heights (0 100, and cm) at the northern and southern sides (a total of four samples per tree). We determined the presence and coverage of epiphytic lichens and bryophytes for a total of 513 host trees. In addition, we measured the elevation (m asl), slope ( ), aspect (cosine transformed), canopy openness (%) and mean tree diameter (MTD, cm) for each plot as a proxy for the stand forest structure. For species identification, we used general (Brodo et al., 2001, Gradstein et al., 2001; Nash et al., 2002, 2004, 2007) and specific keys (e.g. Egea & Torrente 1993; Tehler 1997; Rivas-Plata et al., 2006; Cáceres 2007; Aptroot et al., 2008; Lücking et al., 2008, 2009; Rivas-Plata et al., 2010; Aptroot 2012; Aptroot et al., 2014). The total species richness was defined as the total number of species found in the four grids per tree. For lichen composition, we calculated the mean estimated cover of each species in the four sample grids. 154

166 Light conditions were recorded by measuring canopy openness (%) using sixteen digital hemispherical photographs by plot. The distance between photographs within a plot was 5 m. Digital photographs were always taken on overcast days and at breast height (1.3 meter height), using a horizontally leveled digital camera (Nikon Coolpix 4500) aimed at the zenith and to the north, using the fish-eye lens FCE8, Nikon. Photographs were analyzed using the free software Gap Light Analyzer ver. 2.0 (Frazer et al., 1999). Host tree traits Measured host tree parameters included tree species, tree diameter (DBH), tree slope ( ), tree aspect (cosine transformed), bark depth (mm) and bark texture. Bark texture was assessed in four categories: 1 = Completely smooth, 2 = Smooth without marked fissures, 3= Rough with fissures and 4 = Fissured with deep crevices (Mistry 1998; Mistry & Berardi 2005; Vergara-Torres et al., 2010). Data analyses Alpha diversity was calculated using the Simpson diversity and the Shannon diversity indices. The Simpson index is considered as a measure of species dominances, and the Shannon index was based on the assumption that individuals were randomly selected and that all species were represented in the sample (Magurran 2004). This diversity indices were calculated for each tree and plot with PRIMER v software. The effect of environmental variables on the richness and diversity of epiphytes was modelled by fitting Generalized Mixed Linear Models (GLMMs) at the tree and plot level (McCullagh & Nelder 1989). Factors at tree and plot level were used as predictors: canopy openness, slope, aspect, bark depth, tree diameter (DBH), mean tree diameter (MTD) and tree richness. Predictors were included as explanatory variables (fixed factors), and forest and plot were included as random sources of variation. Effects of random factors were tested using the Wald Z-statistic test. We fitted the mixed models using a Poisson distribution. All GLMM computations were performed using SAS (GLIMMIX ver. 8 for SAS/STAT). In order to prevent multicolinearity problems of some host traits (bark texture and depth) were not included in the models because they showed high colinearity with bark depth. 155

167 The effects of host tree species on the bryophyte and lichen richness were analyzed using generalized linear models (GLM; McCullagh & Nelder 1989), assuming Poisson errors for the response variables. In this model, only woody tree species were considered as potential host trees (Table 1), since they are the most conspicuous and numerous tree species in the studied dry forests. In addition, the majority of cryptogams (91 % of the species, 112 species) preferred this small group of host trees, leading us to adjust a dataset of 112 lichen and bryophyte species and 336 trees belonging to 8 species. To test whether the disturbance level were related with composition of epiphytic species and to detect the effects of forest, plot and host variability, we performed a three-factor permutational multivariate analysis of variance (PERMANOVA) (Anderson et al., 2008). In this analyses, the experimental design included three factors: forest (4 levels, fixed factor), plot (4 levels, random factor nested within forest) and host tree (22 levels, random factor nested within plot and forest) and the trees constituted the replicate (N=513). The cover data (cover percentage of each lichen per tree) were log10 (x+1) transformed to account for contributions by both rare and abundant taxa. Non-metric multidimensional scaling (NMDS) was performed to detect the main factors influencing the epiphytic composition. We used the Bray Curtis dissimilarity distance to compute the resemblance matrix between trees. The results were plotted in a NMDS ordination diagram. Values of the relative species cover and environmental and tree variables were then fitted into the first two axes of the NMDS ordination. Squared correlation coefficients (r 2 ) and empirical p-values (p) were calculated for these linear fittings. Ordination was performed with package vegan (Oksanen et al., 2013) in the R environment (R Development Core Team, 2011). Results A total of 123 epiphytic species (122 lichens and one bryophyte) were recorded and collected in 513 trees (Appendix A). The highest epiphytic richness was found in non-disturbed forests (Fig. 2), which included 28 exclusive species (Appendix A). The more frequent lichen species were Coniocarpon cinnabarinum, Leucodecton occultum, Pseudopyrenula subnudata and Syncesia leproloba. Tree species like Cochlospermum vitifolium and Eriotheca ruizii showed the highest epiphytic richness (Table 1), and the highest values for estimated richness (Chao 2). 156

168 100 A B DF1 DF2 DF3 DF4 Figure 2. Species richness of epiphytic lichens and bryophytes in the two studied dry forest types (A) Forest level and (B) Plot level, with maximum, minimum and median richness values and lower and upper quartiles. DF1 and DF2=undisturbed forest; DF3 and DF4=disturbed forest. Axis X, epiphytic species richness; Axis Y, forest type. Table 1. Characteristics of woody tree species selected as potential host trees. Species richness of bryophytes and lichens in the host trees is indicated as observed species (OS). Chao 2 estimates of total richness are shown in parenthesis. MTD: mean tree diameter; SE: Standard error. Tree number: number of samples trees per species. Hots Bark texture Tree number MTD (cm, ±SE) OS (Chao 2; ±SE) Albizia multiflora (Kunth) Rough with Barneby & J.W. Grimes fissures (±4.0373) 28 (32; ±4.12) Bursera graveolens (Kunth) Completely Triana & Planch. smooth (±6.5278) 33 (61; ±19.83) Smooth without Cochlospermum vitifolium marked 24.81(± (Willd.) Spreng. fissures 29 ) 53 (102; ±34.04) Cynophalla mollis (Kunth) J. Rough with Presl fissures (±4.2193) 38 (42; ±4.26) Eriotheca ruizii (K. Schum.) A. Robyns Completely smooth (± ) 58 (87; ±17.6) Fissured with Geoffroea spinosa Jacq. deep crevices 41 (±7.1152) 42 (75; ±21.43) Tabebuia billbergii (Bureau & Fissured with K. Schum.) Standl. Tabebuia chrysantha (Jacq.) G. Nicholson Ziziphus thyrsiflora Benth. deep crevices 63 (±9.9655) 45 (57; ±10.07) Fissured with deep crevices 20 (± ) 40 (52; ±8.6) Rough with fissures (±4.5695) 28 (36; ±6.87) 157

169 The analysis showed that variables at tree level (i.e. host traits), had a significant effect on species richness (bark depth and DBH) and on the species diversity (bark depth, tree species richness and canopy openness) (Table 2). At plot level, canopy openness was the main factor affecting species richness and diversity (Table 2). We also found that the mean tree diameter (MTD) and tree richness had a significant effect on diversity and epiphytic richness respectively (Table 2). The random variable forest was not significant in any case. Table 2. Results of the generalized linear mixed models of community traits at tree and plot levels. DBH= tree diameter, MTD= mean tree diameter, Coef. = coefficient, SE = standard error. Tree level Coef. (SE) F-value P-value Richness DBH (0.0229) Tree slope (0.0159) Bark depht (0.7270) 29.7 < Canopy openess (0.0596) Tree aspect (0.6346) Tree richness (0.2147) Shannon index DBH (0.0025) Tree slope (0.0017) Bark depht (0.0769) < Canopy openess (0.0065) Tree aspect (0.0683) Tree richness (0.0228) Simpson inverse index DBH (0.0027) Tree slope (0.0019) Bark depht (0.0850) < Canopy openess (0.0074) Tree aspect (0.0771) Tree richness (0.0259) Plot level Richness Canopy openess (0.0049) MTD (0.0098) Tree richness (0.0169) Shannon index Canopy openess (0.0025) MTD (0.0052) Tree richness (0.0097) Simpson inverse index 158

