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Cardisoma Guanhumi Latreille, 1825) in a Restricted‑Access Mangrove Area, Analyzed Using PIT Tags Denise Moraes‑Costa1 and Ralf Schwamborn2*

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Cardisoma Guanhumi Latreille, 1825) in a Restricted‑Access Mangrove Area, Analyzed Using PIT Tags Denise Moraes‑Costa1 and Ralf Schwamborn2* Moraes‑Costa and Schwamborn Helgol Mar Res (2018) 72:1 https://doi.org/10.1186/s10152-017-0504-0 Helgoland Marine Research ORIGINAL ARTICLE Open Access Site fdelity and population structure of blue land crabs (Cardisoma guanhumi Latreille, 1825) in a restricted‑access mangrove area, analyzed using PIT tags Denise Moraes‑Costa1 and Ralf Schwamborn2* Abstract Understanding the patterns of displacement and site fdelity in blue land crabs (Cardisoma guanhumi Latreille, 1825) has important implications for their conservation and management. The central objective of this study was to analyze seasonal variations in site fdelity in C. guanhumi, a species that is intensively exploited in Brazil, in spite of being part of the Ofcial National List of Critically Endangered Species. This species currently sufers multiple severe threats, such as overharvesting and habitat destruction. C. guanhumi were sampled monthly at four fxed sectors that were delim‑ ited at the upper fringe of a restricted-access mangrove at Itamaracá Island between April 2015 and March 2016. One thousand and seventy-eight individuals were captured, measured, sexed, weighed, and their color patterns registered. Of these, 291 individuals were tagged with PIT (Passive Integrated Transponder) tags. Ninety-seven individuals (size range 27.0–62.6 mm carapace width) were successfully recaptured, totaling 135 recapture events. The largest interval between marking and recapture was 331 days. Through the use of mark-recapture-based models, it was possible to 2 estimate the local population as being 1312 ( 417) individuals (mean density 2.23 0.71 ind. m­ − ). Considering the mean density of burrow openings and individuals,± there were 3.4 burrow openings± per individual. C. guanhumi showed a clear philopatric behavior. Seventy-seven percent of recaptured individuals were recaptured in their sector of origin, and the remainder in an adjacent sector. Site fdelity was higher in females. Males showed minimum site fdelity in October, which is most likely related to be the onset of the reproductive season. The present study opens new perspectives for the defnition of reproductive seasons, based on seasonal changes in behavior, and thus to improve the conservation of exploited and severely threatened species. Keywords: Cardisoma guanhumi, PIT tags, Mark-recapture, Philopatric behavior, Diel and seasonal activity patterns, Mangroves Background Various species of decapod crustaceans clearly defne Many animals identify home ranges that they use for for- a home range for foraging and shelter, the regularity aging, shelter [1, 2] and for reproduction [3]. Philopatric and magnitude of dispersion being linked to the balance behavior, i.e., the tendency to prefer, stay in or return to between the intensity of territorial and philopatric behav- a specifc site, has consequences for many areas of biol- ior, foraging ranges, reproductive migrations, and exploi- ogy and ecology, for example in population dynamics [4], tation of new habitats [8]. Carnivorous crabs (Carcinus sexual selection [5], orientation [6] and conservation [7]. maenas) may afect the structure of local oyster beds through philopatric, site-specifc predation [9]. Ocypo- *Correspondence: [email protected] did ghost crabs [10, 11], lobsters [12] and tropical land 2 Department of Oceanography, Federal University of Pernambuco crabs [13] have the ability to return to the same sites after (UFPE), Av. Arquitetura, s/no, CDU, Recife, PE 50670‑901, Brazil foraging, thus showing a strong philopatric behavior. Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Moraes‑Costa and Schwamborn Helgol Mar Res (2018) 72:1 Page 2 of 15 Cardisoma guanhumi Latreille, 1825 (the blue land [30, 31]; Ucides cordatus [32]; Birgus latro [33] and Card- crab, locally known as guaiamum, goiamum or guaiamu), isoma guanhumi [18, 34]. Te latter studies investigated is a brachyuran belonging to the Gecarcinidae family, large-scale spatial displacement and abundance of indi- which inhabits the supralittoral upper fringes of man- viduals at diferent sites in Puerto Rico. groves, grass felds, shrubs and forests [14]. It occurs In this study, we investigated the small-scale site fdelity from Florida (USA), to the state of Santa Catarina, Brazil of C. guanhumi using PIT tags and tested the existence [15, 16]. of seasonal patterns of site fdelity in these crustaceans, Being considered a herbivore–detritivore, its diet has as well as possible diferences between sexes. Also, we been reported to include insects, carrion, feces and even evaluated the size of the population and the relationship members of