Assessment of distribution of two sympatric mud crab species – Panopeus americanus and Panopeus austrobesus – in a Western Atlantic estuarine intertidal zone

Avaliação da distribuição de duas espécies simpátricas de caranguejo-da-lama – Panopeus americanus e Panopeus austrobesus – em uma zona intertidal estuarina do Atlântico Ocidental

Abstract

Sympatric mud crab species Panopeus americanus and Panopeus austrobesus are found in intertidal environments associated with muddy and rocky habitats in the Western Atlantic coast. Therefore, they are a suitable model system to be used in studies focused on investigating biological coexistence aspects between close species, such as population structure and habitat. The aims of the current study are to describe and compare the distribution of two sympatric mud crab species – P. americanus and P. austrobesus – based on their spatial and temporal distribution, in a low human impact estuarine complex area. The hypothesis that these two species show similar distribution, although one species is more abundant than the other, was herein tested. Sampling was carried out in the intertidal zone of a specific area in Cananeia estuarine complex, São Paulo State, Southeastern Brazil, in different periods of time for two years. Both species presented similar pattern distribution and frequency, with predominance in the middle and high intertidal zones, including all demographic categories. However, Panopeus americanus was more abundant and presented smaller mean size in all sampling zones. The pronounced disparity in size between the species suggests divergent dietary preferences, potentially related to prey size allowing the coexistence of these sympatric and syntopic species. The predominance of these two species in the upper intertidal zones was understood as a strategy for avoiding competition with the intertidal alpheid shrimps.

Keywords
Brachyura; coexisting species; microhabitat distribution; Panopeidae

Resumo

As espécies simpátricas de caranguejo-da-lama Panopeus americanus e Panopeus austrobesus são encontradas em ambientes entremarés associados a habitats lamacentos e rochosos, bem como em simpatria na costa do Atlântico Ocidental. Portanto, constituem um sistema modelo adequado para ser utilizado em estudos focados na investigação de aspectos de coexistência biológica entre espécies semelhantes, como estrutura populacional e habitat. Os objetivos do presente estudo são descrever e comparar a microdistribuição de duas espécies simpátricas de caranguejo-da-lama – P. americanus e P. austrobesus – com base na avaliação de sua distribuição espacial e temporal, em uma área estuarina complexa e com baixo impacto antrópico. A hipótese de que estas duas espécies apresentam microdistribuição semelhante, embora uma espécie seja mais abundante que a outra, foi testada. A amostragem foi realizada na zona entremarés de uma área específica do complexo estuarino de Cananeia, Estado de São Paulo, Sudeste do Brasil, em diferentes períodos durante dois anos. Ambas as espécies apresentaram microdistribuição e frequência semelhantes, principalmente nas zonas entremarés média e alta. Entretanto, Panopeus americanus foi mais abundante e apresentou menor tamanho médio em todas as zonas amostrais. A pronunciada disparidade de tamanho entre as espécies sugere preferências alimentares divergentes, potencialmente relacionadas ao tamanho das presas possibilitando a coexistência dessas espécies simpátricas. A predominância dessas duas espécies nas zonas intermareais superiores também indica uma estratégia para evitar a competição com os camarões alfeídeos.

Palavras-chave
Brachyura; espécies coexistentes; distribuição de microhabitat; Panopeidae

Introduction

Species interactions in a given community are of major importance to gather information about the function and dynamics of ecosystems. This knowledge is essential to support decision-making for conservation, biodiversity management and overall health of natural systems (Neylan et al. 2019). Coexistence among congeneric species is a key aspect to help better understanding their influence on communities’ spatial and temporal distribution. Biological processes capable of interfering with this coexistence process are scale-dependent (Hart et al. 2017). Divergence among niches is a factor capable of explaining species interaction at local scale (Kneitel and Chase 2004). Traits, such as selecting different habitats and consuming food deriving from different sources, may avoid competition between species and enable their coexistence (Stearns 1976). Investigating the coexistence of species living in mangroves, as well as their habitats, can be a fruitful environmental assessment aspect given their richness, specificity and diversity (Amaral et al. 2010). Analyzing ecological roles played by crabs and their impact on crab abundance, diversity, distribution and coexistence, at both spatial and temporal scale, as well as assessing mangrove features, can provide information on habitat quality and indicate likely changes in mangroves (Lee et al. 1999, Krausman 1999, Macintosh et al. 2002, Freitas et al. 2021).

