Introduction
Currently, around 4900 crustacean species have been recognized for their terrestrial conquest, among which crabs from the Brachyura infraorder are included. These crabs are part of the Order Decapoda, one of six crustacean lineages known to have successfully colonized terrestrial ecosystems (Marin and Tiunov, Reference Marin and Tiunov2023). According to Wolfe et al. (Reference Wolfe, Ballou, Luque, Watson-Zink, Ahyong, Barido-Sottani, Chan, Chu, Crandall, Daniels, Felder, Mancke, Martin, Ng, Ortega-Hernández, Theil, Pentcheff, Robles, Thoma, Tsang, Wetzer, Windsor and Bracken-Grissom2022), crabs transitioned from marine to non-marine habitats between 5 and 15 times, while making the reverse journey 3–4 times. This diversification primarily occurred in the Triassic period, with family-level divergences happening in the late Cretaceous and early Paleogene periods. The most derived crabs, commonly referred to as ‘true crabs’ (Eubrachyura), diverged from their ancestral brachyurans during the Cretaceous period (Tsang et al., Reference Tsang, Schubart, Ahyong, Lai, Au, Chan, Ng and Chu2014; Luque et al., Reference Luque, Xing, Briggs, Clark, Duque, Hui, Mai and McKellar2021; Watson-Zink, Reference Watson-Zink2021), and present some of the highest levels of terrestrial adaptations among the six grades proposed by Watson-Zink (Reference Watson-Zink2021), which were possible due to morphological, reproductive (e.g. aerial respiration, moulting, and development) and physiological changes (e.g. osmoregulation, nitrogen excretion, desiccation resistance, and thermoregulation).
Terrestrial and semi-terrestrial crabs comprise approximately 300 species. A high adaptation to a terrestrial lifestyle can be observed in the family Gecarcinidae (Marin and Tiunov, Reference Marin and Tiunov2023), where the species colonize land through marine environments (including intertidal mudflats, sandflats, mangrove forests, etc.) (Watson-Zink, Reference Watson-Zink2021). These crabs have a life history characterized by juvenile and adults occurring in terrestrial habitats, while their larvae undergo a planktotrophic development that spans approximately 15–30 days in the marine environment (five to six zoeal stages and one megalopa) (Colavite et al., Reference Colavite, Tavares, Mendonca and Santana2021). The success of these species depends equally on the capacity of migration between the land-sea gradient in both phases and on their adaptations to survive in both environments (Bliss and Mantel, Reference Bliss and Mantel1968; Burggren and McMahon, Reference Burggren and McMahon1988; Hartnoll, Reference Hartnoll, Castro, Davie, Ng and Richer de Forges2010; Watson-Zink, Reference Watson-Zink2021; Marin and Tiunov, Reference Marin and Tiunov2023). Some gecarcinid species are endemic to oceanic islands, which poses an additional challenge for their migratory behaviour since the residence sites are even further from the sea (Doi et al., Reference Doi, Kato, Itoh, Mizutani and Kohno2019; João et al., Reference João, Kriegler, Freire and Pinheiro2021), and sometimes reach more than 1000 metres of altitude (e.g. Gecarcinus ruricola in Caribbean Islands - Hartnoll et al., Reference Hartnoll, Baine, Grandas, James and Atkin2006). Indeed, studying insular gecarcinid species can be challenging due to their isolated habitats; however, there is existing well-documented research focused on understanding the biology and behaviours of crabs within this family (Bliss et al., Reference Bliss, Van Montfrans, Van Montfrans and Boyer1978; Hicks, Reference Hicks1985; Foale, Reference Foale1999; Adamczewska and Morris, Reference Adamczewska and Morris2001; Green, Reference Green2004; Hartnoll et al., Reference Hartnoll, Baine, Grandas, James and Atkin2006, Reference Hartnoll, Baine, Britton, Grandas, James, Velasco and Richmond2007, Reference Hartnoll, Broderick, Godley and Saunders2009, Reference Hartnoll, Weber, Weber and Liu2017; Liu and Jeng, Reference Liu and Jeng2007; López-Victoria and Werding, Reference López-Victoria and Werding2008; Turner et al., Reference Turner, Hallas and Morris2011; Perger, Reference Perger2014; Sanvicente-Añorve et al., Reference Sanvicente-Añorve, Lemus-Santana and Solís-Weiss2016; Tavares and Mendonça, Reference Tavares and Mendonça2022; João et al., Reference João, Duarte, Kriegler, Freire and Pinheiro2023a). However, there is a knowledge gap concerning how these species transition from the larval phase to land. The process of recruitment in these species has received limited attention, with only a few documented events and scarce information available (Hartnoll and Clark, Reference Hartnoll and Clark2006; Hartnoll et al., Reference Hartnoll, Régnier-McKellar, Weber and Weber2014).