its own species [15, 17]. Te blue land crab between crab densities and the density and size of bur- plays an important role as a source of income and food row openings. for local people in the Caribbean and Brazil [15, 18, 19] and has a high socio-economic and socio-cultural impor- Methods tance in the Brazilian northeast [20]. Study area Cardisoma guanhumi is a gregarious species, where Te study area (Fig. 1) is a well-preserved mangrove these crabs build deep burrows or galleries in sandy and patch located inside the National Center for Research muddy soils and does not usually share them [15]. Te and Conservation of Aquatic Mammals of the Brazilian burrows are deep and tortuous [21, 22], always extending ICMBio agency (CMA/ICMBio), at Itamaracá Island, into the groundwater [14]. Pernambuco State, Brazil (07°48′36″S, 034°50′26″W at Individuals of C. guanhumi tolerate environments that 07°48′31″S, 034°50′15″W). are highly contaminated with household waste, sewage Te vegetation inside the mangrove patch is charac- and chemical contaminants of water and soil [22]. Adult terized by Rhizophora mangle and Conocarpus erectus. C. guanhumi can withstand high levels of acidity, salinity Four sampling sectors (A, B, C and D) were defned at and hypoxia [23]. the upper fringe of the mangrove, where Cardisoma Despite the probable advantage over many other spe- guanhumi burrows were observed (Fig. 1). Additionally cies regarding pollutant tolerance and soil type pref- to the mangrove tree species R. mangle and C. erectus, erence, this species is severely threatened by human typical beach vegetation also occurred at the sampling interventions such as overharvesting and the destruction sites, such as Terminalia catappa and Syzygium cumini, of its coastal and estuarine habitats. forming a line of dense shrubs at the upper margin of the Several studies have addressed specifc aspects of the mangrove. biology of C. guanhumi [14, 24, 25], as well as popula- According to the classifcation of Köppen [35], the tion aspects [26]. Yet, there are no studies on the season- climate of Itamaracá Island, Pernambuco, is of the wet ality of individual behavior or small-scale site fdelity for tropical type Ams’ [36]. Te rainy season in this region this important land crab. Te hypothesis that C. guan- reaches from March to August, the peak dry season humi returns to its home site after foraging excursions from November to January. Monthly accumulated rain- is of great ecological and socio-economic interest. Is fall values at Itamaracá during peak rainy season, in June site fdelity equal between males and females? How are and July 2015, were 234.1 and 291.0 mm, respectively. these crabs distributed in their home ranges? Are there During peak dry season, rainfall in Itamaracá was zero seasonal variations in site fdelity, that may be related to in November 2015, 88.5 mm in December 2015 and climatic and reproductive cycles? 65.2 mm in January 2016 [37]. In recent years, there has been a sharp decline in the populations of these brachyurans in Brazil. Tus, in 2004, Sampling strategy this species was included in the “Brazilian List of Aquatic Four sectors were established along the upper fringe of Invertebrates and Overexploited or Treatened Fishes” the CMA mangrove, designated A, B, C and D, with a [27]. Ten years later, C. guanhumi was listed in the “Of- total upper edge length of 189 m (Fig. 1). Crabs that cial National List of Endangered Species” as a “Critically were sampled in each sector were generally released at Endangered” species [28], remaining in this category a fixed point located at the center of their home sec- until the present day. tor, except during a translocation experiment (Experi- In order to study animals in natural environments, it is ment II, see below). The four release points were 46 m often necessary to mark them individually. More recently, (A–B), 66 m (B–C) and 59 m (C–D) apart from each PIT (Passive Integrated Transponder) tagging was used other. The four sectors had the following approximate for several crustacean species: Macrobrachium rosenber- upper edge lengths: 29, 51, 61 and 48 m, respectively gii and Cancer magister [29]; Paralithodes camtschaticus (Fig. 1). Moraes‑Costa and Schwamborn Helgol Mar Res (2018) 72:1 Page 3 of 15 Fig. 1 Map of the study area showing sampling sectors A, B, C and D, at the upper fringe of the CMA mangrove at Itamaracá Island, Pernambuco State, Brazil Within these four sectors, sixteen transects perpendic- Te maximum extent of recognizable C. guanhumi ular to the upper margin of the mangrove (4 transects per burrows into the vegetation at the upper edge of the sector) provided a framework for a detailed mapping of mangrove was estimated to be on average three meters, 2 the distribution, bathymetry and relief of crab burrows, resulting in a total area of 189 m × 3 m = 567 m , when including the measurement of the diameters and densi- adding up all four sectors.
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