Estuarine complex areas encompass mangroves that, in their turn, form habitats typical of coastal wetlands found in intertidal zones along tropical and subtropical latitudes (Tomlinson 1986, Beger et al. 2010). These environments are essential to both aquatic and terrestrial organisms, since they are one of the most productive ecosystems in the world (Goessens et al. 2019, Hamilton 2020). This ecosystem is acknowledged for providing several ecosystem services, such as biodiversity maintenance, nutrient cycling, breeding and nursery habitat, flood control, shoreline stabilization and erosion control, storm protection and pollution control filter (Junk et al. 2014, Barbier 2017).

Information on species richness and interaction are essential to help featuring and assessing this ecosystem, given its high diversity level (Rog et al. 2017). Crabs play essential ecological role in mangroves due to their large number of species and abundance (Nagelkerken et al. 2008, Mokhtari et al. 2015). In addition, they are seen as ecosystem engineers in mangroves because they can affect energy flow, as well as sediment structure and chemistry (Kristensen 2008). Furthermore, crabs form an important link between the basal food web components and the highest trophic levels, consequently, they are capable of affecting different fish and bird species, among other taxa (Macintosh et al. 2002).

Sympatric crab species like Panopeus americanus de Saussure, 1857 and Panopeus austrobesus Williams, 1983 are widely distributed in intertidal enviroments throughout the Western Atlantic (Melo 1996, 2008), including São Paulo State coast (Mantelatto et al. 2020). Oliveira-Rogeri et al. (2023) recently performed an integrative study focused on explaining the taxonomy and distribution range of mud crab species belonging to genus Panopeus in the Southwestern Atlantic zone. Their findings have evidenced six different Panopeus species in the investigated region. According to the aforementioned authors, Panopeus austrobesus presented wide distribution in almost all Brazilian states and in all marine provinces bordering the country. On the other hand, morphologically similar species, such as Panopeus occidentalis, presented a more limited range; its Southern incidence was observed between Southern Pernambuco and Northern Rio de Janeiro states. Consequently, the aforementioned study suggested that previously studies focused on investigating P. occidentalis along the Brazilian Southeastern coast likely analyzed P. austrobesus populations.

The sympatric crab species P. americanus and P. austrobesus are suitable to investigate coexistence between similar species, since they inhabit the same ecosystem although they have different reproduction patterns (Peres et al. 2018 and Vergamini and Mantelatto, 2008a,b, both the references as P. occidentalis). Habitats occupied by P. americanus and P. austrobesus comprise algae and roots, and both species can be found under rocks and gravel, or buried in sand (Melo 1996, 2008).

The aims of the current study were to describe and compare the distribution of the sympatric mudcrab species P. americanus and P. austrobesus, based on assessing their spatial and temporal distribution in an estuarine intertidal zone located in a well-preserved estuarine complex in Western Atlantic coast. We hypothesized that the investigated species show similar distribution in the intertidal zones, although one species is more abundant than the other. Species size and distribution based on demographic categories, juveniles, adults and ovigerous females were also analyzed.

Material and Methods

1.

Study site

Sampling was done in the intertidal zone of the intertidal zone in Cananeia estuarine complex, São Paulo State, Southeastern Brazil (25°04’11.2”S, 48°03’08.9”W); this site is a well-preserved area and is considered one of the most productive estuaries in the world (Diegues 1987, Cunha-Lignon et al. 2011) (Figure 1). The substrate of this site is mainly composed of a mixed sediment of sand and mud, on which randomly distributed gravels and boulders are laid. Although these gravels remain exposed to the air during the low tide, small water puddles provide a moisture refuge to Panopeus americanus and P. austrobesus. The estuarine complex edges hold a dense mangrove forest (Figure 2A-B).

Figure 1
Location of the study area in the intertidal estuarine complex of Cananeia, São Paulo, Southeastern Brazil. Adapted from Pescinelli et al. (2021).

Figure 2
(A-B) view of the sampling area, intertidal zone of the estuary of Cananeia, São Paulo, South-eastern Brazil. (C) dorsal view of a male of Panopeus americanus and (D) Panopeus austrobesus. Photograph by Pescinelli RA.

2.

Sampling and data analysis

Sampling was carried out in an area of approximately 600 m². Collections were performed in June, July, August, October and December 2015, as well as in February 2016, during spring low-tide periods. These dates were selected due to good weather conditions, as well as to the ease of access and the longer low tide time during the collection.

The intertidal area was divided into three sub-areas parallel to the waterline, in the following zones according with the position of the sampling area relative to the waterline at high and low tide: low intertidal zone (the nearest to the waterline), middle intertidal zone (that between the low and high zones) and high intertidal zone (the adjacent to the supralittoral zone and the farthest from the waterline). Three 1-m² sampling units were established in each sub-area; in total, nine sampling units were obtained per month. Sampling units in each sub-area were equidistant from each other, based on the methodology adapted from Vergamini et al. (2008b) and Costa-Souza et al. (2014) (for further details, see Pescinelli et al. 2017).