170 Canopy openess (0.0104) MTD (0.0228) Tree richness (0.0390) P-values < 0.05 are considered significant and marked in bold. Models between epiphytic richness and host tree species showed that tree species is a relevant predictor of species richness (Table 3). The tree species Cochlospermum vitifolium had the highest coefficient, followed by Eriotheca ruizii and Bursera graveolens, while the coefficients for Tabebuia billbergii and Tabebuia chrysantha had the lowest values (Table 3). Table 3. Results of the generalized linear models between epiphyte richness and host tree species. Coef. = coefficient, SE = Standard error. Variable Coef. SE P-value Species Bursera graveolens < Cochlospermum vitifolium < Cynophalla mollis Eriotheca ruizii < Geoffroea spinosa Tabebuia billbergii Tabebuia chrysantha Ziziphus thyrsiflora P-values < 0.05 are considered significant and marked in bold. Multivariate statistical analyses showed that epiphytic composition was structured according to the different spatial scales, and a large component of variation was associated with the tree level, followed by forest and plot (Table 4). Table 4. Results of three-factor PERMANOVA analysis of species composition by forest, plot and host tree. df= degrees of freedom, MS= mean sum of squares, Pseudo- F= F value by permutation, CV=coefficient of variation. Source df MS Pseudo-F P CV (%) Forest Plot(Forest) Host tree Error Host traits showed a significant relationship with the NMDS ordination axes (Table 5). Thus, correlations were strong with host tree species, bark texture and depth and DBH on the two axes of the species ordination (Table 5). 159

171 Table 5. Squared correlation coefficients (r 2 ) of environmental categorical factors and current environmental vectors fitted on the first two axes of the NMDS ordination. Significant values (p < 0.05) with strong correlations are in bold. Vectors NMDS1 NMDS2 r 2 P-value Mean tree diameter < Slope Bark depth < Aspect Altitude Canopy openess Plot slope Plot aspect Plot DBH Tree abundance per plot Tree richness per plot Tree diversity per plot (Shannon index) Tree diversity per plot (Simpson index) Plot Factors Disturbance Disturbed Undisturbed Bark texture < Fissured with deep crevices Rough with fissures Smooth without fissures Completely smooth Host tree species < Albizia multiflora Bursera graveolens Cochlospermum vitifolium Cynophalla mollis Eriotheca ruizii Geoffroea spinosa Tabebuia billbergii Tabebuia chrysantha Ziziphus thyrsiflora

172 Consistently, host tree species was the most relevant predictor of epiphytic communities of tropical dry forests as supported by Figure NMDS Axis 2 Figure 3. Non-metric multidimensional scaling analysis of species composition for the samples (host trees) in the four studied dry forests. Albizia multiflora ( -0.5 ); Bursera graveolens ( ); Cochlospermum vitifolium ( ); Cynophalla mollis ( ); Eriotheca ruizii ( ); Geoffroea spinosa ( ); Tabebuia billbergii ( ); Tabebuia chrysantha ( ); Ziziphus thyrsiflora ( ) NMDS Axis 1 Discussion Our results demonstrated that deforestation in tropical dry forests had a negative impact on epiphytic diversity, which was related to changes in forests structure (i. e. canopy openness), and particularly with the removal of potential host trees. Thus, host traits (i.e., tree species, bark depth and mean tree diameter), proved to be determinats for epiphytes due to the fact that the majority of epiphytes preferred a small group of host species with specific characteristics. 161

173 The negative correspondence found between the canopy openness and epiphyte richness is a general phenomenon in tropical forests (Gradstein 2008; Li et al., 2013; Benítez et al., 2012; 2015). Werner & Gradstein (2009) pointed out that disturbance in tropical dry forests is a cause for the loss of epiphytic richness which decreases together with canopy cover, although these results are restricted to monospecific forests of Acacia macracantha Willd. The studies centered in other types of forests (i.e. montane rainforests) show that forest disturbance creates a drier microclimate due to canopy disruption that affects negatively to the diversity of nonvascular epiphytes (Nöske et al., 2008; Li et al., 2013; Benitez et al., 2015). Deforestation not only produces canopy disruption but also loss of tree species diversity. In the studied disturbed forests, shrub vegetation is absent and there is a lower diversity and abundance of potential host trees (e.g. Cochlospermum vitifolium and Eriotheca ruizii). Our results suggest that the diversity in the forest community helps to maintain epiphyte richness in lowland dry forests. Several studies in temperate and boreal forests have shown that the diversity of trees is a key factor for epiphyte richness which is related with host preference (Nascimbene et al., 2009; Király et al., 2013). In contrast, this specifity between epiphytes and the tree species has been rarely found in tropical rain forests, which might be related to the high tree species diversity, complexity of forest structure, humus and moss cover on the bark surface or stochastic effects of species dispersion (Sipman & Harris, 1989; Cáceres et al., 2007; Gradstein & Culmsee, 2010; Soto-Medina et al., 2012). However, the seasonal dry tropical forests are characterized by low species tree diversity (Murphy & Lugo 1986; Gentry 1995), caused by the occurrence of extensive arid periods with high light levels (Werner & Gradstein 2009). Additionally, humus layer and bryophyte cover and diversity are generally low or absent in these forests (Cornelissen & Ter Steege 1989, Gradstein et al., 2001), which, together with the cited characteristics, could drive epiphytes to select specific hosts trees. In this study, much of the variability of the lichen species richness and composition was explained by the host tree species characteristics, emphasizing the importance of tree species and the strong host preference of non-vascular epiphytes in dry forests. This idea is supported by several studies that found relation between host tree species and diversity of epiphytes (Löbel et al., 2006; Hirata et al., 2009; Vergara- Torres et al., 2010; Király & Ódor 2010; Király et al., 2013; Li et al., 2015). 162

174 Tree characteristics affecting the richness and composition of epiphytes are related with substrate quality (i.e. bark texture and depth), which depends on the host tree species. Thus, host trees with a smooth bark (E. ruizii and C. vitifolium) harboured higher species richness than trees with fissured bark (e.g. Cynophalla mollis), which were much poorer in epiphyte species. In this regard, Löbel et al. (2006) and Rosabal et al. (2013) found a negative correlation between bark roughness and species richness of lichens (although only for those with a crustose growth form). Following this pattern, host trees of E. ruizii and B. graveolens with smooth bark hosted a different epiphytic community than C. mollis and T. billbergii trees with a fissured bark. In accordance, Fritz & Brunet (2010) have shown that several crustose lichens were associated with mature trees with a smooth bark, and therefore limited primarily by the availability of the bark substrate. We observed that lichens with a crustose growth form were dominant in our study and they were better associated with hosts of smooth bark, due to the fact that they have thin thalli and grow directly on the surface of the substrate attached through the medullary hyphae (Büdel & Scheidegger 2008). However, other bark characteristics of host trees such as bark stability, water-capacity and ph are considered important factors in the distribution and establishment of epiphytes communities (Löbel et al., 2006; Cáceres et al., 2007; Gradstein & Culmsee 2010; Soto-Medina et al., 2012; Rosabal et al., 2013) On the other hand, another factor affecting epiphytic species richness and composition is the tree diameter (DBH). Thus, forest disturbance may also have immediate negative effects on the persistence of non-vascular epiphytes due to the removal of large trees. Several studies found that old and big trees are highly important for the diversity of epiphyte assemblages (Fritz et al., 2008; Lie et al., 2009; Benitez et al., 2015). However, in this study tree diameter had a negative effect on species richness; this could be explained by the presence of large trees in the disturbed forests wich host low epiphytic diversity. We found also that tree diameter explained a large percentage of the variation in epiphyte species composition. Other studies have also found relation between epiphytic composition and tree diameter or tree age (Nascimbene et al., 2009; Marmor et al., 2011; Soto-Medina et al., 2012; Rosabal et al., 2013; Benitez et al., 2015). We therefore conclude that tropical forest disturbance reduces cryptogamic epiphytic diversity. Particularly, by the removal of host trees. Epiphytic species loss is most severe in disturbed forest due to loss of potential host trees such as Eriotheca ruizii and Cochlospermum vitifolium that maintain high species richness. Disruption of 163

