Abstract

The morphology of the first zoeal stage of the decorator crab Macrocoeloma subparallelum (Stimpson, 1860) from Cuba is described and compared with the available descriptions for the genus. Among Macrocoeloma Miers, 1879 species, the first zoea of M. subparallelum can be differentiated only by the number of aesthetascs and setae of the antennule (4 and 2, respectively). Recently, Macrocoeloma has been placed as an incertae sedis genus in Majoidea, closely allied to other Epialtidae and Pisinae members. The distinct spine in the distal segment of the endopod of the first maxilliped in the zoeal stages of Macrocoeloma is similar to what we observe in other Epialtidae genera, a character that supports the recent phylogenetic findings.

Key words
Cuba; Pisinae; Epialtidae; Mithracidae; larval development

Introduction

Majoid crabs, commonly known as decorator or spider crabs, form one of the most diverse groups among brachyurans including nowadays six families with a total of 907 valid species (Davie et al., 2015Davie, P.J.; Guinot, D. and Ng, P.K. 2015. Systematics and classification of Brachyura. p. 1049-1130. In: P. Castro; P.J.F. Davie; D. Guinot; F.R. Schram and J.C. von Vaupel Klein (eds), Treatise on Zoology - Anatomy, Taxonomy, Biology . The Crustacea, Vol. 9, Part C (2 vol.). Leiden, Brill .). It is a superfamily that is distributed throughout nearly all oceans and is well represented, especially in warm regions, with about 239 species in the Americas, 124 species in the western Atlantic, and 115 species in the eastern Pacific (Griffin, 1966Griffin, D.J.G. 1966. A review of the Australian majid spider crabs (Crustacea, Brachyura). Australian Zoologist, 13: 259-298, pls. 15-17. ; Boschi, 2000Boschi, E.E. 2000. Biodiversity of marine decapod brachyurans of the Americas. Journal of Crustacean Biology, 20(3): 337-342.).

Among majoids, the genus MacrocoelomaMiers, 1879Miers, E.J. 1879. On the classification of the Maioid Crustacea or Oxyrhyncha, with a synopsis of the families, sub-families and genera. Journal of the Linnean Society of London, Zoology, 14(79): 634-673, pls 12-13. has been traditionally considered a member of the family Mithracidae; however, recent phylogenetic studies have suggested the exclusion of Macrocoeloma from this family, being now an incertae sedis group closely allied to other Epialtidae genera (Windsor and Felder, 2014Windsor, A.M. and Felder, D.L. 2014. Molecular phylogenetics and taxonomic reanalysis of the family Mithracidae Macleay (Decapoda: Brachyura: Majoidea). Invertebrate Systematics, 28(2): 145-173. ). Currently, there are 14 described species of Macrocoeloma (see Ng et al., 2008Ng, P.K.L.; Guinot, D. and Davie, P.J.F. 2008. Systema brachyurorum: Part 1. An annotated checklist of extant brachyuran crabs of the world. The Raffles Bulletin of Zoology, 17: 1-286.), of which 10 are distributed in the western Atlantic from North Carolina to Brazil (Melo, 1996Melo, G.A.S. 1996. Manual de identificação dos Brachyura (caranguejos e siris) do litoral brasileiro. São Paulo, Plêiade/FAPESP ed., 603p.; Coelho et al., 2008Coelho, P.A., Almeida, A.O. and Bezerra, L.E.A. 2008. Checklist of the marine and estuarine Brachyura (Crustacea: Decapoda) of the northern and northeastern Brazil. Zootaxa, 1956: 1-58.). The larval development of only two Caribbean species belonging to this genus is known: that of Macrocoeloma camptocerum (Stimpson, 1871Stimpson, W. 1871. Preliminary report on the Crustacea dredged in the Gulf Stream in the Straits of Florida by L.F. de Pourtales, Assist. U. S. Coast Survey. Part I. Brachyura. Bulletin of the Museum of Comparative Zoology at Harvard College, 2(2): 109-160.) and Macrocoeloma diplacanthum (Stimpson, 1860Stimpson, W. 1860. Notes on North American Crustacea, in the Museum of the Smithsonian Institution, No. II. Annals of the Lyceum of Natural History of New York, 7(1): 177-246, Plates II and V. ). Both have been partially described in the thesis of Yang (1967Yang, W.T. 1967. A study of zoeal, megalopal, and early crab stages of some oxyrhynchous crabs (Crustacea: Decapoda). University of Miami, Coral Gables, Florida, United States, Ph.D. Dissertation. 459p. [Unpublished].), and the latter has been re-described by Marques et al. (2003Marques, F.P.L.; Pohle, G.W. and Vrbova, L. 2003. On the larval stages of Macrocoeloma diplacanthum (Decapoda: Brachyura: Majidae), with a review of mithracine phylogenetic aspects. Journal of Crustacean Biology , 23(1): 187-200.).