Two people have manually collected the crabs in a 2-h catch effort per person (one hour before and one hour after the exact lowest tide time in the day). Gravel, boulders sediments were removed from the collection spot in order to enable capturing the specimens. All Panopeus americanus and P. austrobesus individuals found in each sampling unit were collected. Then, crabs were placed in coolers filled with crushed ice. All collected individuals were identified in laboratory, according to Melo (1996) and Oliveira-Rogeri et al. (2023). The sex of each crab was identified based on pleon morphology and on paired males’gonopods. Carapace width (CW) was measured with digital caliper (0.01 mm). Crabs were classified into juveniles and adults, based on morphological sexual maturity values estimated by Carvalho-Batista et al. (2015) and Santos et al. (2017).

Homoscedasticity (Levene) and normality (Shapiro–Wilk) tests were carried out as statistical analysis prerequisites (Zar 1996). Temporal distribution was analyzed based on species’ incidence in the sampled months. Mann-Whitney test (α = 0.05) was used to investigate differences in CW mean (mm) between Panopeus americanus and P. austrobesus, in each intertidal zone. Generalized linear model (GLM) was used to analyze the effect of zones (low, middle and high) on crabs’ mean abundance value. Similarity in spatial distribution (intertidal zones) was analyzed through non-metric multidimensional scaling analysis (NMDS). ANOSIM test was used to compare the separation degree between intertidal zones.

Results

In total, 211 crabs were collected: 133 Panopeus americanus (63%) and 78 P. austrobesus (37%). Although crabs of both species were collected in all monthly-sampling and in the three intertidal zones, P. americanus was the most abundant both in the collection months and in those zones (Figure 3). Abundance data did not present normal distribution (Shapiro-Wilk, P < 0.05). However, both species showed similar spatial distribution and frequency (%) rates: presence in all intertidal zones with gradual increase of abundance towards the intertidal high zone (Table 1, Figure 4A). Moreover, ovigerous females were only collected in the middle and high intertidal zones (Figure 4A).

Figure 3
Temporal distribution of Panopeus americanus and Panopeus austrobesus during the sampling period in the estuarine complex of Cananeia, São Paulo, Southeastern Brazil.

Table 1
Abundance, carapace width (CW) (mm) and frequency (%) of Panopeus americanus and Panopeus austrobesus according to sampling zones in the estuarine complex of Cananeia, São Paulo, Southeast Brazil.

Zones	Panopeus americanus				Panopeus austrobesus
	N	Min–Max	Mean ± SD	%	N	Min–Max	Mean ± SD	%
Low intertidal	28	5.91–18.95	12.94 ± 2.92	21.3	13	5.83–43.67	20.76 ± 11.81	16.6
Middle intertidal	43	7.11–26-44	13.80 ± 4.13	32.4	29	7.84–45.85	21.96 ± 9.71	37.2
High intertidal	62	6.42–26.75	14.33 ± 4.44	46.3	36	5.38–45.71	24.41 ± 11.69	46.2
Total	133	5.91–26.75	13.80 ± 4.07	100	78	5.38–45.85	22.89 ± 10.97	100

Figure 4
(A) Spatial distribution of juveniles, males, non-ovigerous females and ovigerous females of Panopeus americanus and Panopeus austrobesus in the intertidal zones in the estuarine complex of Cananeia, São Paulo, Southeastern Brazil. (B) Minimum, maximum (whiskers), median (horizontal lines) and mean (x) of the CW of both species are also plotted.

There was a significant difference in the mean CW between P. americanus and P. austrobesus (Mann-Whitney test P < 0.05). Despite its higher abundance, P. americanus presented smaller mean CW in all sampled zones (Figure 4B).

The generalized linear model (GLM) revealed a significant association between the mean abundance and spatial distribution of both species. The significant association was observed between the zones (GLM P < 0.05). As there was no difference in the spatial distribution between the species (GLM P > 0.05) (Figure 5A), Non-Metric Dimensional Scaling (NMDS) with the Bray-Curtis index was performed for the grouped species. It revealed a significant difference between the zones low vs. middle zones, and between low vs. high intertidal zones (ANOSIM P < 0.05). The NMDS showed no significant difference between the zones middle vs. high intertidal zones (ANOSIM P > 0.05), revealing a higher similarity of these zones with overlapping clusters (Figure 5B).

Figure 5
(A) Generalized linear models (GLM) showing the relationship between the mean abundance of Panopeus americanus and Panopeus austrobesus in the spatial (zones) scale. (B) Non-metric multidimensional scaling (NMDS) showing the distribution of grouped species in the intertidal zones.