175 the canopy leads to microclimatic changes that affect species richness of epiphytic lichens. Therefore host preference and change in the tree species composition play an important role in epiphytic communities of seasonal tropical dry forests. Consequently, only the protection of remnants of undisturbed dry forest characterized by potential host trees might help to preserve a rich and diverse community of epiphytic lichens. Acknowledgments: Financial support for this study was granted by the Universidad Técnica Particular de Loja (PROY_CCNN_941), the Secretaría Nacional de Educación Superior, Ciencia, Tecnología e Innovación of Ecuador and the Ministerio de Ciencia e Innovación of Spain (project EPICON, CGL ). We thank A. Arévalo, E. Gusmán, F. Gaona and G. Cango for their help with fieldwork and Ministerio del Ambiente del Ecuador by providing access to the studied areas. References Acebey, A., Gradstein, S. R. & Krömer, T. (2003). Species richness and habitat diversification of bryophytes in submontane rain forest and fallows of Bolivia. Journal of tropical ecology, 19(01): Anderson, M.J., Gorley, R.N. & K.R. Clarke. (2008). PERMANOVA + for PRIMER: Guide to Software and statistical Methods. PRIMER-E. Plymouth, UK. Aptroot, A. (2012) A world key to the species of Anthracothecium and Pyrenula. The Lichenologist, 44(1): Aptroot, A., Lücking, R., Sipman, H.J.M., Umaña, L. & Chaves, J.L. (2008). Pyrenocarpous lichens with bitunicate asci. A first assessment of the lichen biodiversity inventory in Costa Rica. Bibliotheca Lichenologica, 94: Aptroot, A., Menezes, A. A., Xavier-Leite, A. B., dos Santos, V. M., Alves, M. M. E., & da Silva Cáceres, M. E. (2014). Revision of the corticolous Mazosia species, with a key to Mazosia species with 3-septate ascospores. The Lichenologist, 46 (4): Aragón, G., López, R., & Martínez, I. (2010). Effects of Mediterranean dehesa management on epiphytic lichens. Science of The Total Environment, 409(1): Avila-Cabadilla, L. D., Stoner, K. E., Henry, M., & Añorve, M. Y. A. (2009). Composition, structure and diversity of phyllostomid bat assemblages in different successional stages of a tropical dry forest. Forest Ecology and Management, 164

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180 Mooney H. A. & Medina E. (Eds.), Seasonally dry tropical forests. Cambridge University Press, Cambridge, pp Murphy, P. G., & Lugo, A. E. (1986). Ecology of tropical dry forest. Annual review of ecology and systematics, Nascimbene, J., Marini, L., Motta, R., & Nimis, P. L. (2009). Influence of tree age, tree size and crown structure on lichen communities in mature Alpine spruce forests. Biodiversity and Conservation, 18(6): Nash III, T. H., Gries, C. & Bungartz, F. (2007). Lichen Flora of the Greater Sonoran Desert Region, vol. 3. Lichens Unlimited, Tempe, Arizona, 567 pp. Nash III, T. H., Ryan, B. D., Gries, C. & Bungartz, F. (2002). Lichen Flora of the Greater Sonoran Desert Region, vol. 1. Lichens Unlimited, Tempe, Arizona, 532 pp. Nash III, T.H., Ryan, B.D., Diederich, P., Gries, C. & Bungartz, F. (2004). Lichen Flora of the Greater Sonoran Desert Region, vol. 2. Lichen Unlimited: Tempe, Arizona 742 pp. Nash, T. H. (1996). Lichen biology. Cambridge University Press, 303 pp. Normann, F., Weigelt, P., Gehrig-Downie, C., Gradstein, S. R., Sipman, H. J., Obregon, A., & Bendix, J. (2010). Diversity and vertical distribution of epiphytic macrolichens in lowland rain forest and lowland cloud forest of French Guiana. Ecological Indicators, 10(6): Nöske, N. M., Hilt, N., Werner, F. A., Brehm, G., Fiedler, K., Sipman, H. J., & Gradstein, S. R. (2008). Disturbance effects on diversity of epiphytes and moths in a montane forest in Ecuador. Basic and Applied Ecology, 9(1): Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., & Oksanen, M. J. (2013). Package vegan. Community ecology package, version, 2(9). Rivas-Plata, E., Lücking, R., Aptroot, A., Sipman, H.J.M., Chaves, J.L., Umaña, L. & Lizano, D. (2006). A first assessment of the Ticolichen biodiversity inventory in Costa Rica: the genus Coenogonium (Ostropales: Coenogoniaceae), with a worldwide key and checklist and a phenotype-based cladistic analysis. Fungal Diversity, 23: Rivas-Plata, E., Lücking, R., Sipman, H. J., Mangold, A., Kalb, K., & Lumbsch, H. T. (2010). A world-wide key to the thelotremoid Graphidaceae, excluding the Ocellularia-Myriotrema-Stegobolus clade. The Lichenologist, 42: Rosabal, D., Burgaz, A. R., & Reyes, O. J. (2013). Substrate preferences and phorophyte specificity of corticolous lichens on five tree species of the montane rainforest of Gran Piedra, Santiago de Cuba. The Bryologist, 116(2):

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182 Appendix A. Number of trees on which each species appears in the four forests. Asterisks denotes exclusive species per forest. Taxa DF1 DF2 DF3 DF4 Bryophytes Cololejeunea minutissima ssp. myriocarpa (Nees & Mont.) R.M. Schust Lichens Arthonia aff. antillarum (Fée) Nyl. 5* Arthonia antillarum (Fée) Nyl Arthonia aff. conferta (Fee) Nyl. 1* Arthonia elegans (Ach.) Almq. 4 1 Arthonia pruinata (Pers.) Steud. ex A.L. Sm Arthonia sp 1 1 Bacidia sp Bacidia sp2 1* Bacidia sp3 2 8 Bactrospora denticulata (Vain.) Egea & Torrente 8* Bactrospora myriadea (Fée) Egea & Torrente. 2* Bathelium degenerans (Vain.) R. C. Harris Buellia sp Caloplaca sp Caloplaca wrightii (Willey) Fink Coccocarpia pellita (Ach.) Müll. Arg. 1* Coenogonium pineti (Ach.) Lücking & Lumbsch 4 4 Coniocarpon cinnabarinum DC Chapsa dilatata (Müll. Arg.) Kalb 2* Chapsa diploschistoides (Zahlbr.) Frisch 2 16 Chapsa sp 1* Cresponea flava (Vainio) Egea & Torrente Cryptothecia striata Thor 1 1 Chrysothrix sp Chrysothrix xanthina (Vain.) Kalb Dirinaria aegialita (Afz.) B. Moore 4* Dirinaria aff. aegialita (Afz.) B. Moore 4 2 Dirinaria aff. confluens (Fr.) D. D. Awasthi. 2 8 Dirinaria applanata (Fée) D. D. Awasthi 1 2 Dirinaria confluens (Fr.) D. D. Awasthi. 1 1 Dirinaria papillulifera (Nyl.) D. D. Awasthi Dirinaria picta (Sw.) Clem. & Shear Dirinaria sp 1* Diplolabia afzelii (Ach.) A. Massal. 2* Enterographa compunctula (Nyl.) Redinger 18 1 Enterographa quassiaecola Fée 1 2 Fibrillithecis halei (Tuck. & Mont.) Mangold

183 Fissurina incrustans Fée 1* Fissurina nitidescens (Nyl.) Nyl Fissurina egena (Nyl.) Nyl. 3 1 Fissurina sp 1 4 Glyphis scyphulifera (Ach.) Staiger Glyphis cicatricosa Ach Graphis aff. dendrogramma Nyl. 5* Graphis aff. subcontorta (Müll. Arg.) Lücking & Chavez 1 1 Graphis anfractuosa (Eschw.) Eschw Graphis argentata Lücking & Umaña Graphis dendrogramma Nyl Graphis leptoclada Müll. Arg. 12* Graphis subcontorta (Müll. Arg.) Lücking & Chavez Graphis caesiella Vain. 2* Graphis sp Gyalidea sp 4 6 Haematomma aff. nicoyense Nelsen, Lücking & Chaves 1* Helminthocarpon leprevostii Fee. 3* Herpothallon sp Hyperphyscia adglutinata (Flörke) 1 2 Lecanographa laingiana Diederich, Egea & Sipman Lecanographa illecebrosula (Müll. Arg.) Egea & Torrente. 1* Lecanographa lyncea (Sm.) Egea & Torrente Lecanora chlarotera Nyl. 1 3 Lecanora helva Stizenb Lecanora sp Lecanora sp 2 4* Lecanora sp 3 1* Leptogium cyanescens (Pers.) Körb. 1* Leucodecton occultum (Eschw.) A. Frisch Lithothelium illotum (Nyl.) Aptroot Mazosia carnea (Eckfeldt) Aptroot & M. Cáceres 8 1 Megalospora sulphurata var. sulphurata Meyen 1* Melaspilea sp 1* Mycoporum eschweileri (Müll. Arg.) R. C. Harris 1 1 Ocellularia sp 1 4 Opegrapha aff. vulgata (Ach.) Ach. 6* Opegrapha difficilior Nyl Opegrapha trilocularis Müll. Arg Ophegrapha sp 6* Parmotrema exquisitum (Kurok.) DePriest & B. W. Hale Pertusaria texana Mull. Arg. 3* Pertusaria sp 1 1* Pertusaria sp Phaeographis punctiformis (Eschw.) Müll. Arg. 1* 172