Macrocoeloma subparallelum (Stimpson, 1860Stimpson, W. 1860. Notes on North American Crustacea, in the Museum of the Smithsonian Institution, No. II. Annals of the Lyceum of Natural History of New York, 7(1): 177-246, Plates II and V. ) is a western Atlantic species found in the Gulf of Mexico, the Antilles, Venezuela, and in Brazil as far south as the Espírito Santo State, from shallow waters to 25 m deep (Rodriguez, 1980Rodriguez, G. 1980. Los Crustaceos Decapodos de Venezuela. Caracas, Instituto Venezolano de Investigaciones Cientificas, 494p.; Melo, 1996Melo, G.A.S. 1996. Manual de identificação dos Brachyura (caranguejos e siris) do litoral brasileiro. São Paulo, Plêiade/FAPESP ed., 603p.; Felder et al., 2009Felder, D.L; Álvarez, F.; Goy, J.W. and Lemaitre, R. 2009. Decapoda (Crustacea) of the Gulf of Mexico, with comments on the Amphionidacea. p. 1019-1104. In: D.L. Felder and D.K. Camp(eds), Gulf of Mexico Origin, Waters, and Biota, Vol 1, Biodiversity. College Station, Texas, Texas A&M University Press. ), and appears to prefer coral substrates (Rathbun, 1925Rathbun, M.J. 1925. The spider crabs of America. Bulletin of the United States National Museum, 129: 1-613.). Despite being widely distributed, M. subparallelum is rarely collected, with only very few records in the literature (e.g. Rathbun, 1925Rathbun, M.J. 1925. The spider crabs of America. Bulletin of the United States National Museum, 129: 1-613.; Rodriguez 1980Rodriguez, G. 1980. Los Crustaceos Decapodos de Venezuela. Caracas, Instituto Venezolano de Investigaciones Cientificas, 494p.; Scelzo and Varela, 1988Scelzo, M. A. and Varela, R. 1988. Crustáceos Decápodos Litorales de la Isla La Blanquilla, VenezuelaMemoria de la Sociedad de Ciencias Naturales La Salle, 47(129): 33-54.).

We describe herein the first larval stage of M. subparallelum from Cuba and compare it with the available descriptions for the genus.

Material and Methods

Two ovigerous females of M. subparallelum were collected in November 1994 in the beach of Jaimanitas, Havana, Cuba, between 1-2 meters of depth. The ovigerous females were held in an aquarium in a temperature-controlled room (24 ± 2°C) until hatching, which occurred at night. After hatching, the zoeas were fixed in 70% ethanol. Twenty specimens of the first zoeal stage were stained using methylene blue, acid fuchsin and/or chlorazol black, and then dissected in a light stereomicroscope Leica Wild M8 for morphological descriptions. For slide preparations polyvinyl lactophenol or Canada balsam were used as mounting mediums. The larval description follows the pattern used in previous works (e.g. Pohle and Marques, 2000Pohle, G. and Marques, F.P.L. 2000. Larval stages of Paradasygyius depressus Bell, 1835 (Crustacea: Decapoda: Brachyura: Majidae) and a phylogenetic analysis for 21 genera of Majidae. Proceedings of the Biological Society of Washington, 113(3): 739-760.; Santana et al., 2003Santana, W.; Pohle, G. and Marques, F. 2003. Zoeal stages and megalopa of Mithrax hispidus (Herbst, 1790) (Decapoda: Brachyura: Majoidea: Mithracidae): a reappraisal of larval characters from laboratory cultured material and a review of larvae of the Mithrax-Mithraculus species complex. Invertebrate Reproduction and Development , 44(1): 17-32.; 2004Santana, W.; Marques, F. and Pohle, G. 2004. Larval stages of Stenocionops furcatus (Olivier, 1781) (Decapoda: Brachyura: Majoidea) and a reappraisal of larval morphological characters for Mithracidae. Journal of Plankton Research, 26(8): 859-874.; Colavite et al., 2014Colavite, J.; Santana, W. and Pohle, G. 2014. Larval development of the spider crab Menaethius monoceros (Latreille, 1825) (Crustacea: Decapoda: Brachyura: Epialtidae). Journal of Natural History, 48(37-38): 2273-2292.) and the description of setae follows Pohle and Telford (1981), but here included only analysis by light microscopy (LM), using an Olympus CHA equipped with camera lucida. Some of the setae designated as plumose herein may be plumodenticulate due to the lower resolution limits of LM as compared to scanning electron microscopy (SEM). Description guidelines of Clark et al. (1998Clark, P.F.; Calazans, D.K. and Pohle, G. 1998. Accuracy and standardization of brachyuran larval descriptions. Invertebrate Reproduction and Development, 33(2-3): 127-144.) were generally followed. A minimum of five zoeae were measured for carapace length (from the basis of the rostrum to the posterior margin of the carapace in lateral view) and total length (from the tip of the rostrum to the furcal shaft in lateral view). The adult females were measured for carapace width (CW) including branchiostegal spines.