Discussion

The current study has comprehensively assessed the distribution patterns of two sympatric mud crab species – Panopeus americanus and P. austrobesus – in a Western Atlantic estuarine intertidal zone. The present findings substantiated the initial hypothesis and confirmed that both species share the same distribution and coexist within identical intertidal zones (middle and high levels). However, P. americanus was more abundant than P. austrobesus in all sampled zones. Despite this discrepancy in abundance, the distribution and frequency of both species remained similar in all investigated zones – the highest abundance was observed in the middle and high intertidal zones.

Different demographic categories (juveniles, as well as adult male and female individuals) have also evidenced the preference of both species for middle and high intertidal zones. Assumingly, competition in ecological contexts is higher when species have niche overlapping, i.e., use similar resources in space and time (Rosenfeld 2002). This competition type can lead to likely exclusion of one species from the community. Results in the current study have evidenced that not only both species are present in the intertidal ecosystem, but that they have also same distribution pattern in the intertidal zone (high abundance in middle and high zones). This pattern was also observed for P. americanus by Vergamini and Mantelatto (2008b) who analyzed a crab population in the remnant mangrove of Araçá, near São Sebastião Channel, on the Northern coast of São Paulo State, Brazil. Interestingly, although both investigated areas (Araçá and Cananeia), are located along the same São Paulo State coast, they are approximately 400 km away from each other and, present different geomorphological features. However, their mud-crab populations present the same genetic and taxonomic aspects (Oliveira-Rogeri et al. 2023), as well as show similar distribution pattern.

The temporal distribution also showed the same pattern for both species. Despite the higher abundance of P. americanus specimens during all sampling period, P. austrobesus increased in abundance in December and February. These results may be correlated to different reproductive periods, especially during December, when P. austrobesus’ abundance surpassed that of P. americanus. According to Peres et al. (2018), P. americanus presents continuous reproduction, whereas P. austrobesus (assessed as P. occidentalis) presents seasonal reproduction between September and March – our results corroborate these authors’ observation. Considering both species have similar spatial distribution, the following question arises: How can one explain their interspecific coexistence? The explanation for this factor may lie on poorly-explored niche features that go beyond temporal and spatial distribution aspects. Niche specializations can happen in the least obvious ways, such as varying activity patterns (Albrecht and Gotelli 2001). Although the diet of other panopeid crabs includes barnacles, oysters, mollusks and other crabs (Guida 1976, Brown and Haight 1992, Milke and Kennedy 2001), unfortunately, no data are available about the natural diet of P. americanus nor P. austrobesus. Certainly, the pattern of spatial distribution observed in the present study may be associated with different diet and/or food of different sizes, as their body size is quite different.

The pronounced disparity in size of the two species suggests divergent dietary preferences, potentially related to prey size, in this syntopic setting. It is conceivable that P. americanus predominantly preys upon smaller organisms, whereas P. austrobesus, prey larger items. While direct dietary analysis was not conducted in this study, the observed size variation is indicative of potential dietary specialization based on prey dimensions. The substantial difference in average size between the two species, and consequent consumption of prey of differing sizes, likely contributes significantly to their coexistence within the middle and high intertidal zones. A study on the diet of both species, as well as a morphological analysis on the mouth morphology and size of structures related to feeding habit, could confirm the difference in feeding between the species studied here.

Another aspect to be evaluated would be different reproductive traits. Peres et al. (2018) reported that sympatric congeneric species can adopt life history strategies to avoid competition and to enable coexistence, such as females from the same area that do not share same reproductive features. According to results by Peres et al. (2018), P. americanus has shown higher fecundity and reproductive output, as well as smaller embryo size, than P. austrobesus. Certainly, these contrasting characteristics allow these two populations from Cananeia estuarine complex to share the same habitat.

Based on the current findings, the different demographic categories followed the same spatial distribution of the species. The coexistence of ovigerous females of both species corroborates the results observed by Peres et al. (2018), according to whom, different reproductive traits may be mainly accountable for avoiding juvenile competition.

The spatial distribution pattern observed in the present study may be also correlated to availability of cracks and refuges amongst boulders and gravels, as well as to the presence of other decapods in the intertidal zone, as shown by Generalized linear models (GLM) and Non-metric multidimensional scaling (NMDS). In the study site, rocks are exposed to the air during low tide periods (See Figure 2A-B), but certainly small water puddles around them provide refuge an immediate water to Panopeus americanus and P. austrobesus.