184 Phaeographis decipiens Müll. Arg. 1* Phaeographis inusta (Ach.) Müll. Arg. 7 2 Phaeographis subtigrina (Vainio) Zahlbr. 4 2 Phaeographis intricans (Nyl.) Vain Phaeographis lobata (Eschw.) Müll. Arg. 1* Phaeographis brasiliensis (A. Massal.) Kalb & Matthes-Leicht Phaeographis sp 1 1* Phaeographis sp 2 1* Porina nucula Ach. 1* Porina tetracerae (Afz. in Ach.) Müll. Arg Physcia crispa Nyl Physcia endochrysea Kremp Physcia sorediosa (Vain.) Lynge Phyllopsora sp Polymeridium subcinereum (Nyl.) R.C. Harris 25 1 Pyrenula erumpens R. C. Harris Pyrenula immissa (Stirt.) Zahlbr Pyrenula ochraceoflava (Nyl.) R.C. Harris Pyrenula psoriformis Zahlbr. 2* Pyrenula subcongruens Müll.Arg Pseudopyrenula diluta (Fée) Müll. Arg Pseudopyrenula subnudata Müll.Arg Pyxine cocoës (Sw.) Nyl Ramalina darwiniana var. darwiniana Aptroot & Bungartz 1 3 Ramonia valenzueliana (Mont.) Stizenb. 1* Rinodina sp Sarcographa tricosa (Ach.) Müll. Arg Schismatomma spierii Aptroot & Sparrius Stigmatochroma gerontoides (Stirt.) Marbach 1* Stirtonia dubia A. L. Sm. 5* Stirtonia ramosa Makhija & Patw Stirtonia sp 15 2 Syncesia effusa (Fée) Tehler Syncesia glyphysoides (Fée) Tehler 2* Syncesia leprobola Nyl. ex Tehler Syncesia farinacea (Fée) Tehler Syncesia graphica (Fr.) Tehler Tephromela atra (Huds.) Hafellner Thelotrema sp 1* Trypethelium eluteriae Spreng

185 174

186 CAPÍTULO V / CHAPTER V Additions to the bryophyte flora of Ecuador 2 Adiciones a la Flora de Briófitas del Ecuador 2 Angel Benitez 1, Robbert Gradstein 2, Maria Prieto 3, Gregorio Aragón 3, Alejandra Moscoso 4 & Michael Burghardt 4 1 Departamento de Ciencias Naturales-Departamento de Sistemática y Diversidad- Herbario HUTPL, Universidad Técnica Particular de Loja, San Cayetano s/n, Loja, Ecuador. 2 Muséum National d Histoire Naturelle, C.P. 39, 57 rue Cuvier, Paris cedex 05, France. 3 Área de Biodiversidad y Conservación, ESCET, Universidad Rey Juan Carlos, Móstoles, E-28933, Madrid, España. 4 Escuela de Ciencias Biológicas, Pontificia Universidad Católica del Ecuador, Quito, Ecuador. Benitez, A., Gradstein, R., Prieto, M., Aragón, G., Moscoso, A., & Burghardt, M. (2012). Tropical Bryology 34: Notothylas vitalii Udar & D.K. Singh 175

187 176

188 Abstract Ecuador has a very diverse bryophyte flora with about 950 species of mosses and 700 of liverworts and hornworts. Nevertheless, the distribution of the species within the country remains incompletely explored and many species are only known from very few collections. This paper presents new additions to the liverwort and hornwort flora of Ecuador. The hornwort Notothylas vitalii and the liverworts Blepharostoma trichophyllum, Frullania setigera, Isopaches bicrenatus, Platycaulis renifolia and Symphyogyna apiculispina are new to the country, four species are new to southern Ecuador, eighteen are new to the province of Loja, ten are new to Napo, six are new to Pichincha and one species is new to the provinces of El Oro and Carchi respectively. The record of Notothylas vitalii is the first one outside Brazil and constitutes the first record of the genus Notothylas from mainland Ecuador. The rare monospecific genus Platycaulis was previously known only from the type locality in the Venezuelan Andes, and the holarctic Isotaches bicrenatus in the tropics only from two mountains in southeastern Brazil. Several new records were gathered in very humid and bryophyterich, wind-stricken, foggy superpáramo vegetation in the Páramo de la Virgen (Napo) at m. For all species notes on their geographical distribution and habitats in Ecuador as well as their world range are provided. Keywords: Anthocerophyta, Isopaches bicrenatus, Marchantiophyta, Notothylas vitalii, Olgantha, Platycaulis renifolia, new bryophyte records, superpáramo, Triandrophyllum eophyllum. 177

189 178

190 Introducción La flora de briófitas en Ecuador es muy diversa con unas 950 especies de musgos (Churchill et al. 2000) y 700 de hepáticas y antocerotes (León-Yánez et al. 2006, Benitez & Gradstein 2011). Sin embargo, el conocimiento de su biodiversidad es todavía incompleto y poco estudiado. Las colecciones, en su mayoría, provienen de pocas áreas (León-Yánez et al. 2006, Schäfer-Verwimp et al. 2006, Benitez & Gradstein 2011). Recientemente, Benitez & Gradstein (2011) registraron ocho nuevas especies para Ecuador, entre ellas dos para el nuevo mundo, Metzgeria saccata Mitt., Zoopsidella caledonica (Steph.) R.M. Schust. Adicionalmente Gradstein & Schäfer- Verwimp (2012) registraron dos especies, y describen un nuevo taxón para la ciencia, Archilejeunea nebeliana Gradst. & Schäf.-Verw. En esta publicación se presentan nuevas adiciones a la flora de hepáticas y antocerotes del Ecuador. Seis especies son nuevas para el país (Blepharostoma trichophyllum (L.) Dumort., Frullania setigera Steph., Isopaches bicrenatus (Schmidel) H. Buch, Notothylas vitalii Udar & D.K. Singh, Platycaulis renifolia R.M. Schust. y Symphyogyna apiculispina Steph.), cuatro son nuevas para el sur de Ecuador, 18 nuevas para la provincia de Loja, 10 nuevas para la provincia de Napo, seis nuevas para la provincia de Pichincha y una nueva para la provincia de El Oro y otra para la provincia del Carchi. Se confirma la existencia de Anthelia y Lepidozia auriculata Steph. para el país. Hay nuevos registros del superpáramo, en el Páramo de la Virgen al este de Quito, en la provincia de Napo, cerca del borde con la provincia de Pichincha. Aquí, a los m, justo bajo la estación de radio transmisión de la cumbre, se encuentra una vegetación de briofitas terrestres muy rica en especies. La zona corresponde a un superpáramo nublado, muy húmedo, expuesto y azotado por el viento, la vegetación de esta localidad se caracteriza por la presencia de arbustos enanos de Loricaria ilinissae (Benth.) Cuatrec. esparcidos en pendientes pronunciadas. Esta es la localidad tipo del género Olgantha (Schuster 1996; hoy = Triandrophyllum) y de Harpalejeunea grandistipula R.M. Schust. (Schuster 1999; ver también Schäfer-Verwimp et al. 2006), que fueron colectadas aquí por el Dr. Rudoph M. Schuster en Es la única localidad ecuatoriana para los géneros Anthelia, Blepharostoma e Isopaches. Durante una corta visita a esta localidad el 9 de diciembre de 2000 por SRGr, SLY y AM se registraron más de 60 especies, incluyendo cerca de 40 especies de hepáticas y más de 20 especies de musgos. Algunas de estas también 179