There are two well-documented recruitment processes for insular gecarcinids in the literature, the Christmas Island red crab Gecarcoidea natalis (Hicks, Reference Hicks1985; Hicks et al., Reference Hicks, Rumpff and Yorkston1990) and the Caribbean black crab Gecarcinus ruricola (Hartnoll and Clark, Reference Hartnoll and Clark2006). In both cases, a notable similarity is the mass return of megalopae, which creates a visually striking phenomenon where the tideline is painted with a red colour. This mass return event greatly facilitates the understanding of the overall recruitment process in both species. Furthermore, it appears that the behaviours of egg release and subsequent return of recruits in gecarcinid crabs are connected to the phases of the full or new moon (Hicks, Reference Hicks1985; Liu and Jeng, Reference Liu and Jeng2005, Reference Liu and Jeng2007; Hartnoll and Clark, Reference Hartnoll and Clark2006). Among all other gecarcinid species where there is some recorded information about recruitment in the literature, the only common characteristic is the presence of megalopae on land (Johngarthia lagostoma (H. Milne Edwards 1837) and J. weileri – Hartnoll et al., Reference Hartnoll, Régnier-McKellar, Weber and Weber2014; J. planata – Erhardt and Niassaut, Reference Erhardt and Niassaut1970; Gecarcoidea lalandii, erroneously named as G. natalis in the study – Webb, Reference Webb1922; and Tuerkayana celeste – Hicks et al., Reference Hicks, Rumpff and Yorkston1990). Although these works provide only basic records, they do suggest that gecarcinid megalopae could live on land, even venturing more than 100 metres away from the shoreline. Unfortunately, the recruitment events can be infrequent and sporadic, as observed for Gecarcinus ruricola presenting an interval between each recruitment every 5 or 6 years (Hartnoll and Clark, Reference Hartnoll and Clark2006), which makes documenting and studying these events difficult.
Population studies on insular gecarcinids have highlighted the absence of records on first crab instars and juvenile individuals. As a result, these studies have indicated a concerning pattern of population aging (Hartnoll et al., Reference Hartnoll, Broderick, Godley and Saunders2009; Turner et al., Reference Turner, Hallas and Morris2011); however, this could partially be attributed to methodological limitations. The habitat preferences and distribution of juvenile crabs remain unclear, which can lead to sampling biases that primarily capture adult individuals (Turner et al., Reference Turner, Hallas and Morris2011). In addition, there is evidence that juveniles of certain crab species occupy specific habitats such as crevices and areas under rocks (as Tuerkayana hirtipes – Hicks et al., Reference Hicks, Rumpff and Yorkston1990) or could be associated with adult burrows (as described for T. hirtipes – Hicks et al., Reference Hicks, Rumpff and Yorkston1990; and for Cardisoma carnifex – Vannini et al., Reference Vannini, Berti, Cannicci and Innocenti2003). Cleary, associating with adult burrows can be considered an adaptive strategy because burrows remain for at least five years in some cases (Green, Reference Green2004), providing a humid and thermally stable habitat (Greenaway, Reference Greenaway1989; Berti et al., Reference Berti, Cannicci, Fabbroni and Innocenti2008), with chambers where leaves are stored by the owner crab (O'Dowd and Lake, Reference O'Dowd and Lake1989; Vannini et al., Reference Vannini, Berti, Cannicci and Innocenti2003).
Johngarthia lagostoma, commonly known as the yellow land crab, is an endemic species of insular land crab found in four islands around the world, in the South Atlantic Ocean (Rocas Atoll, Fernando de Noronha, Ascension Island, and Trindade Island, according to Melo, Reference Melo1996). Few studies were conducted about their biology, mostly on Ascension and Trindade islands (Ascension: Hartnoll et al., Reference Hartnoll, Broderick, Godley and Saunders2009, Reference Hartnoll, Broderick, Musick, Pearson, Stroud and Saunders2010; Trindade: João et al., Reference João, Kriegler, Freire and Pinheiro2021, Reference João, Duarte, Bispo da Silva, Freire and Pinheiro2022, Reference João, Duarte, Kriegler, Freire and Pinheiro2023a, Reference João, Duarte, Freire and Pinheiro2023b; Tavares and Mendonça, Reference Tavares and Mendonça2022; Entringer and Srbek-Araujo, Reference Entringer and Srbek-Araujo2023), where J. lagostoma population structure was considered skewed for adult individuals (Hartnoll et al., Reference Hartnoll, Broderick, Godley and Saunders2009; João et al., Reference João, Duarte, Kriegler, Freire and Pinheiro2023a). In addition, the lack of clear information about the recruitment of J. lagostoma is of particular concern for Brazilian islands (Rocas Atoll, Fernando de Noronha, and Trindade Island) where this species is categorized as Endangered – EN (Santana and Coelho, Reference Santana and Coelho2018; MMA, Reference MMA - Ministério do Meio Ambiente2022), following the IUCN criteria (IUCN, 2012). A pressing concern that requires immediate investigation is the recruitment of J. lagostoma to each island, as this information is crucial for assessing the species' demographics and informing conservation strategies (Pinheiro et al., Reference Pinheiro, Santana, Rodrigues, Ivo, Santos, Torres, Boos, Dias-Neto, Pinheiro and Boos2016). The only note about the species recruitment in Trindade Island was made in 1987, where initial crab stages were observed in galleries constructed by adults (Tavares and Mendonça, Reference Tavares and Mendonça2022). So, in this study, we evaluate the association between the first instars of J. lagostoma and adult crab burrows in Trindade Island (Brazil) to co-inhabiting behaviour, analysing recruits' relative growth, population density, and size in function of the lunar phases (full, waning, new, and waxing moons).
