BIOTROPICA 39(4): 525–529 2007 10.1111/j.1744-7429.2007.00300.x Determinants of Lichen Diversity in a Rain Forest Understory L. A. Dyer1 Department of Ecology and Evolutionary Biology, 310 Dinwiddie Hall, Tulane University, New Orleans, Louisiana 70118, U.S.A. and D. K. Letourneau Department of Environmental Studies, Interdisciplinary Sciences Building, University of California, Santa Cruz, California 95064, U.S.A. ABSTRACT Change in lichen diversity is often used as a bioindicator to estimate effects of atmospheric pollution, but natural variation in lichen cover and species richness can be very high. We examined the top-down effects of spore-consuming ants and the bottom-up effects of nutrient and light availability on lichen diversity associated with the leaf surface of the rain forest understory plant, Piper cenocladum. Plots containing P. cenocladum were randomly assigned to treatments in factorial experiments that included high and low light levels, nutrient enrichment, and presence and absence of the ant mutualist, Pheidole bicornis. At the conclusion of the experiments, plants were harvested and size of leaves, secondary metabolite content (amides), epiphyll cover, and the species richness of the lichens (which comprised 85% of the epiphyll community) were quantified. Epiphyll cover (mosses, liverworts, and lichens) was greater on plants that had ant-mutualists and balanced resources. Lichen species richness was greater for plants with balanced resources, particularly for those with high light availability. Relationships between toxins and lichen cover and richness were weak and unclear. In this system, natural sources of variation were reliable determinants of lichen diversity and both biotic and abiotic influences were important. Key words: Costa Rica; mutualisms; Piper cenocladum; resource availability; toxins; tropical rain forest. MUTUALISMS ARE STILL NEGLECTED IN THEORY AS IMPORTANT FORCES in the dynamics of biotic communities, but some wellstudied model systems suggest that they have measurable direct and indirect effects on all food webs (Hacker & Gaines 1997, Hay et al. 2004). The ant plant, Piper cenocladum (Piperaceae C. DC), is involved in a mutualism that has strong effects on understory plants in a tropical rain forest (Letourneau et al. 2004). Leaves of this plant are often colonized by another common mutualistic pair: lichens (i.e., heterotrophic mycobionts and autotrophic photobionts). Lichens are found in most terrestrial systems and are well defended against herbivores (Seaward 1977, Gauslaa 2005), but they are very susceptible to toxins and mechanical disruption. Lichens lack a protective cuticle, absorbing water and nutrients over their entire surface and also airborne pollutants in the same way (Hawksworth & Rose 1976). Since they are highly sensitive to atmospheric changes, they may be good bioindicators of environmental quality and may serve as a proxy for forest health variables that are difficult to measure directly (McCune 2000). They are also sensitive to depositional compounds and chemical changes in their host’s substrates, but lichen mortality levels depend on the taxon, with sensitive species dying at low levels of exposure to toxins while others may be highly resistant (Farmer et al. 1992). The rich literature on effects of pollutants on lichens has been recently supplemented by thorough investigations of abiotic determinants of lichen cover and diversity, especially in the tropics (e.g., Lücking 1998a, 1999a). One clear attribute of foliicolous lichen diversity is that, at very small scales, it can be comparable to alpha 1 Received 26 June 2006; revision accepted 14 October 2006. Corresponding author; e-mail: orugas@hotmail.com diversity of tropical trees at larger scales. For example, Lücking and Matzer (2001) found 49 species of lichens on a single dicot leaf from a wet forest in Costa Rica. Lücking and colleagues have also documented variation in diversity caused by altitude, humidity, and light availability in Costa Rica, with the shady understory of lowland rain forests containing the highest species richness of lichens (Lücking 1998a,b, 1999a,b,c; Lücking & Matzer 2001). These authors argue that niche relationships are not important determinants of lichen diversity within a habitat because resource requirements should be similar across species of lichens. However, few studies have experimentally examined how resource availability, along with biotic interactions, such as mutualism and predation, affect lichen diversity. In this study, we examined how manipulation of several biotic and abiotic factors affected lichen cover and diversity associated with the leaf surface of the rain forest understory plant, P. cenocladum C. DC. In particular, we tested the hypotheses that increased levels of natural plant toxins, decreased resource availability, and spore consumption by omnivorous ants would cause lower cover and species richness of foliicolous lichens. METHODS STUDY SYSTEM.