191 fueron colectadas en junio de 2008 por uno de los coautores (MB). Las especies de musgos en la comunidad de briofitas terrestres incluyeron a Andreaea rupestris Hedw., Anomobryum julaceum (P. Gaertn., B. Mey. & Scherb.) Schimp., Bartramia mathewsii Mitt., B. potosica Mont., Dicranum frigidum Müll. Hal., Entosthodon jamesonii (Taylor) Mitt., Eobruchia ecuatoriana Steere, Pleurozium schreberi (Brid.) Mitt., Rhacocarpus purpurascens (Brid.) Paris, Racomitrium crispipilum (Taylor) A. Jaeger, Syntrichia andicola (Wilson) R.H. Zander, Thuidium peruvianum Mitt. y varios miembros no identificados de los géneros Breutelia, Bryum, Campylopus, Pohlia, Zygodon y Pottiaceae. Las briofitas encontradas en la rica vegetación incluyen a las hepáticas Anastrophyllum auritum (Lehm.) Steph. (una forma pequeña, depauperada), A. nigrescens (Mitt.) Steph., A. tubulosum (Nees) Grolle, Andrewsianthus jamesonii (Mont.) Váňa, Aneura pinguis (L.) Dumort., Anthelia juratzkana (Limpr.) Trevis., Blepharostoma trichophyllum, Cephalozia crossii Spruce, Cheilolejeunea oncophylla (Ångstr.) Grolle & E. Reiner, Chiloscyphus breutelii (Gottsche) J.J. Engel & R.M. Schust., Gongylanthus granatensis (Gottsche) Steph., G. liebmannianus (Lindenb. & Gottsche) Steph., G. limbatus (Herzog) Grolle & Váňa, Gymnomitrium laceratum (Steph.) Horik., Herbertus acanthelius Spruce, Isopaches bicrenatus, Isotachis lopezii (R.M. Schust.) Gradst., Jensenia spinosa (Lindenb. & Gottsche) Grolle, Leptoscyphus gibbosus (Taylor) Mitt., Metzgeria fruticola Spruce, Plagiochila bifaria (Sw.) Lindenb., P. cleefii Inoue, P. dependula Taylor, P. punctata (Taylor) Taylor, P. revolvens Mitt., Riccardia spp., Solenostoma sphaerocarpum (Hook.) Steph., Stephaniella paraphyllina J.B. Jack, Symphyogyna brasiliensis Nees, Syzygiella sonderi (Lindenb. & Gottsche) K. Feldberg et al. (= Cryptochila grandiflora [Lindenb. & Gottsche] Grolle), Triandrophyllum eophyllum (R.M. Schust.) Gradst. y T. subtrifidum (Hook f. & Taylor) Fulford & Hatcher. Además, observamos una rica comunidad de hepáticas epífitas en las ramas de Loricaria y Baccharis a m, la cual incluye muchas especies características de los altos Andes como Chiloscyphus fragmentissimus (R.M. Schust.) J.J. Engel & R.M. Schust. (= Campanocolea fragmentissima R.M. Schust.), Diplasiolejeunea replicata (Spruce) Steph., Drepanolejeunea andina Herzog, Frullania peruviana Gottsche, F. tetraptera Nees & Mont., Harpalejeunea grandistipula R.M. Schust, Metzgeria agnewii Kuwah., Microlejeunea colombiana Bischler, Lejeunea catinulifera Spruce y Radula tenera Mitt. En este artículo se detallan los registros nuevos más interesantes entre nuestras colecciones. Previamente, A. Schäfer-Verwimp y otros obtuvieron registros florísticos nuevos de los parches de bosque de Polylepis pauta Hieron. en el paso de Papallacta a 4000 m, en la provincia de Pichincha (Schäfer-Verwimp et al. 2006). Ellos registraron 180

192 numerosas especies nuevas para Napo y Pichincha. Muchas de las especies encontradas por estos autores fueron nuevamente registradas durante nuestra visita en el Los especímenes están depositados en los Herbarios de la Universidad Técnica Particular de Loja (HUTPL; colecciones de A. Benítez) y de la Pontificia Universidad Católica del Ecuador, Quito (QCA; colecciones de S.R. Gradstein et al. y de M. Burghardt et al.), algunos duplicados están en el herbario privado de A. Schäfer- Verwimp, Alemania. A continuación se presentan las especies de hepáticas y antoceros en orden alfabético con una breve descripción de su ecología y distribución geográfica. Los nuevos registros para el país llevan un asterisco. La nomenclatura de las especies de hepáticas y antoceros y su distribución geográfica sigue a Léon-Yánez et al. (2006) y al nuevo catálogo de las hepáticas de Colombia (Gradstein & Uribe en prep.). ANTHOCEROTOPHYTA (HORNWORTS) Anthoceros punctatus L. Loja: ciudad de Loja, invernadero de orquídeas UTPL, S, W, 2120 m, en suelo formando manchas verde oscuras junto a Lunularia cruciata (L.) Dumort., muy abundante, 14/06/2011, Benitez 6 (HUTPL). Distribución geográfica: subcosmopolita, en Ecuador previamente conocida en las islas Galápagos y la provincia de Zamora Chinchipe a m. Nueva para la provincia de Loja. *Notothylas vitalii Udar & D.K. Singh Loja: Zapotillo, bosque seco tropical, S, W, 400 m, en suelo formando grandes manchas verdes en lugares más o menos expuestos y junto a Riccia sp., muy rara, 15/3/2012, det. A. Schäfer-Verwimp, Benitez 423 (HUTPL). El Oro: Reserva Ecológica Arenillas (REMA), bosque seco tropical, S, W, m, en suelo formando grandes manchas verdes junto a Riccia sp., muy común, 5/5/2012, Benitez 536 (HUTPL). Notothylas vitalii se caracteriza por presentar talos pequeños de 0,5 a 2 cm de diámetro, esporas amarillas, eláteres unicelulares y cápsulas que se abren en dos valvas longitudinales (Gradstein & Costa 2003). Distribución geográfica: previamente conocida de Brasil, con una distribución general sobre los 500 m (Gradstein & Costa 2003). Nueva para Ecuador y primer registro del 181

193 género Notothylas en Ecuador continental. La presencia de N. vitalii en el sur de Ecuador constituye una extensión notable de su distribución. El registro de la especie en el bosque seco tropical de la provincia de El Oro, a 50 m, es el más bajo en América tropical. MARCHANTIOPHYTA (LIVERWORTS) Andrewsianthus jamesonii (Mont.) Váňa Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: México a Bolivia, E África; en Ecuador previamente conocida de las provincias de Pichincha y Tungurahua a m. Nueva para la provincia de Napo. Aneura pinguis (L.) Dumort. Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre, cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: subcosmopolita; en Ecuador previamente conocida de las provincias de Tungurahua y Zamora Chinchipe a m. Nueva para la provincia de Napo y el registro más alto en el país. Se estima que A. pinguis incluye un complejo de especies (Wachowiak et al. 2007). Se desconoce cuál es la relación taxonómica de las plantas del Ecuador en este complejo de especies. Anthelia juratzkana (Limpr.) Trevis. Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: ampliamente distribuida en la región holártica, rara en el trópico, colectada algunas veces en localidades alto-alpinas por encima de 4000 m en México, Venezuela, Ecuador y Bolivia (Gradstein et al. 2001). En Ecuador, este 182

194 especie era conocida solamente del Páramo de la Virgen donde fue colectada una vez por Dr. Schuster en 1993 (Schuster 1996); el material falta en los herbarios ecuatorianos. Con este registro se confirma la presencia de la especie en el país. La presencia de Anthelia en el país no está mencionada en el Catálogo de las Hepáticas del Ecuador (León-Yánez et al. 2006). Austrofossombronia peruviana (Gottsche) Crand.-Stotl., Stotler & A.V.Freire Loja: ciudad de Loja, fragmento de bosque montano secundario, S, W, 2620 m, forma grandes manchas verdes junto a Marchantia sp., sobre suelo fangoso en un arroyo, muy rara, 14/3/2010, Benitez 233 (HUTPL). Pichincha: páramo muy húmedo con Plantago rigida ca. 1 km E de la cumbre del Guagua Pichincha, 4000 m, en suelo, 18/1/2008, Burghardt et al (QCA). Distribución geográfica: Andes tropicales, de 3500 hasta 4750 m; en Ecuador previamente conocida de las provincias de Carchi, Chimborazo y Morona Santiago a m. Nueva para las provincias de Loja y Pichincha. El registro de Loja es el más bajo para esta especie y extiende su área de distribución ecuatoriana al sur del país. *Blepharostoma trichophyllum (L.) Dumort. Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: ampliamente distribuida en la región holártica; especie rara en las montañas tropicales (Gradstein & Váňa 1987), en el Neotrópico conocida de Costa Rica, Venezuela, Colombia y Perú, a m. Nueva para Ecuador. Cephalozia crossii Spruce Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: ampliamente distribuida en América tropical; en Ecuador previamente conocida de las provincias de Tungurahua y Zamora Chinchipe a m. Nueva para la provincia de Napo y el registro de mayor altura en el país. Cheilolejeunea oncophylla (Ångstr.) Grolle & E. Reiner 183