Mud crabs are not the only organisms using these habitats throughout the intertidal zone. Alpheus snapping shrimps were observed in high abundance during collection procedures in the present study (data not shown), mainly in the low intertidal zone. Previous studies focused on alpheid shrimps in this same area have shown that many of them inhabit the same intertidal zone, but in highest abundance in the low intertidal zone (Pescinelli, pers. obs.). Thus, Panopeus predominance in the middle and high intertidal zones may be a strategy to avoid competition for space with alpheid shrimps. Alpheus brasileiro (Pescinelli et al. 2017, 2018) and Alpheus carlae (Ghizelli-Fraga et al. 2021) were the most abundant snapping shrimp species found in the study site, whereas Alpheus buckupi, Alpheus petronioi and Alpheus estuariensis, the least abundant (Almeida et al. 2018). Pescinelli et al. (2017) conducted a study on social monogamy of A. brasileiro in this same area and observed male and female individuals living together in the same space, besides their high territorialism and territorial defense (Mathews 2002). This behavior and the strong weaponry of these shrimps are factors likely influencing Panopeus species’ distribution in the intertidal zone. In addition, species of the genus Panopeus, as P. americanus studied by Carvalho-Batista et al. (2015) show evidences of cryptic/non-cryptic color pattern in males and females and relationships to morphological and functional sexual maturity, which is another variable in the life strategy in this complex intertidal system.

Considering that studied populations of P. americanus and P. austrobesus coming from Cananeia mangrove and from São Sebastião Channel show the same pattern of spatial distribution in the intertidal zone, certainly, biological factors such as competition, reproductive trait and social organization are stronger that physical features in determining such pattern. Cananeia mangrove is one of the five least degraded and most productive estuaries worldwide (Schaeffer-Novelli et al. 1990), and it is supposed that it provides abundant food resources and diverse habitat refuges. In contrast, São Sebastião Channel is in frequent influence of water pollution and urban development.

On top of that, the availability of refuges can also be a decisive factor in the investigated intertidal zone. Rocks distributed throughout the intertidal zone, as well as their use as refuge by crabs and snapping shrimp species, creates a scenario featured by high competition for space, which is essential to enable species survival. This refuge not only provides protection from desiccation, but also from nekton predators during the high tide, as well as from birds and other predators during the low tide.

The hypothesis of species coexistence within intertidal zones, although with different abundance was confirmed. Furthermore, differences in the crabs’ mean size were observed. Despite the similarity in space occupied by each species, the current findings have suggested that different activity patterns, such as divergent dietary preferences, allow the same distribution of crabs. Due to the great importance of Cananeia mangrove, data on crab populations living in the intertidal zone are essential to help monitoring this ecosystem. Thus, the current findings on the distribution and abundance of sympatric mud-crab species P. americanus and P. austrobesus can be used as indicators to help detecting and assessing disturbances in this important ecosystem.

Acknowledgments

The authors thank LABCAM co-workers for their help during the fieldwork and São Paulo Research Foundation FAPESP (Post-doctoral scholarship 2020/14484-3 to RAP; Thematic Biota 2010/50188-8, Thematic Biota INTERCRUSTA 2018/13685-5 to FLM and RCC and Regular Research Grant 2024/01176-0 to RAP). We are also grateful to the National Council for Scientific and Technological Development – CNPq (Post-doctoral scholarship 155813/2018-8 to RAP and research scholarships PQ 302253/2019-0 and PQ 304368/2022-9 to FLM and RCC, respectively; and to PPBio – Rede Costeira Marinha 442421/2023-0 to FLM, RCC and RAP). Special thanks are due to Lucas Oliveira-Rogeri for species identification and anonymous reviewers for comments and suggestions.

Data Availability

Supporting data are available at <https://doi.org/10.48331/scielodata.T4SALV>.