Specimens of larval stages and the two spent female crabs (CW 24.1 mm and CW 23.95 mm) have been deposited at the GICUDONE - Grupo de Investigación in Carcinologia de la Universidad de Oriente, Escuela de Ciencias Aplicadas del Mar, Margarita Island, Venezuela (accession number # GIC-1001).

Results

Morphological description

Carapace length. 0.63 mm ± 0.15 (0.61-0.65 mm).

Total length. 2.02 mm ± 0.05 (1.97-2.07 mm).

Carapace (Fig. 1A). With dorsal spine, curved posteriorly, rostral spine smooth, ventrally directed, almost reaching antenna endopod bud, lateral spines absent. Pair of short simple setae anteriorly just above eyes, simple seta dorsolaterally to dorsal spine. Ventral margin with densely plumose 'anterior setae' (Clark et al., 1998Clark, P.F.; Calazans, D.K. and Pohle, G. 1998. Accuracy and standardization of brachyuran larval descriptions. Invertebrate Reproduction and Development, 33(2-3): 127-144.) posterior to scaphognatite notch, followed by 5-6 smaller plumose setae. Eyes sessile. Small indistinct prominence frontally between dorsal spine and rostrum bearing cuticular dorsal organ (sensuMartin and Laverack, 1992Martin, J.W. and Laverack, M.S. 1992. On the distribution of the crustacean dorsal organ. Acta Zoologica, 73(5): 357-368.; Lerosey-Aubrill and Meyer, 2013Lerosey-Aubrill, R. and Meyer, R. 2013. The sensory dorsal organs of crustaceans. Biological reviews of the Cambridge Philosophical Society, 88(2): 406-426.).

Figure 1
Macrocoeloma subparallelum (Stimpson, 1860Stimpson, W. 1860. Notes on North American Crustacea, in the Museum of the Smithsonian Institution, No. II. Annals of the Lyceum of Natural History of New York, 7(1): 177-246, Plates II and V. ) first zoeal stage. (A) Lateral view; (B) antennule; (C) antenna; (D) mandible, right side; (E) mandible, left side; (F) maxillule; (G) maxilla; (H) maxilliped I; (I) maxilliped II; (J) maxilliped III and pereopods; (K) pleon. Scale bars: A, 0.3 mm; B-G, 0.1 mm.

Antennule (Fig. 1B). Unsegmented, smooth, conical. Terminally with 2 long, 2 shorter aesthetascs, 2 short simple setae.

Antenna (Fig. 1C). Birramous, protopod long, pointed, bearing two rows of sharp spinules; endopod bud approximately less than half of protopod size; exopod unsegmented, slightly longer than protopod, with long spinulated distal process; pair of setae about one third from tip, uneven, one small simple, one larger serrulate.

Mandible (Fig. 1D, E). Asymmetrical, with medial toothed molar processes uneven; enlarged lateral incisor processes; 2-3 marginal teeth between molar and incisor processes. Internal margin of incisor processes with a series of teeth, ending in a larger tooth in both mandibles. Palp absent.

Maxillule (Fig. 1F). Coxal endite with seven setae: four terminal graded plumodenticulate, 3 plumodenticulate subterminally. Basial endite with seven setae: five terminal plumodenticulate cuspidate, one subterminal plumodenticulate, one plumose proximally. Two-segmented endopod, proximal segment with long plumodenticulate seta, distal segment with five long plumodenticulate setae: one subapical, four apical. Exopod seta absent.

Maxilla (Fig. 1G). Coxal endite bilobed, proximal lobe with 4-5 setae: 3-4 plumose, 1 plumodenticulate; distal lobe with five plumodenticulate setae. Microtrichia present on both endites. Basial endite bilobed, proximal and distal lobes with five and four plumodenticulate setae, respectively. Endopod unsegmented, unilobed, with five plumodenticulate apical setae; microtrichia on lateral margin. Scaphognatite marginally with 10-11 densely plumose setae, including distal process.