195 Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: ampliamente distribuida en América tropical; en Ecuador previamente solo conocida de la Reserva Biológica San Francisco (prov. Zamora Chinchipe) a m. Nueva para la provincia de Napo, segundo registro en el país y el registro de mayor altura de C. oncophylla. Chiloscyphus vermicularis (Lehm.) Hässel de Menendez (Clasmatocolea vermicularis (Lehm.) Grolle) Loja: Amaluza, bosque montano primario, S, W, 2600 m, en suelo fangoso junto a un arroyo, formando grandes matas verde pálidas o amarillas junto a Marchantia sp., muy rara, 19/5/2010, Benitez 318 (HUTPL). Distribución geográfica: América tropical, África, regiones templadas del Sur; en Ecuador previamente conocida de las provincias de Pichincha, Tungurahua y Zamora Chinchipe a m. Nueva para la provincia de Loja. *Frullania setigera Steph. Loja: Parque Nacional Podocarpus, Cajanuma, bosque nublado alto-montano, S, W, 2800 m, en tronco, 11/11/2009, Gradstein (QCA). Distribución geográfica: América tropical (Guatemala, Costa Ria, Colombia, Trinidad, Brasil), especie poco conocida. Nueva para Ecuador. Gongylanthus liebmannianus (Lindenb. & Gottsche) Steph. Loja: ciudad de Loja, Punzara alto, páramo, S, W, 2770 m, en suelo húmedo y rocas cubiertas de suelo, forma grandes matas pardo claras, muy abundante, 24/5/2010, Benitez 427 (HUTPL). Distribución geográfica: México a Bolivia, en Ecuador previamente conocida de las provincias de Chimborazo, Napo y Zamora Chinchipe, m. Nueva para la provincia de Loja. *Isopaches bicrenatus (Schmidel) H. Buch Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al , det. J. Váňa (QCA). 184

196 Distribución geográfica: ampliamente distribuida en la región holártica; especie rarísima en el trópico, previamente solamente conocida de dos localidades en la Sierra de Mantiqueira en el sureste de Brasil a 2400 m (Gradstein & Costa 2003). Nueva para Ecuador y primer registropara los Andes. Isotachis lacustris Herzog Loja: Parque Nacional Colambo-Yacuri, Jimbura, páramo, S, W, 3400 m, en suelo fangoso de un arroyo formado grandes matas pardas o negras, muy abundante, 8/7/2010, Benitez 267 (HUTPL). Napo/Pichincha: Páramo de la Virgen, N del paso de Papallacta, ca. 0,5 km S de la estación de radio, 4200 m, en el margen de una laguna y en pequeños ríos, 5/4/2008, Burghardt et al. 6869, 6875 (QCA). Distribución geográfica: Andes tropicales, en Ecuador previamente solamente conocida del páramo de El Ángel (Carchi), m. Nueva para las provincias de Loja, Napo y Pichincha. El registro de Loja amplía su área de distribución ecuatoriana al sur del país. Isotachis lopezii (R.M. Schust.) Gradst. Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: Andes tropicales (Venezuela a Bolivia), Costa Rica; en Ecuador previamente conocida de las provincias de Carchi y Zamora Chinchipe a m. Nueva para la provincia de Napo y el registro de mayor altura de I. lopezii. Isotachis serrulata (Sw.) Gottsche Loja: Jimbilla, bosque húmedo de neblina montano, S, W, 2740 m, crece en el suelo fangoso y sobre rocas de un arroyo junto a Marchantia sp., muy abundante, 10/6/2011, Benitez 256 (HUTPL). Distribución geográfica: América tropical, en Ecuador previamente conocida de las provincias de Esmeraldas, Morona Santiago, Pichincha y Zamora Chinchipe a m. Nueva para la provincia de Loja. Jensenia spinosa (Lindenb. & Gottsche) Grolle Loja: Parque Nacional Podocarpus, Cajanuma, páramo, S, W, 185

197 3150 m, crece en el suelo fangoso de la vegetación, muy común, 2/4/2010, Benitez 258 (HUTPL). Distribución geográfica: América tropical, África; en Ecuador previamente conocida de las provincias de Carchi, Napo y Zamora Chinchipe, m (León-Yánez et al. 2006; Benitez & Gradstein 2011). Nueva para la provincia de Loja. Lejeunea reflexistipula (Lehm. & Lindenb.) Gottsche Loja: Loma del Oro, páramo, S, W, 3300 m, crece en el suelo húmedo y en el mantillo de la vegetación y en la base de arbustos junto a Metzgeria sp., muy abundante, 10/5/2010, Benitez 256, det. A. Schäfer-Verwimp (HUTPL). Distribución geográfica: América tropical, en Ecuador previamente conocida de las provincias de Carchi, Morona Santiago, Napo, Pastaza, Tungurahua y Zamora Chinchipe a m. Nueva para la provincia de Loja. *Lepidozia auriculata Steph. Pichincha: paso de Papallacta, S, W, 4000 m, en bosque muy húmedo de Polypelis pauta, sobre base de tronco, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: Colombia y Perú a m; reportado de Ecuador (Chimborazo) como registro dudoso (Léon-Yánez et al. 2006). Primer registro confirmado para el Ecuador. Lepidozia cupressina (Sw.) Lindenb. Pichincha: paso de Papallacta, S, W, 4000 m, en bosque muy húmedo de Polypelis pauta Hieron. sobre base de tronco, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: América tropical, África, W Europa; en Ecuador previamente conocida de la provincia de Zamora Chinchipe a m. Nueva para la provincia de Pichincha y segundo registro del país. Lunularia cruciata (L.) Dumort. Loja: ciudad de Loja, invernadero de orquídeas UTPL, S, W, 2120 m, en suelo, forma grandes manchas verdes junto a Anthoceros punctatus L. muy abundante, 14/8/2011, Benitez 255 (HUTPL). Distribución geográfica: subcosmopolita pero escasa en los trópicos; en Ecuador previamente conocida en la provincia de Pichincha a 2850 m. Nueva para la provincia de Loja. Este registro amplía su área de distribución ecuatoriana al sur del país. 186

198 Noteroclada confluens Hook. & Wils. Loja: Parque Nacional Colambo-Yacuri, Jimbura, páramo, S, W, 3400 m, en suelo fangoso junto a un arroyo formando grandes matas verde pálidas, muy rara, 8/7/2010, Benitez 272 (HUTPL). Distribución geográfica: América tropical y austral (Crandall-Stotler et al. 2010), en Ecuador previamente conocida de las provincias de Carchi, Chimborazo, Morona Santiago, Pichincha y Zamora Chinchipe a m. Nueva para la provincia de Loja. Plagiochasma rupestre (J.R. Forst. & G. Forst.) Steph. Loja: Catamayo-Palo Blanco, matorral seco, S, W, m, crece en suelo y en rocas húmedas en lugares expuestos y soleados cerca de un arroyo, forma grandes manchas verdes, muy rara, 24/1/2012, Benitez 420 (HUTPL). Distribución geográfica: pantropical y regiones mediterráneas; en Ecuador previamente conocida de las provincias de Pastaza, Tungurahua y las Islas Galápagos a m. Nueva para la provincia de Loja. Este registro amplía su área de distribución ecuatoriana al sur del país. Plagiochila cleefii Inoue Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: páramos de Colombia y Ecuador, en Ecuador previamente conocida de Cajanuma, Parque Nacional Podocarpus (prov. Loja) a 3150 m. Nueva para la provincia de Napo, segundo registro en el país y el registro de mayor altura de P. cleefii. Plagiochila dependula Taylor Loja: Parque Nacional Podocarpus, Cajanuma, páramo, S, W, 3150 m, sobre la base de arbustos (Miconia sp.) y entre la hojarasca de la vegetación junto a Plagiochila ensiformis Taylor, muy abundante, 2/4/2010, Benitez 258 (HUTPL). Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca del estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al (QCA). 187

