Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Revision of the Parasesarma guttatum species complex reveals a new pseudocryptic species in south-east African mangroves

Sara Fratini https://orcid.org/0000-0002-5754-8830 A B G , Stefano Cannicci https://orcid.org/0000-0002-4504-0765 A C , Francesca Porri D E and Gianna Innocenti F
+ Author Affiliations
- Author Affiliations

A Department of Biology, University of Florence, via Madonna del Piano 6, Sesto Fiorentino, Italy.

B Mangrove Specialist Group, IUCN Species Survival Commission, 28 rue Mauverney, CH-1196 Gland, Switzerland.

C The Swire Institute of Marine Science and the School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Hong Kong, Hong Kong SAR.

D South African Institute for Aquatic Biodiversity, Private Bag 1015, 6140 Grahamstown, South Africa.

E Department of Zoology & Entomology, Rhodes University, 6140 Grahamstown, South Africa.

F Natural History Museum, Zoological Section, University of Florence, via Romana 17, I-50125 Florence, Italy.

G Corresponding author. Email: sara.fratini@unifi.it

Invertebrate Systematics 33(1) 208-224 https://doi.org/10.1071/IS18028
Submitted: 30 March 2018  Accepted: 12 September 2018   Published: 6 February 2019

Abstract

Parasesarma De Man, 1895 is the most speciose genus in the family Sesarmidae (Decapoda: Brachyura: Thoracotremata). In the western Indian Ocean, Parasesarma is represented by five species only, although some genetic evidence suggests that P. guttatum could be a species complex comprising two cryptic species. Accordingly, P. guttatum is here split into two pseudocryptic species, and a new species, Parasesarma capensis, sp. nov., is described. P. capensis, sp. nov. fills the same ecological niche as P. guttatum south of the Mozambique Channel. While variation in mitochondrial DNA and morphological differences clearly distinguish the two species, there is no nuclear genetic variation. This may reflect a short history of reproductive isolation. The distinguishing morphological characters of the new species are the 13–15 rounded tubercles on the movable finger, the upper surface of the palm with three transverse crests (one regularly tuberculate and two pectinated), and the shape of the first gonopod. Phylogenetic inference analyses show a sister-species relationship between P. guttatum and P. capensis, sp. nov., and strongly suggest that at least two East African Parasesarma species need a taxonomic revision. The description of this new sesarmid species from the south-eastern African coast sheds new light on the overall biogeographic patterns and general biodiversity of this taxon within the western Indian Ocean.

Additional keywords: mitochondrial DNA, nuclear marker, Sesarmidae, speciation, systematic relationship, taxonomy.


References

Avise, J. C. (2004). ‘Molecular Markers, Natural History and Evolution.’ 2nd edn. (Sinauer Associates: Sunderland, MA.)

Bickford, D., Lohman, D. J., Sohdi, N. S., Ng, P. K., Meier, R., Winker, K., Ingram, K., and Das, I. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22, 148–155.
Cryptic species as a window on diversity and conservation.Crossref | GoogleScholarGoogle Scholar |

Bolton, J. J., Leliaert, F., de Clerck, O., Anderson, R. J., Stegenga, H., Engledow, H. E., and Coppejans, E. (2004). Where is the western limit of the tropical Indian Ocean seaweed flora? An analysis of intertidal seaweed biogeography on the east coast of South Africa. Marine Biology 144, 51–59.
Where is the western limit of the tropical Indian Ocean seaweed flora? An analysis of intertidal seaweed biogeography on the east coast of South Africa.Crossref | GoogleScholarGoogle Scholar |

Cannicci, S., Ritossa, S., Ruwa, R. K., and Vannini, M. (1996). Tree fidelity and hole fidelity in the tree crab Sesarma leptosoma (Decapoda, Grapsidae). Journal of Experimental Marine Biology and Ecology 196, 299–311.
Tree fidelity and hole fidelity in the tree crab Sesarma leptosoma (Decapoda, Grapsidae).Crossref | GoogleScholarGoogle Scholar |