Materials and methods
Study area and recruits sampling
All the samples were carried out on Trindade Island (20° 29″ S- 29° 20.7″ W), a volcanic island located in the South Atlantic, approximately 1200 km off the Brazilian coast (Figure 1A, B). A portion of Trindade Island has been designated as a large marine protected area since 2018 (ICMBio, 2018). The island is permanently inhabited by the Brazilian Navy, with a human population of around 40 people, including military and researchers. The sampling took place on the eastern face of Trindade Island, specifically at Andradas Beach (Figure 1C), which is known to be an important reproductive site for J. lagostoma (João et al., Reference João, Duarte, Kriegler, Freire and Pinheiro2023a). To evaluate the co-habitation of recruits on galleries of adult conspecific, we conduct samples in January 2020, during the reproductive season of J. lagostoma, which typically occurs between December and May for Rocas Atoll and Ascension Island (Teixeira, Reference Teixeira1996; Hartnoll et al., Reference Hartnoll, Broderick, Musick, Pearson, Stroud and Saunders2010), and between October to April for Trindade Island (Tavares and Mendonça, Reference Tavares and Mendonça2022; João et al., Reference João, Duarte, Kriegler, Freire and Pinheiro2023a).
Geographic location of Trindade Island (Brazil). Where: (A) Southeast Brazilian coast showing the position of the Trindade Island; (B) general view of the Trindade Island indicating the study area location (gray circle); (C) general view of Trindade Island; (D) general view of the study area (Andradas Beach); (E) frontal view of a Johngarthia lagostoma adult in the Andradas Beach; and (F) dorsal view of a J. lagostoma recruit (scale: 1 cm).
At Andradas Beach (Figure 1D), J. lagostoma is the exclusive species known to construct galleries in the supralittoral zone, primarily associated with sand hill vegetation. These burrows are called ‘transit burrows’ by Hartnoll et al. (Reference Hartnoll, Broderick, Musick, Pearson, Stroud and Saunders2010) due to be constructed during migration or larval release but subsequently abandoned. For each lunar phase (full, waning, new, and waxing), we systematically examined a minimum of 25 random and visibly active burrows, characterized by the absence of debris accumulation and the presence of other biogenic signals (e.g. tracks and faeces) close to the opening. During the day period, when crabs typically remain within their burrows, each gallery was carefully and manually excavated until reaching its end or until to attain an adult of J. lagostoma (Figure 1E). In this process, all excavated sediment was collected and placed in a plastic tray and then sieved. All adult crabs collected during the excavation were identified based on their respective gallery numbers, sexed, and reserved in plastic boxes to be released back onto the beach at the end of these procedures. The sex was verified by inspection of abdominal dimorphism (males, subtriangular; and females, semi-rounded) and the number of pleopod pairs (males, two uniramous pairs; and females, four biramous pairs). Following the sieving of the sediment, the recruits (Figure 1F) of each burrow were carefully placed in labelled individual plastic tubes with their corresponding gallery number. These tubes were transported to the laboratory, where the recruits were crioanesthetized and subsequently preserved in 70% alcohol. Finally, after excavation, the sediment surrounding the burrows collapsed, mitigating the risk of sampling the same burrow other times. Moreover, during each lunar phase, samples were taken from different locations within the sand dune vegetation to prevent potential bias due to previous sampling.
Recruits: recognition, measurements, and biometric relationships
In the laboratory, all recruits were evaluated to be identified as megalopae or juveniles of J. lagostoma species, using diagnostic characters informed for Gecarcinids by Cuesta et al. (Reference Cuesta, García-Guerrero and Hendrickx2007), respectively. Following, each exemplar was measured using an image analysis system (KS-300®-Zeiss®) integrated to a stereomicroscope (Axiolab®-Zeiss®, 0.01 mm). The carapace width (CW, mm) was determined as the maximum cephalothorax distance between the lateral margins and used as the reference for body size in crabs. Frequency histograms were constructed using 1 mm CW size classes, from which the Fisher asymmetry coefficient (SK, skewness) was calculated according to Sokal and Rohlf (Reference Sokal and Rohlf2012), as recommended by Pinheiro et al. (Reference Pinheiro, Souza, Boos and Duarte2022), and categorizing the size distribution as symmetric (−0.5 ≤ SK ≤ 0.5), positive asymmetric (SK > 0.5) of negative asymmetric (SK<−0.5).
Biometry of juveniles was registered in some morphological structures (also in millimetres), represented by: carapace length (CL, distance between the frontal to posterior margin of carapace); major cheliped propodus length (PL, distance between end of the fixed finger and the tooth at the propodus-carpus joint); and abdominal width (AW, greatest width in the fifth somite). Additionally, the weight of each recruit (WT, in grams) was recorded using a digital analytical scale (Ohaus, 0.0001 g). Individuals with carapace damage or missing appendages were excluded from the biometric analysis. Since sexual dimorphism recognized was not present in the recruits, they were not sexed.