199 Distribución geográfica: Andes tropicales, en Ecuador previamente conocida de las provincias de Pichincha y Zamora Chinchipe, m (León-Yánez et al. 2006; Benitez & Gradstein 2011). Nueva para las provincias de Loja y Napo. Plagiochila fuscolutea Taylor Loja: Parque Nacional Podocarpus, bosque nublado alto-montano, S, W, 2900 m, sobre la base de arbustos y entre la hojarasca de la vegetación junto a Metzgeria sp. y Riccardia sp., muy abundante, 2/4/2010, Benitez 258 (HUTPL). Distribución geográfica: Andes tropicales, en Ecuador previamente conocida de las provincias de Azuay, Carchi, Cotopaxi, Pichincha, Tungurahua y Zamora Chinchipe a m. Nueva para la provincia de Loja. Plagiochila ovata Lindenb. Pichincha: paso de Papallacta, S, W, 4000 m, en bosque muy húmedo de Polypelis pauta, en suelo con Plagiochila dependula, P. ensiformis y Syzygiella rubricaulis, 7/12/2009, Gradstein et al (QCA), ibid., en bosque de Gynoxis, 4000 m, en suelo con Plagiochila dependula y P. ensiformis, 20/6/2008, Burghardt et al (QCA). Distribución geográfica: México a Bolivia por encima de 2600 m (Müller et al. 1999); en Ecuador previamente conocida las provincias de Morona Santiago y Napo a m. Nueva para la provincia de Pichincha. Plagiochila punctata (Taylor) Taylor Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: América tropical, E África y W Europa (Heinrichs et al. 2005); en Ecuador previamente conocida de las provincias de Tungurahua y Zamora Chinchipe a m. Nueva para la provincia de Napo y el registro de mayor altura de P. punctata. *Platycaulis renifolia R.M. Schust. Carchi: Volcán Chiles, N de Tufiño-Maldonado road, 3600 m, en humedal de páramo creciendo entre almohadillas densas de Oreobolus obtusangulus Gaudich., 25/8/1997, P.M. Ramsay et al (QCA). 188

200 Distribución geográfica: única especie en el género Platycaulis y endémica de los Andes del Norte, previamente conocida solo del ejemplar tipo de los Andes de Venezuela (Páramo de Tamá), donde fue colectado por Dr. Schuster en 1978 (Schuster 1995). Segundo registro en el mundo y primer registro para el Ecuador. Platycaulis renifolia (familia Lophocoleaceae) es una especie rara de las turberas parameñas, reconocida por su color pardo oscuro, hábito lateralmente comprimido, hojas reniformes, anfigastros bífidos con lobos ciliados y rizoides fasciculados en las bases de los anfigastros. La especie es algo similar a Plagiochila dependula pero se reconoce por su estatura más pequeña, la presencia de anfigastros y sus rizoides fasciculados (anfigastros ausentes y rizoides dispersos en P. dependula). La ortografía "Platycaulis renifolius" en la publicación original (Schuster 1995) es un error. Porella brachiata (Taylor) Spruce Loja: ciudad de Loja, fragmento de bosque montano secundario, S, W, 2600 m, epífita sobre la corteza y base de árboles (Myrcianthes fragans (Sw) McVaught) y en el suelo sobre rocas, forman grandes manchas verdes oscuras, muy rara, 6/7/2010, Benitez 253, det. A. Schäfer-Verwimp (HUTPL). Distribución geográfica: especie endémica de los Andes del Norte, en Ecuador previamente conocida de la provincia de Pichincha. Nueva para la provincia de Loja. Este registro amplía su área de distribución ecuatoriana al sur del país. Pseudocephalozia quadriloba (Steph.) R.M. Schust. Pichincha: Páramo de Pichincha, 1 km E de la cumbre del Guagua Pichincha, páramo muy húmedo, 4000 m, entre Campylopus sp., 7/2/2008, Burghardt et al (QCA). Distribución geográfica: Costa Rica, Andes tropicales, regiones templadas del S; en Ecuador previamente conocida de la provincia de Carchi y Zamora Chinchipe, m. Nueva para la provincia de Pichincha. Riccardia andina (Spruce) Herzog Pichincha: paso de Papallacta, S, W, 4000 m, en bosque muy húmedo de Polypelis pauta, en corteza con Herbertus grossispinus (= H. sendtneri auct.), Leptoscyphus gibbosus, Plagiochila dependula y varios musgos, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: Andes tropicales; en Ecuador previamente conocida de las provincias de Los Ríos, Napo, Pastaza y Zamora Chinchipe, m. Nueva para la provincia de Pichincha y el registro de mayor altitud de R. andina. 189

201 Solenostoma callithrix (Lindenb. & Gottsche) Steph. (Jungermannia callithrix Lindenb. & Gottsche) Loja: Zamora Huayco Alto, Reserva Privada El Madrigal 5 km de la ciudad de Loja, zona de amortiguamiento del Parque Nacional Podocarpus, bosque siempre verde montano alto, S, W, 2400 m, crece en taludes sobre suelo húmedo en el sendero de llegada a la reserva, muy rara, 8/11/2010, Benitez 348, verif. A. Schäfer-Verwimp y J. Váňa (HUTPL). Distribución geográfica: América tropical, en Ecuador previamente conocida de las provincias de Carchi, Pichincha, Tungurahua y Zamora Chinchipe, m. Nueva para la provincia de Loja. Solenostoma hyalinum (Hook.) Mitt. (Jungermannia hyalina Hook.) Loja: Zamora Huayco Alto, Reserva Privada El Madrigal 5 km de la ciudad de Loja, zona de amortiguamiento del Parque Nacional Podocarpus, bosque siempre verde montano alto, S, W, 2400 m, crece en taludes sobre suelo húmedo y en lugares sombríos, muy común, 11/6/2011, Benitez 257, verif. A. Schäfer-Verwimp y J. Váňa (HUTPL). Distribución geográfica: pantropical y región holártica; en Ecuador previamente conocida de las provincias de Pichincha y Zamora Chinchipe, m. Nueva para la provincia de Loja y el registro de mayor altitud en Ecuador. Solenostoma sphaerocarpum (Hook.) Steph. (Jungermannia sphaerocarpa Hook.) Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 7/12/2009, Gradstein et al (QCA). Distribución geográfica: ampliamente distribuida en la región holártica y en las montañas tropicales (Gradstein & Váňa 1987); en Ecuador previamente conocida de las provincias de Carchi y Zamora Chinchipe a m. Nueva para la provincia de Napo. *Symphyogyna apiculispina Steph. Loja: Zamora Huayco Alto, Reserva Privada El Madrigal 5 km de la ciudad de Loja, zona de amortiguamiento del Parque Nacional Podocarpus, bosque siempre verde montano alto, S, W, 2400 m, crece sobre troncos en descomposición y entre la hojarasca de la vegetación, en lugares sombríos y húmedos 190

202 cerca de arroyos, muy rara, 26/3/2010, Benitez 202, verif. A. Schäfer-Verwimp (HUTPL). Symphyogyna apiculispina es muy similar a S. brogniartii Mont., pero difieren en que la primera presenta papilas mucilaginosas solo en el margen del talo con dos células de longitud y las lobulaciones del talo no llegan hasta el nervio central, a diferencia en S. brogniartii donde las lobulaciones del talo llegan al nervio central y las papilas se localizan en el margen y la superficie dorsal del talo (Uribe & Aguirre 1995). Distribución geográfica: previamente conocida solo de Bolivia y Colombia, m. Nuevo registro para Ecuador. A pesar de ser una especie cortícicola, también crece sobre troncos en descomposición, hojarasca, base de troncos y en el suelo en zonas muy húmedas y sombrías (Uribe & Aguirre 1995), lo que concuerda con nuestras observaciones. Triandrophyllum eophyllum (R.M. Schust.) Gradst. (Olgantha eophylla R.M. Schust.) Napo: Páramo de la Virgen, N del paso de Papallacta, en ladera rocosa NW de la cumbre cerca de la estación de radio, S, W, m, hepática terrestre en superpáramo muy húmedo, 20/6/2008, M. Burghardt et al. 7407, 7434b (QCA), ibid., 7/12/2009, Gradstein et al (QCA). Distribución geográfica: especie endémica para Ecuador y solamente conocida de la localidad tipo en el Páramo de la Virgen donde fue colectada por Dr. Schuster en 1993 (Schuster 1996). La especie fue descrita como un género nuevo monospecífico, Olgantha R.M. Schust., qué es actualmente considerado como sinónimo de Triandrophyllum (Gradstein et al. 2001). Las colecciones reportadas de T. eophyllum son las primeras desde 1993; estas confirman la ocurrencia de la especie en su única localidad conocida. La especie crece junto con T. subtrifidum (Hook.f. & Taylor) Fulford & Hatcher (especímenes Burghardt 7434a y Gradstein 12205, herbario QCA), segunda especie neotropical en el género Triandrophyllum y ampliamente distribuida en los Andes. A veces las dos especies crecen mezcladas y pueden ser dificiles de distinguir. Se reconoce a T. eophyllum por sus hojas más cóncavas y tan anchas como largas (más largas que anchas en T. subtrifidum) y el ápice de las hojas minutamente bífido (a veces trífido) hasta 1/10 de la hoja (más profundamente bífido o trífido, hasta 1/8-1/4(-1/2) de la hoja en T. subtrifidum). 191