Maxilliped I (Fig. 1A, H). Coxa without seta. Basis with 10 plumodenticulate setae arranged 2+2+3+3. Endopod 5-segmented with 3,2,1,2,4 plumodenticulate setae, with strong accessory spine on distal segment. Exopod incompletely bisegmented with four plumose terminal natatory setae.

Maxilliped II (Fig. 1A, I). Coxa without seta. Basis with three plumodenticulate setae. Endopod three-segmented, with 0,1,4 sparsely plumodenticulate setae, distal segment with three subapical, two apical setae. Exopod incompletely bisegmented with four plumose terminal natatory setae.

Maxilliped III (Fig. 1A, J). Present as a small bud. Endo and exopod distinct.

Pereopods (Fig. 1A, J). Present as small buds, chela distinct, without apparent segmentation.

Pleon (Fig. 1A, K). Five pleonites. First pleonite with pair of middorsal, long, plumodenticulate setae, pleonites 2-5 with pair of shorter posterodorsal simple setae each. Posterolateral margin of second pleonite with blunt process, pleonites 3-5 with spines; second pleonite with pair of dorsolateral processes. Pleopod buds rudimentary.

Telson (Fig. 1K). Bifurcated, indistinct median notch, three pairs of plumodenticulate setae (Type 13-viii sensuPohle and Telford, 1981Pohle, G. and Telford, M. 1981. Morphology and classification of decapod crustacean larval setae: a scanning electron microscope study of Dissodactylus crinitichelis Moreira, 1901 (Brachyura: Pinnotheridae). Bulletin of Marine Science, 31(3): 736-752.) on inner margin; each furcal shaft proximally bearing a distinct lateral spine, furcal shafts covered with rows of spinules to just below the tips.

Discussion

Macrocoeloma subparallelum closely resembles congeners for which the first larval stage has been described. Macrocoeloma subparallelum, M. diplacanthum and M. camptocerum differ only in the number of aesthetascs and setae of the antennule; while the former has 4 aesthetascs and 2 setae, the latter two have 3 and 1, respectively. Another minor difference can be observed in the number of setae in the ventral margin of the carapace: M. subparallelum and M. diplacanthum have six to seven setae, while M. camptocerum has only six (Yang, 1967Yang, W.T. 1967. A study of zoeal, megalopal, and early crab stages of some oxyrhynchous crabs (Crustacea: Decapoda). University of Miami, Coral Gables, Florida, United States, Ph.D. Dissertation. 459p. [Unpublished].; Marques et al., 2003Marques, F.P.L.; Pohle, G.W. and Vrbova, L. 2003. On the larval stages of Macrocoeloma diplacanthum (Decapoda: Brachyura: Majidae), with a review of mithracine phylogenetic aspects. Journal of Crustacean Biology , 23(1): 187-200.).