—All experiments were conducted at La Selva Biological Station, Heredia Province, Costa Rica, located at 10◦ 25′ N, 84◦ 05′ W at ca 100 m asl. McDade et al. (1994) provide extensive ecosystem and community descriptions of the lowland wet forest at La Selva. Piper cenocladum shrubs are common in the understory of wet forests throughout the lowlands of Costa Rica (Burger 1971). The stems of this plant are usually hollow due to the presence of  C 2007 The Author(s) C 2007 by The Association for Tropical Biology and Conservation Journal compilation  525 526 Dyer and Letourneau Pheidole bicornis Forel ants, which remove the pith and reside in stems and petioles. Pheidole bicornis harvests food bodies produced by the plant, and removes insect eggs, some vines, and small phylloplane particles from the leaves (Risch et al. 1977; Letourneau 1983, 1998). The clerid beetle ant-predators Tarsobaenus letourneauae (= Phyllobaenus sp.) also occur as larvae inside the hollow petioles where they may kill adult ants and feed on both ant brood and food bodies (Letourneau 1990). These beetle larvae do not interact with organisms on the leaf surface, but they do cause significant decreases in leaf toxins (levels of toxins are highest in plants without ants, intermediate in ant plants, and lowest in beetle plants; Dyer et al. 2004). The toxins produced in leaves of P. cenocladum are nitrogen-containing compounds known as Piper amides: piplartine, 4′ –desmethylpiplartine, and cenocladamide (Dodson et al. 2000). FIELD EXPERIMENTS.—The field experiment is described fully in Dyer and Letourneau (1999). Briefly, we established 240 P. cenocladum cuttings in the forest understory in a factorial design of three treatments: fertilizer versus no fertilizer, high light versus low light, and ant presence versus ant exclusion. Each of the cuttings contained ant colonies, three leaves with less than 5 percent herbivore damage, four leaf nodes, and minimal epiphyll cover. To measure the effects of enriched plant resources (soil nutrients and light) on epiphyll cover and lichen diversity, we fertilized half (randomly assigned) of the plants with Once
slow release fertilizer (NPK 13:13:13 plus micronutrients), and we designated all plants as receiving either relatively high or relatively low light according to the amount of canopy cover. To exclude ants from half of the transplants, we introduced 0.1 cc of dilute insecticide (0.85 mg Diazinon
wettable powder per liter of distilled water) into petioles of each plant at 2–3 mo intervals (Dyer & Letourneau 1999). Data used in this study are from measurements on new growth (plant material produced after transplanting) taken 22 mo after treatments were applied. For each plant, we measured total leaf area for the first new leaf that was produced after experimental treatments were established (counting the number of 0.23 cm2 grid squares on a transparent thermoplastic overlay) and used the same method to measure percent epiphyll cover on the leaf. All lichens on the first leaf that grew after treatments were applied were identified to species at the end of the experiment by R. Lücking. The exact age of leaves was unknown, but because we only included new growth, all measures of lichen cover in this study are measures of lichens colonizing after treatments were applied. This method ensured that all leaves for which lichen measurements were recorded were approximately 22-mo old and similar in size. Amide content for all leaves in this experiment and the shadehouse experiment (described below) was quantitatively determined using the methods described in Dodson et al. (2000) and Dyer et al. (2004). SHADEHOUSE EXPERIMENT.