203 Agradecimientos Agradecemos a A. Schäfer-Verwimp y J. Váňa por ayudar en la identificación de algunas especies y a dos revisores anónimos por sus correcciones del manuscrito. El trabajo de campo en el sur del país fue financiado por la Universidad Técnica Particular de Loja y la Secretaría Nacional de Educación Superior, Ciencia, Tecnología e Innovación del Ecuador (SENESCYT). También agradecemos a Cesar Aguirre, Ministerio del Ambiente de El Oro-Reserva Ecológica Arenillas (REMA) y Naturaleza y Cultura Internacional por proporcionar el acceso a las áreas de estudio. Bibliografía Benitez, A. & S. R. Gradstein Adiciones a la flora de briófitas del Ecuador. Cryptogamie Bryologie 32: Churchill, S. P., D. Griffin & J. Muñoz A Checklist of the mosses of the tropical Andean countries. Ruizia 17: Crandall-Stotler, B., R. E. Stotler, L. Zhang & L. L. Forrest On the morphology, systematics and phylogeny of Noteroclada (Noterocladaceae, Marchantiophyta). Nova Hedwigia 91: Gradstein, S. R. & D. P. Costa The Hepaticae and Anthocerotae of Brazil. Memoirs of the New York Botanical Garden 87: Gradstein, S. R. & A. Schäfer-Verwimp A new species of Archilejeunea (Spruce) Schiffn. (Lejeuneaceae) from Ecuador. Cryptogamie Bryologie 33: Gradstein, S. R. & J. Vána On the occurrence of Laurasian liverworts in the Tropics. Memoirs of the New York Botanical Garden 45: Heinrichs, J., M. Lindner, H. Groth & C. Renker Distribution and synonymy of Plagiochila punctata (Taylor) Taylor, with hypotheses on the evolutionary history of Plagiochila sect. Arrectae. Plant Systematics and Evolution 250: León-Yánez, S., S. R. Gradstein & C. Wegner Hepáticas (Marchantiophyta) y Antoceros (Anthocerotophyta) del Ecuador, catálogo. Publicaciones del Herbario QCA, Pontificia Universidad Católica del Ecuador, Quito. Müller., J., J. Heinrichs & S. R. Gradstein A revision of Plagiochila sect. Plagiochila in the Neotropics. The Bryologist 102: Schäfer-Verwimp, A., R. Wilson, S. Yandún, K. Feldberg, M. Burghardt & J. Heinrichs Additions to the bryophyte flora of Ecuador. Cryptogamie Bryologie 27:

204 Schuster, R. M Venezuelan Hepaticae VI. On Platycaulis Schust. (Jungermanniales). Nova Hedwigia 61: Schuster, R. M On Olgantha Schust., gen. n. Isophylly an evolution of Jungermanniales. Nova Hedwigia 63: Schuster, R. M Harpalejeunea (Spr.) Schiffn. I. Studies on a new Andean species of Harpalejeunea. Journal of the Hattori Botanical Laboratory 87: Uribe, J. & J. Aguirre Las especies Colombianas del género Symphyogyna (Hepaticae: Pallaviciniaceae). Caldasia 17: Wachowiak, W., A. Bączkiewicz, E. Chudzińska & K. Buczkowska Cryptic speciation in liverworts a case study in the Aneura pinguis complex. Botanical Journal of the Linnean Society 155:

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206 CAPÍTULO VI / CHAPTER VI More than one hundred new records of lichens from Ecuador ANGEL BENITEZ 1*, GREGORIO ARAGÓN 2, YADIRA GONZÁLEZ 1 & MARÍA PRIETO 2 1 Sección de Ecología y Sistemática, Departamento de Ciencias Naturales, Universidad Técnica Particular de Loja, San Cayetano s/n, Loja, Ecuador. 2 Área de Biodiversidad y Conservación, Departamento de Biología y Geología, Universidad Rey Juan Carlos, Móstoles, E-28933, Madrid, España. Benítez, Á., Aragón, G., González Y. & Prieto, M Artículo en revisión en Polish Botanical Journal. Chapsa diploschistoides (Zahlbr.) Frisch 195

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208 Abstract Ecuador is considered one of the richest and most diverse country on Earth, and it is expected to hold a high richness of lichenized fungi. However, studies centered on these organisms are still scarce and focused on very specific areas, so that the actual knowledge of the species number is still incomplete. In this study we report twelve species new to South America and 50 species new to Ecuador, for which we provide data on ecology and distribution. In addition, we found 41 species that were previously recorded from Galapagos Islands and were found for the first time in mainland Ecuador. Finally, 31 species have been found for the first time in El Oro or Loja provinces. In total 134 species are new for South America, Ecuador or different provinces, thus widening considerably the known distribution of the species and the lichen Flora of the country. The results of this research support the need to conduct additional taxonomic and floristic studies in the near future. Key words: diversity, epiphytic lichens, South America, tropical montane forests, dry forests. 197

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210 INTRODUCTION Lichens are a very diverse group with ca estimated species around the world (Lücking et al. 2009a), and ca species estimated for the Neotropics. Tropical Andes is considered the most diverse area for lichens (Lücking et al. 2009a; Sipman 2011). However, the present knowledge is still far from the estimates, and in countries like Bolivia, Chile, Peru and Venezuela only a quarter of the estimated number of species have been reported (Marcano et al. 1996; Galloway & Quilhot 1998; Ramos 2014; Rodriguez-Flakus et al. 2014). In Ecuador, ca. 900 lichen species have been recorded for mainland (Cevallos 2012; Prieto et al. in prep.) and 633 (including lichenicolous) for Galapagos Islands (Bungartz et al. 2016), a relatively low species number compared with the estimates. Collecting efforts have focused on sites and habitats located in Napo, Pichincha and Zamora Chinchipe provinces, while in provinces such as Esmeraldas, Los Ríos and Manabí there are scarce contributions (Lücking 1999a; Nöske et al. 2007; Cevallos 2012). Moreover, most studies have focused on the most conspicuous species rather than on crustose microlichens, therefore not allowing reliable estimates of total species richness (Arvidsson 1991; Lücking 1999; Nöske et al. 2007; Lücking et al. 2009a; Cevallos 2012). Recently, Benitez et al. (2012) documented about 119 macrolichen species in six forests in Loja province, which demonstrates the great diversity that the southern region of Ecuador houses. Thus, the main objective of this study is to contribute to the knowledge of the lichen diversity in Ecuador, by providing information on the ecology and distribution of the less known species. MATERIALS AND METHODS The study was conducted in the southern region of Ecuador in different tropical forest fragments (montane and dry forests) located in El Oro and Loja provinces, in the private Madrigal reserve, the Colambo-Yacuri National Park and the ecological reserve Arenillas (REMA) (Figure 1). 199

211 Figure 1: Ecuadorian map showing collection sites of lichens Specimens were collected as part of parallel ecological studies carried out by the authors. The specimens were identified using numerous published keys which are incorporated in the text for species reported for the first time from Ecuador. General keys (Brodo et al. 2001; Nash III et al. 2002, 2004, 2007) were also used for identification. Standard microscopy techniques and spot tests based on thallus fluorescence under ultraviolet light (UV), reactions with K (10% water solution of potassium hydroxide), C (commercial bleach) and Lugol s solution (I) were checked in some species. For the nomenclature of the species we followed MycoBank ( and LIAS (A Global Information System for Lichenized and Non-Lichenized Ascomycetes: Specimens were deposited in the Herbarium of Universidad Técnica Particular de Loja (HUTPL), at the Bryophytes and Lichens Collection. New records from Ecuador are marked with an asterisk (*) and those new for South America with two asterisks (**). For each new record the following information has been included 1) locality and collection number, 2) references where morphological or anatomical characteristics are described, 3) iconography, where an image or drawing of habit or some morphological or anatomical character appears, 4) ecology, in the study area, 5) general distribution 200