References

• ALBRECHT, M. & GOTELLI, N.J. (2001). Spatial and Temporal Niche Partitioning in Grassland Ants. Oecologia, 126, 134–141. https://doi.org/10.1007/s004420000494.
  » https://doi.org/10.1007/s004420000494
• ALMEIDA, A.O., TEROSSI, M., BURANELLI, R.C., CASTILHO, A.L., COSTA, R.C., ZARA, F.J. & MANTELATTO, F.L. (2018). Checklist of decapods (Crustacea) from the coast of São Paulo State (Brazil) supported by integrative molecular and morphological data: II. Infraorder Caridea: Family Alpheidae. Zootaxa, 4450, 331–358. https://doi.org/10.11646/zootaxa.4450.3.2.
  » https://doi.org/10.11646/zootaxa.4450.3.2
• AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica, 10, 219–230. https://doi.org/10.1590/S1676-06032010000100022.
  » https://doi.org/10.1590/S1676-06032010000100022
• BARBIER, E.B. (2017). Marine ecosystem services. Current Biology, 27, 507–510. http://dx.doi.org/10.1016/j.cub.2017.03.020.
  » https://doi.org/10.1016/j.cub.2017.03.020
• BEGER, M., GRANTHAM, H.S., PRESSEY, R.L., WILSON, K.A., PETERSON, E.L., DORFMAN, D., MUMBY, P.J., LOURIVAL, R., BRUMBAUGH, D.R. & POSSINGHAM, H.P. (2010). Conservation planning for connectivity across marine, freshwater, and terrestrial realms. Biological Conservation, 143, 565–575. http://dx.doi.org/10.1016/j.biocon.2009.11.006.
  » https://doi.org/10.1016/j.biocon.2009.11.006
• BROWN, K.M. & HAIGHT, E.S. (1992). The foraging ecology of the Gulf of Mexico stone crab Menippe adina (Williams et Felder). Journal of Experimental Marine Biology and Ecology, 160, 67–80. https://doi.org/10.1016/0022-0981(92)90111-M.
  » https://doi.org/10.1016/0022-0981(92)90111-M
• CARVALHO-BATISTA, A., PESCINELLI, R.A., GARCIA, J.R., GUERRA, P.G.M., PARDO, L.M. & MANTELATTO, F.L. (2015). Crypsis in the mud crab Panopeus americanus Saussure, 1857 (Decapoda; Panopeidae): relationship to sexual maturity. Crustaceana, 88, 963–977. https://doi.org/10.1163/15685403-00003461.
  » https://doi.org/10.1163/15685403-00003461
• COSTA-SOUZA, A.C., ROCHA, S.S., BEZERRA, L.E.A. & ALMEIDA, A.O. (2014). Breeding and heterosexual pairing in the snapping shrimp Alpheus estuariensis (Caridea: Alpheidae) in a tropical bay in northeastern Brazil. Journal of Crustacean Biology, 34, 593–603. https://doi.org/10.1163/1937240X-00002258.
  » https://doi.org/10.1163/1937240X-00002258
• FREITAS JR, F., PESCINELLI, R.A., COSTA, R.C., HILESHEIM, J.C., DIEH, F.L. & BRANCO, J.O. (2021). Brachyuran crab diversity across spatial and temporal scales in a mangrove ecosystem from the western Atlantic. Regional Studies in Marine Science, 43,101703. https://doi.org/10.1016/j.rsma.2021.101703.
  » https://doi.org/10.1016/j.rsma.2021.101703
• GHIZELLI-FRAGA, B., COSTA, R.C. & PESCINELLI, R.A. (2021). Life history traits of the snapping shrimp Alpheus carlae (Decapoda: Alpheidae) from the south-eastern coast of Brazil. Zoological Studies, 60, e62. https://doi.org/10.6620/ZS.2021.60-62.
  » https://doi.org/10.6620/ZS.2021.60-62
• GOESSENS, A., SATYANARAYANA, B., STOCKEN, T.V., ZUNIGA, M.Q., MOHD-LOKMAN, H., SULONG, I. & DAHDOUH-GUEBAS, F. (2014). Is Matang mangrove forest in Malaysia sustainably rejuvenating after more than a century of conservation and harvesting management? Plos One 9, e105069. https://doi.org/10.1371/journal.pone.0105069.
  » https://doi.org/10.1371/journal.pone.0105069
• GUIDA, V.G. (1976). Sponge predation in the oyster reef community as demonstrated with Cliona celata Grant. Journal of Experimental Marine Biology and Ecology, 25, 109–122. https://doi.org/10.1016/0022-0981(76)90012-5.
  » https://doi.org/10.1016/0022-0981(76)90012-5
• HAMILTON, S.E. (2020). Botany of mangroves. Mangroves and Aquaculture, 33, 1–40. https://doi.org/10.1007/978-3-030-22240-6_1.
  » https://doi.org/10.1007/978-3-030-22240-6_1