To test the fit between all biometric measures, morphological relationships were examined by using carapace width (CW) as the independent variable and the other measures (CL, PL, AW, and WT) as the dependent variables. Regression analysis was employed to determine the fit, employing the power function (Y = aXb) in each biometric relationship. To accomplish this, all variables were log-transformed to calculate the linear models for allometric growth rates. The slope value (constant ‘b’) was used to determine relative growth to each relationship (CL × CW, PL × CW, and AW × CW), where growth patterns could be categorized as isometric (b = 1), positive allometric (b > 1), or negative allometric (b < 1). The same was conducted with the WT × CW relationship, in this case with b-values characterizing these weight's growth patterns in relation to 3 (Pinheiro and Fiscarelli, Reference Pinheiro and Fiscarelli2009). Student's t-tests were conducted to assess departures from isometry in all relationships (α = 0.05), using b-values of 1 or 3 in each case.
Relationship between juvenile recruits' traits with lunar phases and adult body size
To assess the influence of lunar phases on J. lagostoma recruitment, the density of juvenile recruits (DE, individuals per burrow) and corporal measures (CW and WT) values were used as dependent variables, while the lunar phases (full, waning, new, and waxing) were treated as factors. The normality assumption and homogeneity of variances for all dependent variables were assessed using Shapiro–Wilk (W) and Levene (L) tests, respectively. Since the data did not meet the assumptions of parametric distribution, a Kruskal–Wallis test (Sokal and Rohlf, Reference Sokal and Rohlf2012) was conducted. In cases where statistically significant differences were observed, post-hoc Dunn tests were performed to compare the median values across different lunar phases. All these statistical analyses were performed using R version 4.2.1 (R Core Team, Reference R Core Team2022) with the ‘dunnTest’ function available in the ‘FSA’ package (Ogle et al., Reference Ogle, Doll, Wheeler and Dinno2023).
Evaluation of a possible association between juvenile recruits' density/burrow (DE) and mean juvenile recruits' body size (CWJ), both in relation to adults' body size (CWA), was submitted to regression analysis by linear regression analysis, represented by DE vs CWJ and CWJ vs CWA, respectively. This association was also evaluated by Pearson's linear correlation coefficient (r), considering ‘n-2’ degrees of freedom.
Results
Recruits' occurrence and biometric relationships
A total of 128 burrows were examined, of which 54.7% (n = 70) were empty without any recruits or owners. In 23.4% of the burrows (n = 30), both J. lagostoma owner and recruits were present, while in 21.9% (n = 28) only the recruits were found inhabiting the galleries. Among the burrows with both owners and recruits, 53.3% had ovigerous females (n = 16), 43.3% had males (n = 13), and only 3.3% had non-ovigerous females (n = 1). A total of 113 J. lagostoma recruits were sampled, with a density (DE) ranging from 1 to 10 ind./burrow (mean ± standard deviation: 1.7 ± 0.9 ind./gallery; and variation coefficient: 52.9%), and their carapace width (CW) ranged from 2.9 to 7.5 mm (4.9 ± 0.7 mm; and 14.3%, respectively) (Table 1). The size frequency histogram indicated a symmetric distribution for all sampled recruits (SK = 0.3, Figure 2).
Regression analysis using all biometric relationships of Johngarthia lagostoma recruits from Trindade Island, Brazil
Where: AW, abdominal width; CL, carapace length; CW, carapace width; PL, cheliped propodus length; R 2, coefficient of determination; t, calculated t-value evaluating departure from isometry (b = 1), expressed by *P ≤ 0.05 or nsP > 0.05; and WT, weight.
Abundance of Johngarthia lagostoma recruits in a size-frequency histogram showing a symmetric distribution (SK = 0.28). Where: CW, carapace width; and numbers above the bars, N of each size-class.
Inside the burrows, the presence of both owners and recruits was not random. Even in the absence of an owner, the burrows appeared to have been recently abandoned, as indicated by the absence of debris and the well-structured entrance and tunnels. The owner was consistently found at the deepest part of the gallery, which varied in distance from approximately 20 to 100 cm from the ground surface. Regardless of the presence or absence of the owner, the recruits were never found in this deepest part of the gallery but were commonly associated with small crevices along the sides of the tunnels. These crevices seemed to be used by the owners for storing food, represented by the accumulation of leaves and bioturbated sediment.
All biometric relationships showed statistical significance (P < 0.05), displaying a positive correlation (ρ ≥ 0.85; P < 0.001), and demonstrating good fits (R 2 ≥ 0.70) in the regression analysis (Table 1). The slopes calculated for CL × CW (b = 0.93) and AW × CW (b = 0.93) indicated isometry, meaning there was proportional growth between the dependent variables and CW. On the other hand, the PL × CW relationship exhibited a lower slope (b = 0.77) and confirmed negative allometry, indicating that there was greater growth in CW compared to PL. Lastly, the WT × CW relationship confirmed isometry (b = 3.11), showing that the weight (WT) and CW grew proportionally in the recruited individuals.