—The shadehouse fragment experiment was conducted using P. cenocladum fragments grown in a controlled environment—a shade cloth enclosed structure provided protection from herbivores and other stresses. Leaves harvested from this experiment were younger and grown under a more controlled en- vironment, thus they provide an additional test of direct effects of our manipulations on lichen cover (but not species richness). The experiment is described in Dyer et al. (2004). Sixty plant fragments were cut and grown in a 20 percent ambient light shadehouse in pots with field-collected ultisol soil. The cuttings were left for 1 mo to establish, and then were randomly assigned to fertilizer, light and symbiont treatments in a factorial design. There were three levels of the symbiont treatment: controls with no symbionts, a single beetle larva added to the newest open petiole, and ant colonies (queen, brood, workers) added to all hollow petioles. For the light treatment, half of the plants were placed under shade cloth frames to reduce the ambient light to approximately 2 percent. The two levels of fertilizer treatment were 0 g and 5 g of Once
slow release fertilizer (NPK 13:13:13 plus micronutrients); these levels were chosen to be the low versus high nutrient treatments based on results from the field study (Dyer & Letourneau 1999). After 9 mo, the most recent fully expanded leaf from each plant was harvested, measured for leaf area, digitally scanned with a ruler for reference, and dried at room temperature for chemical analyses. These leaves were all approximately 6-mo old and were similar in size. The scanned images were used for calculating percent lichen cover. Using imaging software, we first scaled each leaf image to match the measurements indicated by the ruler, then used pixel counts to calculate leaf size and percent lichen cover. STATISTICAL ANALYSES.—To examine the effects of resource and symbiont manipulations on epiphyll cover and species richness in both experiments, we utilized analysis of covariance (ANCOVA) with resources and symbionts as independent variables, log-transformed percent epiphyll cover and species richness as response variables, and leaf size as a covariate. Species richness was only a dependent variable for field experiments, since reliable identifications were unavailable for shadehouse lichens. Because leaf size was never a significant covariate, it was deleted from all models. Symbiont presence was a dichotomous variable (ants present vs. ants excluded) in the field experiments and had three levels in the shadehouse experiment (control, beetles, ants). The “resource” variable was the same as used in other studies (Dyer & Letourneau 1999, 2003; Dyer et al. 2004) where leaf quality, plant biomass, food body production, detritivore diversity, and amide content were positively affected by balanced resource availability, which is a variable with two levels: balanced (high light, high nutrients and low light, low nutrients) versus unbalanced (high light, low nutrients and low light, high nutrients). Assumptions of ANOVA were tested and satisfied. We used multiple regressions to examine the effects of the three amides on lichen cover and species richness. RESULTS We found 44 species of lichens (Table 1) and five species of bryophytes (Table 2) on 141 leaves from the P. cenocladum fragments in the field. For the shadehouse, we found only seven morphospecies of lichens on 50 leaves. For both experiments, not all plants were examined due to mortality or failure to produce a fully expanded new leaf. Lichen cover and diversity was relatively low compared to other Lichen Diversity 527 TABLE 1. Foliicolous lichen species found on experimental leaves of Piper cenocladum and number of 141 leaves examined that contained each species. TABLE 2. Bryophyte species colonizing experimental leaves of Piper cenocladum and the number of 141 leaves examined that contained each species. Bryophytes Lichens Actinoplaca strigulacea Müll. Arg. Arthonia leptosperma (Müll. Arg.) R. Sant. Aspidothelium fugiens (Müll. Arg.) R. Sant. Frequency 1 16 1 Aspidothelium papillicarpum Lücking, nom. inval Aulaxina intermedia Lücking Aulaxina minuta R. Sant. 1 1 1 Badimia dimidiata (C. Bab. ex Leight.) Vezda Byssoloma absconditum Farkas & Vezda 1 1 Byssoloma aurantiacum Kalb & Vezda Byssoloma minutissimum Kalb & Vezda Byssoloma wettsteinii (Zahlbr.) Zahlbr. 6 11 3 Calopadia sp. Coenogonium subluteum Rehm Dimerella siquirrensis Lücking 1 56 55 Echinoplaca diffluens (Müll. Arg.) R. Sant. Echinoplaca leucotrichoides (Vain.) R. Sant. Echinoplaca pellicula (Müll. Arg.) R. Sant. 1 1 1 Fellhanera angustispora Lücking Fellhanera badimioides Lücking, Lumbsch & Elix Fellhanera lisowskii (Vezda) Vezda 1 1 2 Fellhanera tricharioides Lücking & R. Sant., nom. inval.]