Cannicci, S., Burrows, D., Fratini, S., Smith, T. J., Offemberg, J., and Dahdouh-Guebas, F. (2008). Faunal impact on vegetation structure and ecosystem function in mangrove forests: a review. Aquatic Botany 89, 186–200.
Faunal impact on vegetation structure and ecosystem function in mangrove forests: a review.Crossref | GoogleScholarGoogle Scholar |

Cannicci, S., Bartolini, F., Dahdouh-Guebas, F., Fratini, S., Litulo, C., Macia, A., Mrabu, E. J., Penha-Lopes, G., and Paula, J. (2009). Effects of urban wastewater on crab and mollusc assemblages in equatorial and subtropical mangroves of East Africa. Estuarine, Coastal and Shelf Science 84, 305–317.
Effects of urban wastewater on crab and mollusc assemblages in equatorial and subtropical mangroves of East Africa.Crossref | GoogleScholarGoogle Scholar |

Cannicci, S., Schubart, C. D., Innocenti, G., Dahdouh-Guebas, F., Shahdadi, A., and Fratini, S. (2017). A new species of the genus Parasesarma De Man 1895 from East African mangroves and evidence for mitochondrial introgression in sesarmid crabs. Zoologischer Anzeiger 269, 89–99.
A new species of the genus Parasesarma De Man 1895 from East African mangroves and evidence for mitochondrial introgression in sesarmid crabs.Crossref | GoogleScholarGoogle Scholar |

Chu, K. H., Schubart, C. D., Shih, H. T., and Tsang, L. M. (2015). Genetic diversity and evolution of Brachyura. In ‘Treatise on Zoology – Anatomy, Taxonomy, Biology – The Crustacea, Complementary to the Volumes translated from the French of the Traité de Zoologie 9(C)(I), Decapoda: Brachyura (Part 1). (Eds P. Castro, P. J. F. Davie, D. Guinot, F. R. Schram and J. C. von Vaupel Klein.) pp. 775–820. (Brill: Leiden.)

Clemens, S. C., Murray, D. W., and Prell, W. L. (1996). Non stationary phase of the Plio-Pleistocene Asian Monsoon. Science 274, 943–948.
Non stationary phase of the Plio-Pleistocene Asian Monsoon.Crossref | GoogleScholarGoogle Scholar | 8875928PubMed |

Clement, M., Posada, D., and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 11050560PubMed |

Crosnier, A. (1965). Crustacés Décapodes. Grapsidae et Ocypodidae. Faune de Madagascar 18, 1–143.

Dahdouh-Guebas, F., Giuggioli, M., Oluoch, A., Vannini, M., and Cannicci, S. (1999). Feeding habits of non-ocypodid crabs from two mangrove forests in Kenya. Bulletin of Marine Science 64, 291–297.

Dahdouh-Guebas, F., Verneirt, M., Cannicci, S., Kairo, J. G., Tack, J. F., and Koedam, N. (2002). An exploratory study on grapsid crab zonation in Kenyan mangroves. Wetlands Ecology and Management 10, 179–187.
An exploratory study on grapsid crab zonation in Kenyan mangroves.Crossref | GoogleScholarGoogle Scholar |

Davie, P. J. F., Guinot, D., and Ng, P. K. L. (2015). Phylogeny of Brachyura. In ‘Treatise on Zoology – Anatomy, Taxonomy, Biology – The Crustacea, Complementary to the Volumes translated from the French of the Traité de Zoologie 9(C)(I), Decapoda: Brachyura (Part 1). (Eds P. Castro, P. J. F. Davie, D. Guinot, F. R. Schram and J. C. von Vaupel Klein.) pp. 921–980. (Brill: Leiden.)

De Grave, S., Pentcheff, N. D., Ahyong, S. T., Chan, T., Crandall, K. A., Dworschak, P. C., Felder, D. L., Feldman, R. M., Fransen, C. H. J. M., Goulding, L. Y. D., Lemaitre, R., Low, M. E. Y., Martin, J. W., Ng, P. K. L., Schweitzer, C. E., Tan, S. H., Tshudy, D., and Wetzer, R. (2009). A classification of living and fossil genera of decapod crustaceans. The Raffles Bulletin of Zoology 21, 1–109.

de Ruijter, W. P. M., Ridderinkhof, H., and Ludjeharms, R. E. (2002). Observation of the flow in the Mozambique Channel. Geophysical Research Letters 29, 1401–1403.
Observation of the flow in the Mozambique Channel.Crossref | GoogleScholarGoogle Scholar |

Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
| 22367748PubMed |

Excoffier, L., Laval, L. G., and Schneider, S. (2005). Arlequin, version 3: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.

Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar | 28561359PubMed |

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 7881515PubMed |

Fratini, S., Vannini, M., Cannicci, S., and Schubart, C. D. (2005). Tree-climbing mangrove crabs, a case of convergent evolution. Evolutionary Ecology Research 7, 219–233.

Fratini, S., Ragionieri, L., and Cannicci, S. (2010). Stock structure and demographic history of the Indo-West Pacific mud crab Scylla serrata. Estuarine, Coastal and Shelf Science 86, 51–61.
Stock structure and demographic history of the Indo-West Pacific mud crab Scylla serrata.Crossref | GoogleScholarGoogle Scholar |

Fratini, S., Ragionieri, L., and Cannicci, S. (2016). Demographic history and reproductive output correlates with intraspecific genetic variation in seven species of Indo-Pacific mangrove crabs. PLoS One , .
Demographic history and reproductive output correlates with intraspecific genetic variation in seven species of Indo-Pacific mangrove crabs.Crossref | GoogleScholarGoogle Scholar | 27379532PubMed |

Fusi, M., Giomi, F., Babbini, S., Daffonchio, D., McQuaid, C. D., Porri, F., and Cannicci, S. (2014). Thermal specialization across large geographical scales predicts the resilience of mangrove crab populations to global warming. Oikos 124, 784–795.
Thermal specialization across large geographical scales predicts the resilience of mangrove crab populations to global warming.Crossref | GoogleScholarGoogle Scholar |

Gillikin, D. P., and Schubart, C. D. (2004). Ecology and systematics of mangrove crabs of the genus Perisesarma (Crustacea: Brachyura: Sesarmidae) from East Africa. Zoological Journal of the Linnean Society 141, 435–445.
Ecology and systematics of mangrove crabs of the genus Perisesarma (Crustacea: Brachyura: Sesarmidae) from East Africa.Crossref | GoogleScholarGoogle Scholar |

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.

Hartnoll, R. G. (1975). The Grapsidae and Ocypodidae (Decapoda: Brachyura) of Tanzania. Journal of Zoology 177, 305–328.
The Grapsidae and Ocypodidae (Decapoda: Brachyura) of Tanzania.Crossref | GoogleScholarGoogle Scholar |

Hebert, P. D. N., Ratnasingham, S., and de Ward, J. R. (2003a). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings. Biological Sciences 270, S96–S99.
Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species.Crossref | GoogleScholarGoogle Scholar |

Hebert, P. D. N., Cywinska, A., Ball, S. L., and deWaard, J. R. (2003b). Biological identifications through DNA barcodes. Proceedings. Biological Sciences 270, 313–321.
Biological identifications through DNA barcodes.Crossref | GoogleScholarGoogle Scholar |

Kumar, S., Tamura, K., and Nei, M. (2004). MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.
MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment.Crossref | GoogleScholarGoogle Scholar | 15260895PubMed |

Lutjeharms, J. R. E., Wedepohl, P. M., and Meeuwis, J. M. (2000). On the surface drift at the East Madagascar and the Mozambique Currents. South African Journal of Science 96, 141–147.

Milne-Edwards, A. (1869). Note sur quelques nouvelles espèces du genre Sesarma (Say). Nouvelles archives du Muséum d’Histoire naturelle 5, 25–31.