Relationship between juvenile recruits' traits with lunar phases and adult body size
Firstly, all dependent variables (DE, CW, and WT) were significantly influenced by the lunar phases (DE: KW = 28.3, P = 0.003; CW: KW = 21.4, P = 0.0001; WT: KW = 22.3, P = 0.0001 – Figure 3). For density of juveniles the highest values were recorded during the full moon phase (DE: 1 to 10 ind./gallery = 2.0 ± 2.5 ind./gallery), which decreased significantly during subsequent moon phases (Figure 3A). In the case of CW and WT values (Figure 3B, C), an opposite pattern was observed, with the lowest values registered during the full moon phase (CW: 3.2 to 5.7 mm, 4.7 ± 0.5 mm; WT: 0.003 to 0.06 g, 0.03 ± 0.01 g), followed by an increase, with the highest values observed during the waxing moon phase (CW: 5.4 to 7.5 mm = 6.4 ± 0.9 mm; WT: 0.06 to 0.1 g = 0.1 ± 0.04 g).
Variation of the density (ind./burrow: A), size (CW, carapace width: B) and weight (WT, wet weight: C) of the Johngarthia lagostoma recruits co-inhabiting burrows with conspecific crabs along the lunar phases. Where: line inside the box, median values; rhombus dot, mean values; box, interquartile range (IQRs); whiskers, lowest and highest values within 1.5×IQRs; circle dot, original data on which a random noise was added to avoid overlap. Distinct letters indicate significant differences in the dependent variables between the lunar phases (P ≤ 0.05).
Overall, recruits increased an average size of 1.4 times between full and waxing moons (=39.4% per month), corresponding to an average increase in weight of 3.23 times (323% per month) for the same period. Furthermore, a higher frequency of occurrence of recruits in the galleries (65.9%) was recorded during the full moon, being reduced by 50.5% after one month (lunar cycle), in relation to the lowest percentage recorded on the waxing moon (15.4%). Finally, only one megalopa was registered during the studied period, found inside the galleries inspected in 7.1% (n = 1) in the full moon.
The linear regression analysis for DE vs CWA relationship was not significant (DE = 0.039 CWA – 0.394; R 2 = 0.028; n = 25) with a positive but not significant association between them (r = 0.168; P > 0.001). The same was verified for CWJ vs CWA relationship, which was not significant for the regression (CWJ = 0.0033 CWA – 4.73; R 2 = 0.002; n = 25) and association among these variables (r = 0.045; P > 0.001).
Discussion
The knowledge of gecarcinid crabs recruitment is generally limited (Vannini et al., Reference Vannini, Berti, Cannicci and Innocenti2003; Hartnoll and Clark, Reference Hartnoll and Clark2006; Hartnoll et al., Reference Hartnoll, Régnier-McKellar, Weber and Weber2014), with few reports available for some species, such as J. lagostoma (von Fimpel, Reference von Fimpel1975; Hartnoll et al., Reference Hartnoll, Régnier-McKellar, Weber and Weber2014). Specifically, research on J. lagostoma recruitment has mainly focused on Ascension Island, where megalopae and first instar crabs (4.2 mm CW) were found over 100 metres from the sea (Hartnoll et al., Reference Hartnoll, Régnier-McKellar, Weber and Weber2014).
In Brazilian islands (Fernando de Noronha, Rocas Atoll, and Trindade), information is limited and sometimes unclear. A report mentions a 7 mm dark brown crab leaving the sea on Trindade Island (von Fimpel, Reference von Fimpel1975), raising doubts since other gecarcinid crab recruitment records have found megalopae on land (see Lafaix, Reference Lafaix1969; Klaassen, Reference Klaassen1975; Hicks, Reference Hicks1985; Hartnoll and Clark, Reference Hartnoll and Clark2006; Hartnoll et al., Reference Hartnoll, Régnier-McKellar, Weber and Weber2014), including the anomuran Birgus latro (Drew et al., Reference Drew, Harzsch, Stensmyr, Erland and Hansson2010). Thus, we support the pattern suggested by previous studies, where gecarcinid megalopae enter land and then metamorphose into the first instar stage (Hartnoll et al., Reference Hartnoll, Régnier-McKellar, Weber and Weber2014).
Chemical cues influence the metamorphosis from megalopa to the first juvenile instar in both aquatic and semi-terrestrial brachyurans (see Christy, Reference Christy1989; Wolcott and de Vries, Reference Wolcott and de Vries1994; Andrews et al., Reference Andrews, Targett and Epifanio2001; Diele and Simith, Reference Diele and Simith2007; Simith et al., Reference Simith, Diele and Abrunhosa2010; Christy, Reference Christy2011). These studies suggest that metamorphosis is faster and more targeted when megalopae encounter conspecific cues in sediment. However, its relevance to gecarcinid crabs, especially as their megalopae transition to land, remains unclear. In terrestrial environments, detecting and interpreting chemical cues presents unique challenges (Krång et al., Reference Krång, Knaden, Steck and Hansson2012; Waldrop et al., Reference Waldrop, Miller and Khatri2016). Although it has been hypothesized that the odour within a species' burrow is more concentrated (Schmidt and Diele, Reference Schmidt and Diele2009), this aspect was not studied for J. lagostoma.