. Gyalectidium filicinum Müll. Arg. Gyalideopsis vulgaris (Müll. Arg.) Lücking Mazosia melanopthalma (Müll. Arg.) R. Sant. Paratricharia paradoxa (Lücking) Lücking 1 15 4 1 1 Phylloblastia amazonica Kalb & Vezda Porina epiphylla (Fée) Fée Porina fusca Lücking 26 14 5 Porina limbulata (Kremp.) Vain. Porina lucida R. Sant. Porina mirabilis Lücking & Vezda 3 11 21 Porina rubella (Malcolm & Vezda) Lücking Porina rufula (Kremp.) Vain. Porina radiata Kalb, Lücking & Vezda 11 13 1 Sporopodium leprieurii Mont. Strigula nitidula Mont. Strigula phyllogena (Müll. Arg.) R. C. Harris 1 3 14 Strigula platypoda (Müll. Arg.) R. C. Harris Strigula viridis (Lücking) R. C. Harris Tricharia albostrigosa R. Sant. 17 2 1 Tricharia vainioi R. Sant. Trichothelium epiphyllum Müll. Arg. Trichothelium minus Vain. 2 5 1 Trichothelium minutum (Lücking) Lücking 1 studies of tropical lichens (Lücking 1998a,b Lücking & Matzer 2001), but unlike those surveys, our study did not examine “climax” communities, since we only included new leaves (i.e., this is a measure of colonizers after our manipulations). Frequency Crossidium sp. 34 Cyclodictyon sp. Odontoschisma sp. Radula sp. 5 4 15 Taxilejeunea sp. 1 Low densities and diversities were expected for the young, protected leaves in the shadehouse. Manipulations had strong effects for all experiments, revealing consistent positive effects of ants and balanced resources on lichen cover, and in some cases lichen species richness. Plant chemistry had very little effect on lichens. Plants without ants contained 75 percent lower lichen coverage in shadehouse experiments (F 2,49 = 5.7, P = 0.006) and 23 percent lower total epiphyll coverage in the field (F 1,72 = 5.2, P = 0.03; Fig. 1). In the shadehouse, plants inhabited by beetles also had higher lichen cover than plants without ants, but had less than half of the lichen cover than ant plants (Fig. 1). Exposure of plants to balanced versus unbalanced resources resulted in 89 percent higher lichen coverage in shadehouse experiments (1.7% vs. 0.9% coverage; F 1,49 = 3.9, P = 0.05), but there were no significant effects of resources on total epiphyll coverage in the field (F 1,72 = 2.1, P = 0.2). For both experiments, there were no significant interactions between symbionts and resources (shadehouse: F 1,72 = 1.1, P = 0.3; field: F 1,72 = 1.1, P = 0.3). In the field experiments, overall species richness was 5.0 ± 0.9 SE species per leaf. Richness was increased by 100 percent (from 3.2 to 6.5 species per leaf ) when plants were exposed to balanced versus unbalanced resources (F 1,35 = 3.9, P = 0.05), and light availability FIGURE 1. Percentage lichen cover on experimental plants with and without symbionts (mutualistic ants and predatory beetles). Experiments were conducted in a natural field setting as well as in shadehouses. Percent cover in the field experiment includes all epiphylls, while shadehouse plants were only colonized by lichens. Statistics are reported in the text. 528 Dyer and Letourneau FIGURE 2. Lichen species richness on leaves of plants exposed to high versus low light availability in field experiments. Statistics are reported in the text. was especially important. If light is included as a factor in ANOVA, lichen species richness is significantly higher with slightly more average light availability (F 1,35 = 6.7, P = 0.02; Fig. 2). Ants had no effects on species richness (F 1,35 = 0.6, P = 0.4), and there were no significant interactions between symbionts and resources (F 1,35 = 1.7, P = 0.2). Chemistry had minor effects on lichen cover, and the correlations were possibly weaker due to a latent correlation with ant presence (amide content is at least half when ants are present; Dyer et al. 2004). In the shadehouse experiments, there was no significant relationship between the three amides and total lichen cover (F 3,49 = 0.5, P = 0.7, R2 = 0.03). In the field experiments, amide content was not associated with lichen species richness (F 3,21 = 0.1, P = 0.9, R2 = 0.02) but had a small significant effect on total epiphyll cover (F 3,50 = 2.5, P = 0.05, R2 = 0.15), and the direction of the effect depended on the particular amide. Increased piplartine was associated with lower percent epiphyll cover (standardized parameter estimate [SPE] = −1.8), while high cenocladamide content was associated with higher cover (SPE = 2.2). DISCUSSION Most studies on lichen diversity have been taxonomic or checklists (e.g., Elvebakk & Bjerke 2006, Lücking 2006, Rivas Plata et al. 2006,), or have examined responses to air pollution (e.g., Hauck 2005), pesticides (e.g., Bartok 1999), management (e.g., Anand et al. 2005), and other abiotic components of ecosystems (e.g., fire; Longan et al. 1999). Here, we found another important abiotic predictor of lichen cover and richness: resource availability. Light and mineral nutrients vary considerably between and within forest ecosystems, and our results are consistent with predicted positive effects of enhanced resources on biodiversity (Dobzhansky 1950, Rohde 1992). The effects of light are probably direct effects on lichen growth, whereas any effects of mineral resources or leaf chemistry (both of which affect P. cenocladum leaf quality) on the lichens were most likely due to changes in the quality of leachates, which can be an important source of metabolites for epiphylls and are likely to reflect overall chemistry of the leaf (Wanek & Pörtl 2005). The differences in resource availability, particularly light, were subtle compared to differences examined in other studies. For example, Lücking (1998b) demonstrated that lichen communities differ completely between gaps and understory, which have dramatic differences in light and nutrient availability. For our subtle microsite differences in resource availability (mean canopy cover for high light was 91.7% vs. 96.6% cover for low light), the same assemblage of lichens occurred at the different light and nutrient levels, but they were more abundant and species rich in balanced resource conditions, especially those areas with high light availability. These subtle differences are unlikely to affect plant fitness, but the doubling of lichen cover and species richness on individual leaves caused by some of our manipulations are likely to be important for lichen populations and communities when the total leaf area (as high as 2.5 m2 per plant) and densities of plants per forest (269.7 ± 155.7 plants/ha; Letourneau & Dyer 1998) are considered. In addition, these levels of colonization over the years would lead to considerable lichen cover for the plant, as is the case for many P. cenocladum leaves (Letourneau 1998). The biotic effects on lichen diversity were equally strong, which is a unique and understudied result. Many myrmecophytes are protected from accruing high epiphyll loads via ant consumption of spores and small lichens (Heil & McKey 2003). However, this is not the case for P. cenocladum, for which the presence of ant mutualists was associated with higher lichen cover and richness under natural conditions in the field. Lichen cover was also enhanced by the presence of ants in shadehouses, where herbivores were excluded and colonization should have been impeded by the shade cloth walls of the houses. The mechanism by which ants affected lichen cover is not clear, but it is potentially linked to resource availability. Plants with ants grow more vigorously and provide greater usable nitrogen due to lower levels of amide defenses in both shadehouses and in the field (Dodson et al. 2000, Dyer et al. 2004) and due to lower levels of herbivory in the field (Letourneau 1983, Dyer & Letourneau 1999). Although toxins have well-established effects on lichen abundance and diversity, the effects of natural products on lichens is not well investigated. We found only a weak relationship between amide content and lichen cover in the field and no relationship in the shadehouses; lichen species richness was not at all associated with amide content. The levels of Piper amides found in our experimental leaves are high enough to kill caterpillars (Dyer et al. 2003, Dyer et al. 2004), deter leaf-cutting insects (Dyer et al. 2004), and kill fungi (Capron & Wiemer 1996, Parmar et al. 1997). High levels of one of the amides, piplartine (a known fungicide), was associated with lower lichen cover in the field, which is consistent with amide toxicity and lichen response to toxins. However, a similar compound, cenocladamide, was positively correlated with lichen cover. There are no obvious explanations for such an association, but it does support the concept that some lichens are not sensitive to known toxins. In conclusion, bottom-up increases in lichen diversity due to natural resource availability is one clear dynamic in tropical communities. Biotic interactions also have important effects on Lichen Diversity 529 lichen cover, but the actual mechanisms of how omnivorous ants and natural toxins affect lichens in this system is not clear. Current studies utilizing lichens as bioindicators or examining determinants of lichen diversity should include known top-down and bottom-up forces as natural sources of variation. 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