• HART, S.P., USINOWICZ, J. & LEVINE, J.M. (2017). The spatial scales of species coexistence. Nature Ecology & Evolution, 1, 1066–1073. https://doi.org/10.1038/s41559-017-0230-7.
  » https://doi.org/10.1038/s41559-017-0230-7
• JUNK, W.J., PIEDADE, M.T.F., LOURIVAL, R., WITTMANN, F., KANDUS, P., LACERDA, L.D., BOZELLI, R.L. ESTEVES, F.A., NUNES DA CUNHA, C., MALTCHIK, L., SCHÖNGART, J., SCHAEFFER-NOVELLI, Y. & AGOSTINHO, A.A. (2014). Brazilian Wetlands: Their definition, delineation and classification for research, sustainable management and protection. Aquatic Conservation: Marine and Freshwater Ecosystems, 24: 5–22. https://doi.org/10.1002/aqc.2386.
  » https://doi.org/10.1002/aqc.2386
• KNEITEL, J. & CHASE, J. (2003). Trade-offs in community ecology: Linking spatial scales and species coexistence. Ecology Letters, 7, 69–80. https://doi.org/10.1046/j.14610248.2003.00551.x.
  » https://doi.org/10.1046/j.14610248.2003.00551.x
• KRAUSMAN, P.R. (1999). Some basic principles of habitat use. In: LAUNCHBAUGH, K.L., SANDERS, K.D. and MOSLEY, J.L. (Eds.), Grazing Behaviour of Livestock and Wildlife, Idaho Forest, Wildlife and Range Exp. Sta. Bull., No. 70. University of Idaho, Moscow, ID, pp. 85–90.
• KRISTENSEN, E. (2008). Mangrove crabs as ecosystem engineers; with emphasis on sediment processes. Journal of Sea Research, 59: 30–43. http://dx.doi.org/10.1016/j.seares.2007.05.004.
  » https://doi.org/10.1016/j.seares.2007.05.004
• LEE, S.Y. (1999). Tropical mangrove ecology: Physical and biotic factors influencing ecosystem structure and function. Austral Ecology 24, 355–366. https://doi.org/10.1046/j.1442-9993.1999.00984.x.
  » https://doi.org/10.1046/j.1442-9993.1999.00984.x
• MACINTOSH, D.J. & ASHTON, E.C. 2002. A review of mangrove biodiversity conservation and management. Centre for Tropical Ecosystems Research, 1, 71.
• MANTELATTO, F.L., TAMBURUS, A.F., MAGALHÃES, T., BURANELLI, R.C., TEROSSI, M., NEGRI, M.N., CASTILHO, A.L., COSTA, R.C. & ZARA, F.J. (2020). Checklist of decapod crustaceans from the coast of the São Paulo state (Brazil) supported by integrative molecular and morphological data: III. Infraorder Brachyura Latreille, 1802. Zootaxa, 4872(1), 1–108. https://doi.org/10.11646/ZOOTAXA.4872.1.1.
  » https://doi.org/10.11646/ZOOTAXA.4872.1.1
• MATHEWS, L.M. (2002). Territorial cooperation and social monogamy: factors affecting intersexual behaviours in pair-living snapping shrimp. Animal Behavior, 63, 767–777. https://doi.org/10.1006/anbe.2001.1976.
  » https://doi.org/10.1006/anbe.2001.1976
• MELO, G.A.S. (1996). Manual de Identificação dos Brachyura (Caranguejos e Siris) do Litoral Brasileiro. Plêiade/FAPESP, São Paulo.
• MELO, G.A.S. (2008). The Brachyura (Decapoda) of Ilha Grande bay, Rio de Janeiro, Brazil. Nauplius, 16, 1–22.
• MILKE, L.M. & KENNEDY, V.S. (2001). Mud crabs (Xanthidae) in Chesapeake Bay: claw characteristics and predation on epifaunal bivalves. Invertebrate Biology, 120, 67–77. https://doi.org/10.1111/j.1744-7410.2001.tb00027.x.
  » https://doi.org/10.1111/j.1744-7410.2001.tb00027.x
• NAGELKERKEN, I., BLABER, S.J.M., BOUILLON, S., GREEN, P., HAYWOOD, M., KIRTON, L.G., MEYNECKE, J.O., PAWLIK, J., PENROSE, H.M., SASEKUMAR, A. & SOMERFIELD, P.J. (2008). The habitat function of mangroves for terrestrial and marine fauna: A review. Aquatic Botany, 89, 155–185. https://doi.org/10.1016/j.aquabot.2007.12.007.
  » https://doi.org/10.1016/j.aquabot.2007.12.007
• NEYLAN, I.P., SMITH, C.S., SWANSO, E.D., FEGLEY, S.R. & GITTMAN, R.K. (2019). Interspecific and intraspecific interactions between fiddler crabs Minuca pugnax (mud fiddler) and Leptuca pugilator (sand fiddler) influence species’ burrowing behavior. Journal of Experimental Marine Biology and Ecology, 517, 40–48. https://doi.org/10.1016/j.jembe.2019.05.010.
  » https://doi.org/10.1016/j.jembe.2019.05.010