The lack of records on the early instars of land crab species can be attributed to three main factors, as suggested by Vannini et al. (Reference Vannini, Berti, Cannicci and Innocenti2003): (1) irregular recruitment patterns, which complicate the timing of first instar detection; (2) previous sampling efforts focused primarily on adults, potentially overlooking juvenile habitats; and (3) juvenile recruits, although present, often remain concealed within refuges. Our findings suggest that the latter two factors are particularly relevant to the recruitment of J. lagostoma. The co-habitation observed in our study indicates that J. lagostoma recruits occupy the same habitat as adults but with varying levels of concealment. However, no recruits were found in higher elevation environments (e.g. non-flooded supralittoral or mountainous areas), with or without vegetation.
Although our field research predominantly identified conspecific burrows as habitats for recruits, this does not imply they are the exclusive refuges. Due to the scope of our investigation on Trindade Island, other potential habitats such as crevices and spaces beneath rocks in the supralittoral zone were not explored, leaving open the possibility of additional juvenile habitats. Nevertheless, the information from our study, along with previous records for J. lagostoma (Tavares and Mendonça, Reference Tavares and Mendonça2022) and similar findings for C. carnifex and Gecarcinus lateralis (see Vannini et al., Reference Vannini, Berti, Cannicci and Innocenti2003 and Klaassen, Reference Klaassen1975, respectively), offers valuable insights into where recruits might undergo moulting stages before constructing their own burrows.
The transition to terrestrial environments poses significant challenges for crabs, with desiccation being a major concern, especially on oceanic islands near the equator and tropics. Trindade Island is characterized by intense east winds and frequent heavy rains, often escalating into tropical storms that flood its valleys (Pires et al., Reference Pires, Mansur and Bongiolo2013). These rain events, known as ‘Pirajás,’ occur almost daily during the summer, triggered by the humid oceanic air rising over the island's highest peak, ‘Desejado’ (~600 m), resulting in storm clouds that precipitate around the island (SECIRM, 2017). This study was conducted in January, one of the island's driest months, with an average rainfall of 65 mm (SECIRM, 2017). Although Trindade is the only Brazilian oceanic island with perennial watercourses and springs (Marques et al., Reference Marques, Magalhães-Júnior and Oliveira2019), beaches like Calhetas and Andradas have type IV drainage (direct to the ocean or with limited flow). This highlights the importance of ‘Pirajás’ in maintaining sediment and undergrowth moisture during the key reproductive period of this species, a factor that must be considered.
Gecarcinidae crabs dig burrows in sediment to cool off and may inhabit areas influenced by tides or vegetation (Watson-Zink, Reference Watson-Zink2021). Bliss (Reference Bliss and Whittington1963) observed that terrestrial crabs often occupy elevated areas, creating shallow burrows that avoid groundwater and help maintain low internal moisture. Gecarcinid species within the genera Johngarthia, Gecarcinus, and Gecarcoidea possess a ventral tuft of hydrophilic setae that aids in water retention (Bliss, Reference Bliss and Whittington1963, Reference Oliveira2014; Guinot et al., Reference Guinot, Ng and Moreno2018). In J. lagostoma, these setae are located between the 5th pereopod and the margins of the 1st–2nd pleonal somites (Oliveira, Reference Oliveira2014). More terrestrial species, such as Cardisoma guanhumi and J. lagostoma, also utilize arthrodial membranes for water absorption and have adaptations to minimize water loss, including a strong seal of the branchial chambers (Wolcott, Reference Wolcott1984).
After these rainy events, the water can be retained in the interstices of the sediment, particularly at greater depths, as well as in the larger biomass of undergrowth vegetation (e.g. the grass Cyperus atlanticus). Even during the drier summer months, this vegetation can provide a humid, shaded environment as its dried tussocks droop over the sediment, forming so-called ‘vegetation crowns’. These areas frequently harbour adult J. lagostoma, but notably not their juvenile counterparts. This suggests that factors such as moisture levels and potential chemical signals from adults may not be as influential in recruit behaviour as initially hypothesized, given that recruits are not found in association with adults in these ‘vegetation crowns’. Further investigation is necessary to fully understand these dynamics.