Múrias dos, , Santos, A. M., Cabezas, M. P., Tavares, A. I., Xavier, R., and Branco, M. (2015). tcsBU: a tool to extend TCS network layout and visualization. Bioinformatics 32, 627–628.
tcsBU: a tool to extend TCS network layout and visualization.Crossref | GoogleScholarGoogle Scholar |

Naderloo, R., Schubart, C. D., and Shih, H.-T. (2016). Genetic and morphological separation of Uca occidentalis, a new East African fiddler crab species, from Uca annulipes (H. Milne Edward, 1837) (Crustacea: Decapoda: Brachyura: Ocypodidae). Zoologischer Anzeiger 262, 10–19.
Genetic and morphological separation of Uca occidentalis, a new East African fiddler crab species, from Uca annulipes (H. Milne Edward, 1837) (Crustacea: Decapoda: Brachyura: Ocypodidae).Crossref | GoogleScholarGoogle Scholar |

Nei, M. (1987). ‘Molecular Evolutionary Biology.’ (Columbia University Press: New York.)

Ng, P. K. L., Guinot, D., and Davie, P. J. F. (2008). Systema Brachyurorum: part I. An annotated checklist of extant brachyuran crabs of the world. The Raffles Bulletin of Zoology 17, 1–286.

Ng, P. K. L., Davie, P. J. F., and Li, J. (2016). On the identities of Parasesarma carolinense (Rathbun, 1907) and Parasesarma sigillatum (Tweedie, 1950), with description of a new species from Taiwan (Crustacea: Brachyura: Sesarmidae). The Raffles Bulletin of Zoology 64, 257–268.

Peakall, R., and Smouse, P. E. (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28, 2537–2539.
GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update.Crossref | GoogleScholarGoogle Scholar | 22820204PubMed |

Posada, D., and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
Modeltest: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 9918953PubMed |

Quisthoudt, K., Adams, J., Rajkaran, A., Dahdouh-Guebas, F., Koedam, N., and Randin, C. F. (2013). Disentangling the effects of global climate and regional land-use change on the current and future distribution of mangroves in South Africa. Biodiversity and Conservation 22, 1369–1390.
Disentangling the effects of global climate and regional land-use change on the current and future distribution of mangroves in South Africa.Crossref | GoogleScholarGoogle Scholar |

Ragionieri, L., Fratini, S., Vannini, M., and Schubart, C. D. (2009). Phylogenetic and morphometric differentiation reveal geographic radiation and pseudo-cryptic speciation in a mangrove crab from the Indo-West Pacific. Molecular Phylogenetics and Evolution 52, 825–834.
Phylogenetic and morphometric differentiation reveal geographic radiation and pseudo-cryptic speciation in a mangrove crab from the Indo-West Pacific.Crossref | GoogleScholarGoogle Scholar | 19394431PubMed |

Ragionieri, L., Cannicci, S., Schubart, C. D., and Fratini, S. (2010). Gene flow and demographic history of the mangrove crab Neosarmatium meinerti: a case study from the western Indian Ocean. Estuarine, Coastal and Shelf Science 86, 179–188.
Gene flow and demographic history of the mangrove crab Neosarmatium meinerti: a case study from the western Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Ragionieri, L., Fratini, S., and Schubart, C. D. (2012). Revision of the Neosarmatium meinerti species complex (Decapoda: Brachyura: Sesarmidae), with descriptions of three pseudocryptic Indo-West Pacific species. The Raffles Bulletin of Zoology 60, 71–87.

Rambaut, A., Suchard, M. A., Xie, D., and Drummond, A. J. (2014). Tracer v1.6. Available from: http://beast.bio.ed.ac.uk/Tracer [Verified 3 January 2019].

Rodríguez, F., Oliver, J. F., Marín, A., and Medina, J. R. (1990). The general stochastic model of nucleotide substitution. Journal of Theoretical Biology 142, 485–501.
| 2338834PubMed |

Sambrook, J., and Russell, D. W. (2001). ‘Molecular Cloning: a Laboratory Manual.’ (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY.)

Schouten, M. W. Schouten, M. W. (2003). Eddies and variability in the Mozambique Channel. Deep-sea Research. Part II, Topical Studies in Oceanography 50, 1987–2003.
Eddies and variability in the Mozambique Channel.Crossref | GoogleScholarGoogle Scholar |

Schubart, C. D., and Huber, M. G. J. (2006). Genetic comparisons of German populations of the stone crayfish, Austropotamobius torrentium (Crustacea: Astacidae). Bulletin français de la pêche et de la protection des milieux aquatiques 380–381, 1019–1028.