• OLIVEIRA-ROGERI, L., FRANÇA, N.F.C., PERES, P.A. & MANTELATTO, F.L. (2023). Cleaning the mud: Integrative approach clarifies the taxonomy of mud crabs of the genus Panopeus H. Milne Edwards, 1834 (Decapoda: Brachyura: Panopeidae) along the Southwestern Atlantic. Zoologischer Anzeiger, 307, 96–124. https://doi.org/10.1016/j.jcz.2023.10.001.
  » https://doi.org/10.1016/j.jcz.2023.10.001
• PERES, P.A., TEROSSI, M., IGUCHI, J. & MANTELATTO, F.L. (2018). Can reproductive traits help to explain the coexistence of mud crabs Panopeus (Decapoda: Panopeidae)? A case of two sympatric species inhabiting an impacted mangrove area of Southern Brazil. Invertebrate Reproduction & Development, 62, 154–161. https://doi.org/10.1080/07924259.2018.1465482.
  » https://doi.org/10.1080/07924259.2018.1465482
• PESCINELLI, R.A., ALMEIDA, A.O. & COSTA, R.C. (2018). Population structure, relative growth and morphological sexual maturity of the snapping shrimp Alpheus brasileiro Anker, 2012 (Caridea: Alpheidae) from the south-eastern coast of Brazil. Marine Biology Research, 14, 610–620. https://doi.org/10.1080/17451000.2018.1472383.
  » https://doi.org/10.1080/17451000.2018.1472383
• PESCINELLI, R.A., DAVANSO, T.M. & COSTA, R.C. (2017). Social monogamy and egg production in the snapping shrimp Alpheus brasileiro (Caridea: Alpheidae) from the south-eastern coast of Brazil. Journal of the Marine Biological Association of the United Kingdom UK, 97(7), 1519–1526. https://doi.org/10.1017/S0025315416000904.
  » https://doi.org/10.1017/S0025315416000904
• PESCINELLI, R.A., MANTELATTO, F.L., ALMEIDA, A.O. & COSTA, R.C. (2021). First detailed insights into the life-history traits of the alien shrimp Athanas nitescens (Decapoda: Alpheidae) in the western Atlantic. Marine Ecology, 42, e12655. https://doi.org/10.1111/maec.12655.
  » https://doi.org/10.1111/maec.12655
• ROG, S.M., CLARKE, R.H. & COOK, C.N. (2017). More than marine: revealing the critical importance of mangrove ecosystems for terrestrial vertebrates. Diversity and Distributions, 23, 221–230. https://doi.org/10.1111/ddi.12514.
  » https://doi.org/10.1111/ddi.12514
• ROSENFELD, J.S. (2002). Functional redundancy in ecology and conservation. Oikos 98, 156–162. https://doi.org/10.1034/j.1600-0706.2002.980116.x.
  » https://doi.org/10.1034/j.1600-0706.2002.980116.x
• SCHAEFFER-NOVELLI, Y., MESQUITA, H.S.L. & CINTRÒN-MOLERO, G. (1990). The Cananeia lagoon estuarine system, São Paulo, Brazil. Estuaries, 13, 193–203. https://doi.org/10.2307/1351589. Science, 43: 101703. https://doi.org/10.1016/j.rsma.2021.101703.
  » https://doi.org/10.2307/1351589
• STEARNS, S. (1976). Life-history tactics: a review of the ideas. The Quarterly Review of Biology, 51: 3–47. https://doi.org/10.1086/409052.
  » https://doi.org/10.1086/409052
• TOMLINSON, P.B. (1986). The botany of mangroves. Camb. Univ. Press, 3: 413p. https://doi.org/10.1017/S0266467400002017.
  » https://doi.org/10.1017/S0266467400002017
• VERGAMINI, F.G. & MANTELATTO, F.L. (2008a). Continuous reproduction and recruitment in the narrowback mud crab Panopeus americanus (Brachyura, Panopeidae) in a remnant human-impacted mangrove area. Invertebrate Reproduction & Development, 51, 1–10. https://doi.org/10.1080/07924259.2008.9652251.
  » https://doi.org/10.1080/07924259.2008.9652251
• VERGAMINI, F.G. & MANTELATTO, F.L. (2008b). Microdistribution of juveniles and adults of the mud crab Panopeus americanus (Brachyura, Panopeidae) in a remnant mangrove area in the southwest Atlantic. Journal of Natural History, 42(23-24), 1581–1589. https://doi.org/10.1080/00222930802109157.
  » https://doi.org/10.1080/00222930802109157
• ZAR, J.H. (1996). Biostatistical analysis. Prentice Hall 3, 622p.

Edited by

Associate Editor

Tito Lotufo

Publication Dates

• Publication in this collection
  02 Aug 2024
• Date of issue
  2024

History

• Received
  23 Feb 2024
• Accepted
  28 June 2024