Adults of J. lagostoma are more active at night, likely due to lower temperatures and higher humidity (Hartnoll et al., Reference Hartnoll, Baine, Grandas, James and Atkin2006). Daytime activity varies, with individuals seen at dawn and dusk, but rarely during intense sunlight and low humidity, particularly in the absence of ‘Pirajás’. This susceptibility to desiccation likely affects megalopae and juveniles, suggesting a reliance on summer rains. Additionally, their activity may be synchronized with moon phases that generate higher tidal flooding amplitudes, a pattern common among semi-terrestrial crabs. The association of juvenile recruits with adult burrows could be due to chemical attraction to plant material stored within the burrows, a behaviour also noted in other gecarcinid crabs [e.g. C. carnifex and C. guanhumi as reported by Micheli et al. (Reference Micheli, Gherardi and Vannini1991) and Novais et al. (Reference Novais, Carvalho and Couto2021), respectively], as well as in some semi-terrestrial crabs [e.g. Ucides occidentalis and Ucides cordatus as noted by Twilley et al. (Reference Twilley, Pozo, Garcia, Rivera-Monroy, Zambrano and Bodero1997) and Schories et al. (Reference Schories, Bergan, Barletta, Krumme, Mehlig and Rademaker2003), respectively]. The plant material, rich in nitrogen and carbon, undergoes decomposition, which increases nitrogen content through microbial activity (Nordhaus et al., Reference Nordhaus, Salewski and Jennerjahn2017; Tongununui et al., Reference Tongununui, Kuriya, Murata, Sawada, Araki, Nomura, Morioka, Ichie, Ikejima and Adachi2021; Gao and Lee, Reference Gao and Lee2022). The decomposition process is further enhanced by J. lagostoma during ingestion, breaking down complex molecules into more absorbable forms (Johnston et al., Reference Johnston, Johnston and Richardson2005). Microbial volatile organic compounds (M-VOCs – e.g. alcohols, phenols, etc.) are produced during decomposition (Gray et al., Reference Gray, Monson and Fierer2010; Tongununui et al., Reference Tongununui, Kuriya, Murata, Sawada, Araki, Nomura, Morioka, Ichie, Ikejima and Adachi2021), with their composition depending on the vegetable matrix, microorganisms involved, and fermentation conditions (Rajendran et al., Reference Rajendran, Silcock and Bremer2023). The odours emitted during this process can provide information about food quality and potential benefits or dangers to consumers (Price et al., Reference Price, Denno, Eubanks, Finke and Kaplan2011; Davis et al., Reference Davis, Crippen, Hofstetter and Tomberlin2013). Gecarcinid crabs are particularly sensitive to these odours, as evidenced by their frequent capture using traps baited with aromatic or strong-smelling fruits (e.g. lemon, pineapple, banana, jackfruit) (Krång et al., Reference Krång, Knaden, Steck and Hansson2012). Despite this common attraction in adults, no studies have yet confirmed olfactory attraction in juvenile Gecarcinidae species, highlighting an area for future research.
A question that remains unanswered pertains to the mechanisms through which recruits enter the burrows of larger crabs. Possible factors could include the attractiveness of a moist or shaded environment, the release of pheromonal signals by adults, or the availability of pre-processed food within the burrows, among other factors not addressed by us. While these aspects remain speculative, answers to them could significantly contribute to our understanding of the species' ecology.
The symmetric size distribution of recruits suggests the range at which co-inhabiting behaviour begins and ends, likely around 7 mm CW (Figure 2), when recruits either leave the burrow or are detected and consumed by adults. A similar pattern is observed in U. cordatus, where recruits co-inhabit conspecific burrows until reaching a size that risks detection and cannibalism (Vannini et al., Reference Vannini, Berti, Cannicci and Innocenti2003; Schmidt and Diele, Reference Schmidt and Diele2009). Cannibalism is common among gecarcinid species (Erhardt and Niassaut, Reference Erhardt and Niassaut1970; Bliss et al., Reference Bliss, Van Montfrans, Van Montfrans and Boyer1978; Hicks, Reference Hicks1985; Wolcott, Reference Wolcott, Burggreen and McMahon1988). This risk increases when food is scarce or during stressful periods, such as when females await larval release (Wolcott and Wolcott, Reference Wolcott and Wolcott1984, Reference Wolcott and Wolcott1987; Hartnoll et al., Reference Hartnoll, Broderick, Musick, Pearson, Stroud and Saunders2010). Consequently, crabs larger than 7 mm CW likely leave the burrow to find alternative refuges.
Biometric analysis of recruits reveals trends typical of terrestrial crabs but distinct from adult gecarcinids. For the CL × CW relationship, recruits have a more square-shaped carapace, reflecting a transitional morphology. While megalopae generally have a longer carapace (Cuesta and Anger, Reference Cuesta and Anger2005; Hartnoll and Clark, Reference Hartnoll and Clark2006; Cuesta et al., Reference Cuesta, García-Guerrero and Hendrickx2007; Hartnoll et al., Reference Hartnoll, Régnier-McKellar, Weber and Weber2014), adults show a wider carapace due to negative allometry (Hartnoll et al., Reference Hartnoll, Baine, Grandas, James and Atkin2006). This shift likely aids in adapting to terrestrial habitats, where a broader carapace improves gill chamber space for respiration (Bliss and Mantel, Reference Bliss and Mantel1968; Vannini et al., Reference Vannini, Berti, Cannicci and Innocenti2003). In contrast to typical positive allometry seen in juvenile gecarcinids (Hartnoll et al., Reference Hartnoll, Baine, Grandas, James and Atkin2006; Molina-Ortega and Vázquez-López, Reference Molina-Ortega and Vázquez-López2018; Doi et al., Reference Doi, Kato, Itoh, Mizutani and Kohno2019; João et al., Reference João, Duarte, Bispo da Silva, Freire and Pinheiro2022), our study found negative allometry for chelipeds and isometry for the abdomen in recruits. This suggests that growth during this phase prioritizes overall body size rather than specific structures linked to sexual maturity (Hartnoll, Reference Hartnoll and Abele1982). The WT × CW relationship in recruits also displayed isometry, unlike the negative allometry seen in adults (Hartnoll et al., Reference Hartnoll, Baine, Grandas, James and Atkin2006; Molina-Ortega and Vázquez-López, Reference Molina-Ortega and Vázquez-López2018), reinforcing the focus on balanced body growth during recruitment.