Schubart, C. D., Diesel, R., and Hedges, S. B. (1998). Rapid evolution to terrestrial life in Jamaican crabs. Nature 393, 363–365.
Rapid evolution to terrestrial life in Jamaican crabs.Crossref | GoogleScholarGoogle Scholar |

Schubart, C. D., Cannicci, S., Vannini, M., and Fratini, S. (2006). Molecular phylogeny of grapsoid crabs from East Africa based on two mitochondrial genes and a proposal for refraining from current superfamily classification. Journal of Zoological Systematics and Evolutionary Research 44, 193–199.
Molecular phylogeny of grapsoid crabs from East Africa based on two mitochondrial genes and a proposal for refraining from current superfamily classification.Crossref | GoogleScholarGoogle Scholar |

Shahdadi, A., and Schubart, C. D. (2017). Taxonomic review of Perisesarma (Decapoda: Brachyura: Sesarmidae) and closely related genera based on morphology and molecular phylogenetics: new classification, two new genera and the questionable phylogenetic value of the epibranchial tooth. Zoological Journal of the Linnean Society 182, 517–548.
Taxonomic review of Perisesarma (Decapoda: Brachyura: Sesarmidae) and closely related genera based on morphology and molecular phylogenetics: new classification, two new genera and the questionable phylogenetic value of the epibranchial tooth.Crossref | GoogleScholarGoogle Scholar |

Silva, I. C., Mesquita, N., and Paula, J. (2010). Genetic and morphological differentiation of the mangrove crab Perisesarma guttatum (Brachyura: Sesarmidae) along an East African latitudinal gradient. Biological Journal of the Linnean Society. Linnean Society of London 99, 28–46.
Genetic and morphological differentiation of the mangrove crab Perisesarma guttatum (Brachyura: Sesarmidae) along an East African latitudinal gradient.Crossref | GoogleScholarGoogle Scholar |

Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., and Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.
Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers.Crossref | GoogleScholarGoogle Scholar |

Skov, M. W., Vannini, M., Shunula, J. P., Hartnoll, R. G., and Cannicci, S. (2002). Quantifying the density of mangrove crabs: Ocypodidae and Grapsidae. Marine Biology 141, 725–732.
Quantifying the density of mangrove crabs: Ocypodidae and Grapsidae.Crossref | GoogleScholarGoogle Scholar |

Slim, F. J., Hemminga, M. A., Ochieng, C., Jannink, N. T., Cocheret de la Morinière, E., and van der Velde, G. (1997). Leaf litter removal by the snail Terebralia palustris (Linnaeus) and sesarmid crabs in an East African mangrove forest (Gazi Bay, Kenya). Journal of Experimental Marine Biology and Ecology 215, 35–48.
Leaf litter removal by the snail Terebralia palustris (Linnaeus) and sesarmid crabs in an East African mangrove forest (Gazi Bay, Kenya).Crossref | GoogleScholarGoogle Scholar |

Swofford, D. L. (2002). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods).’ (Sinauer Associates: Sunderland, MA.)

Teske, P. R., von der Heyden, S., McQuaid, C. D., and Barker, N. P. (2011). A review of marine phylogeography in southern Africa. South African Journal of Science 107, 43–53.
A review of marine phylogeography in southern Africa.Crossref | GoogleScholarGoogle Scholar |

Tsang, L. M., Achituv, Y., Chu, K. H., and Chan, B. K. K. (2012). Zoogeography of intertidal communities in the west Indian Ocean as determined by ocean circulation systems: patterns from the Tetraclita barnacles. PLoS One 7, e45120.
Zoogeography of intertidal communities in the west Indian Ocean as determined by ocean circulation systems: patterns from the Tetraclita barnacles.Crossref | GoogleScholarGoogle Scholar | 23024801PubMed |

Vannini, M., and Valmori, P. (1981). Researches on the coast of Somalia. The shore and the dune of Sar Uanle. 30. Grapsidae (Decapoda Brachyura). Monitore Zoologico Italiano (N.S.). Supplemento XIV 14, 57–101.