The larvae of the genus Macrocoeloma can be easily recognized through a combination of characteristics including the presence of a distended forehead with strong underlying muscle bands, a dorsal spine, and a distinct, strong spine in the distal segment of the endopod of the first maxilliped (Yang, 1967Yang, W.T. 1967. A study of zoeal, megalopal, and early crab stages of some oxyrhynchous crabs (Crustacea: Decapoda). University of Miami, Coral Gables, Florida, United States, Ph.D. Dissertation. 459p. [Unpublished].; Marques et al., 2003Marques, F.P.L.; Pohle, G.W. and Vrbova, L. 2003. On the larval stages of Macrocoeloma diplacanthum (Decapoda: Brachyura: Majidae), with a review of mithracine phylogenetic aspects. Journal of Crustacean Biology , 23(1): 187-200.). All of these characteristics are present in M. subparallelum. As noted by Marques et al. (2003)Marques, F.P.L.; Pohle, G.W. and Vrbova, L. 2003. On the larval stages of Macrocoeloma diplacanthum (Decapoda: Brachyura: Majidae), with a review of mithracine phylogenetic aspects. Journal of Crustacean Biology , 23(1): 187-200., this distinct spine can also be found in other Epialtidae species, such as Menaethius monoceros (Latreille, 1825Latreille, P.A. 1825. Histoire Naturelle. Entomologie, ou Histoire naturelle des Crustacés, des Arachnides et des Insectes. Encyclopédie Méthodique, Vol. 10. Paris, Agasse Imprimeur-Libraire, 832p.), PugettiaDana, 1851Dana, J.D. 1851. On the classification of the maioid Crustacea or Oxyrhyncha. American Journal of Science, series 2, 11(33): 425-434. and HueniaDe Haan, 1837 de Haan, W. 1833-1850. Crustacea. In: P.F. von Siebold (ed) Fauna Japonica sive Descriptio Animalium, Quae in Itinere per Japoniam, Jussu et Auspiciis Superiorum, qui Summum in India Batava Imperium Tenent, Suscepto, Annis 1823-1830 Collegit, Noitis, Observationibus et Adumbrationibus Illustravit. Leiden, Lugduni-Batavorum. p. i-xvii, i-xxxi, ix-xvi, 1-243, Pls A-J, L-Q, 1-55, circ. tab. 2(see Ko, 1998Ko, H.S. 1998. Zoeal development of three species of Pugettia (Decapoda: Majidae) with a key to the known zoeas of the subfamily Epialtinae. Journal of Crustacean Biology , 18(3): 499-510.; Kornienko and Korn, 2004Kornienko, E.S. and Korn, O.M. 2004. Morphological features of the larvae of spider crab Pugettia quadridens (Decapoda: Majidae) from the northwestern Sea of Japan. Russian Journal of Marine Biology, 30(6): 402-413.; Marques et al., 2003Marques, F.P.L.; Pohle, G.W. and Vrbova, L. 2003. On the larval stages of Macrocoeloma diplacanthum (Decapoda: Brachyura: Majidae), with a review of mithracine phylogenetic aspects. Journal of Crustacean Biology , 23(1): 187-200.; Colavite et al., 2014Colavite, J.; Santana, W. and Pohle, G. 2014. Larval development of the spider crab Menaethius monoceros (Latreille, 1825) (Crustacea: Decapoda: Brachyura: Epialtidae). Journal of Natural History, 48(37-38): 2273-2292.).

Majoid crabs have a confusing taxonomic history due to several changes in the status of the families and subfamilies and the lack of substantial characters that support grouping of genera at higher taxonomic levels (Ng et al., 2008Ng, P.K.L.; Guinot, D. and Davie, P.J.F. 2008. Systema brachyurorum: Part 1. An annotated checklist of extant brachyuran crabs of the world. The Raffles Bulletin of Zoology, 17: 1-286.). A combination of adult, molecular, and larval characters could be the best way to find diagnostic characteristics for some groups. Despite the placement of Macrocoeloma as an incertae sedis group by Windsor and Felder (2014Windsor, A.M. and Felder, D.L. 2014. Molecular phylogenetics and taxonomic reanalysis of the family Mithracidae Macleay (Decapoda: Brachyura: Majoidea). Invertebrate Systematics, 28(2): 145-173. ), this genus nested close to other Epialtidae and Pisinae members in their analyses. This is what we observe in the first zoeal stage of this genus, with the distinct spine in the distal segment of the endopod of the first maxilliped. This character is similar to what we see in other Epialtidae genera, which supports the recent phylogenetic studies (Windsor and Felder, 2014). However, Epialtidae is the most speciose family of Majoidea, with 452 recognized species (Davie et al., 2015Davie, P.J.; Guinot, D. and Ng, P.K. 2015. Systematics and classification of Brachyura. p. 1049-1130. In: P. Castro; P.J.F. Davie; D. Guinot; F.R. Schram and J.C. von Vaupel Klein (eds), Treatise on Zoology - Anatomy, Taxonomy, Biology . The Crustacea, Vol. 9, Part C (2 vol.). Leiden, Brill .), and shows a high degree of variability in several larval characters (see Clark and Cuesta, 2015Clark, P.F. and Cuesta, J.A. 2015. Larval systematics of Brachyura. p. 981-1048. In: P. Castro; P.J.F. Davie; D. Guinot; F.R. Schram and J.C. von Vaupel Klein (eds), Treatise on Zoology - Anatomy, Taxonomy, Biology. The Crustacea, Vol. 9, Part C (2 vol.). Leiden, Brill.). This could indicate that Epialtidae is not monophyletic in its present composition suggesting the taxonomic reevaluation and additional phylogenetic studies to better define Epialtidae in general and the position of Macrocoeloma in particular.

Acknowledgements

We thank the Universidad de Oriente - UDO, Venezuela, and the Universidade do Sagrado Coração - USC, Brazil for supporting studies on the systematics of decapod crustaceans. This work was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo - FAPESP (WS grant number 2013/01201-0 and JC fellowship number 2016/02775-8).

References

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