Our findings regarding the density of recruits and their body measurements (CW and WT) reveal a distinct pattern associated with lunar phases, at least during our sampling period (January 2020). We observed an inverse relationship, whereby higher recruit densities were observed during the full moon, which subsequently decreased in the following phases. Furthermore, we found that the smallest recruits were sampled during the full moon, while their mean size and weight increased in subsequent moon phases. These observations suggest that there was a peak in recruitment activity during the full moon, followed by growth of the recruits within the owner burrows during the subsequent phases. Worth noting, that only one megalopa was captured in this study during the full moon, confirming the starting point of the recruitment process of this species. The reproductive process of many gecarcinids is known to be influenced by lunar phases, particularly during periods of larger tidal amplitudes, such as the full and new moon (Klaassen, Reference Klaassen1975; Liu and Jeng, Reference Liu and Jeng2005, Reference Liu and Jeng2007). However, the specific timing of recruitment for J. lagostoma remains largely unknown, with only two instances associated with the new moon reported for individuals from Ascension Island (Hartnoll et al., Reference Hartnoll, Broderick, Musick, Pearson, Stroud and Saunders2010). In the case of other gecarcinid species, such as G. lalandii and Epigrapsus notatus, a significant release of larvae by females has been observed during the new moon (Liu and Jeng, Reference Liu and Jeng2007) and full moon (Liu and Jeng, Reference Liu and Jeng2005), respectively.
Recruitment in gecarcinid species is generally sparse, raising concerns for their conservation (Hicks, Reference Hicks1985; Hartnoll and Clark, Reference Hartnoll and Clark2006). Demographic studies of the Gecarcinidae family show low juvenile proportions, ranging from 8.5% for T. hirtipes (Turner et al., Reference Turner, Hallas and Morris2011) to 26% for Gecarcinus ruricola (Hartnoll et al., Reference Hartnoll, Baine, Grandas, James and Atkin2006) and 36.4% for E. notatus (Doi et al., Reference Doi, Kato, Itoh, Mizutani and Kohno2019). Recruitment of individuals under 10 mm CW is rare, typically seen only in species with massive recruitment events (Hicks, Reference Hicks1985; Hartnoll and Clark, Reference Hartnoll and Clark2006). Juvenile J. lagostoma populations vary across islands: 0.7% on Ascension Island, 4.0% at Rocas Atoll (Teixeira, Reference Teixeira1996; Hartnoll et al., Reference Hartnoll, Broderick, Godley and Saunders2009), and 16.4% on Trindade Island (João et al., Reference João, Duarte, Kriegler, Freire and Pinheiro2023a). This percentage for Trindade could increase if individuals from this study are included, showing a relatively better recruitment scenario. Replicating this study's methodology on other islands could confirm co-inhabiting behaviour and reveal changes in population structure, contributing significantly to the management and conservation of J. lagostoma in Brazilian islands.
Our findings offer valuable insights into the recruitment of J. lagostoma, focusing on three key aspects: the behaviour of recruits in conspecific burrows, growth patterns in morphometric traits, and the influence of lunar phases on recruitment. While some findings align with existing literature, others reveal new aspects, such as co-inhabiting behaviour. These insights enhance our understanding of the species’ biology and have important implications for conservation efforts.
Data
The original data of this manuscript are available in https://github.com/marcio-joao/j.lagostoma_recruitment.
Acknowledgements
We thank the Brazilian Navy (First District), Inter-ministerial Secretariat for Marine Resources (SECIRM) and ‘Programa de Pesquisas Científicas da Ilha da Trindade’ (PROTRINDADE), under the commander C. C. Vitória-Régia, who guaranteed our presence in Trindade Island and helped with the project logistic. We thank members of the ‘Projeto Caranguejos de Ilhas Oceânicas’ for help during the field sampling. We thank Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) by the sample permission supported by Sistema de Autorização e Informação da Biodiversidade (SISBIO # 65446). MAAP thanks ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’ (CNPq) for the financial support provided by Universal Project (CNPq # 404224-2016) and for the Research Productivity Fellowship (CNPq # 305957/2019-8 and # 307482/2022-7). IDS thanks ‘Programa Institucional de Bolsas de Iniciação Científica’ (PIBIC) for the scientific-initiation fellowship (#143295/2020-9). MJ thanks ‘Fundação de Amparo à Pesquisa do Estado de São Paulo’ (FAPESP) for the master fellowship (# 2019/16581-9). WS thanks CNPq (PQ2 # 315185/2020-1 e PQ1D 312823/2023-1) and the ‘Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico’ (FUNCAP) for the fellowships (# 6647309/2017 and # PV1-0187-00033.01.00/21).
Authors’ contributions
M.A.A.P. and M.C.A.J. conceived and designed the study. M.C.A.J. and N.K. conducted the field samples. M.A.A.P., I.D.S., and M.C.A.J. analysed the data and made the figures. M.A.A.P., I.D.S., and M.C.A.J. made the first draft of the manuscript. All authors read and approved the final version of the manuscript.
Financial support
This work was supported by ‘Conselho Nacional de Desenvolvimento Científico e Tecnológico’ (CNPq) by Universal Project (CNPq # 404224-2016).
Competing interests
None.
Ethical standards
All permits for sampling were obtained with the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) that was given to the first author the sample permission supported by Sistema de Autorização e Informação da Biodiversidade (SISBIO # 65446).
