Population Density, Microhabitat Use, and Size Characteristics of Pseudothelphusa Dugesi, a Threatened Species of Freshwater

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Population density, microhabitat use, and size characteristics of Pseudothelphusa dugesi, a threatened species of freshwater crab from Mexico (Brachyura: Pseudothelphusidae)

Article in Invertebrate Biology · June 2020 DOI: 10.1111/ivb.12295

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Population density, microhabitat use, and size characteristics of Pseudothelphusa dugesi, a threatened species of freshwater crab from Mexico (Brachyura: Pseudothelphusidae)

Domínguez Emmanuel Carlos Paniagua1 | Uribe Elsah Arce2 | Diego Alfonso Viveros- Guardado1

1Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Abstract Morelos, Cuernavaca, México The brachyuran crab Pseudothelphusa dugesi, or cangrejito barranqueño, is an en- 2 Laboratorio de Acuicultura, Departamento dangered species endemic to Cuernavaca, Morelos, in central Mexico. Individuals of de Hidrobiología, Centro de Investigaciones Biológicas, Universidad Autónoma del P. dugesi inhabit freshwater springs, which are affected by human actions through Estado de Morelos, Cuernavaca, México wastewater drainage, eutrophication, exploitation, and invasive predators such as

Correspondence rainbow trout (Oncorhynchus mykiss). In this study, we evaluated the population den- Elsah Arce Uribe, Laboratorio de sity, microhabitat use, and size characteristics of P. dugesi. Sampling was conducted Acuicultura, Departamento de Hidrobiología, Centro de Investigaciones in May, July, and December of 2018 and March of 2019, during the dry and rainy Biológicas, Universidad Autónoma del seasons in a natural protected area, the Barranca de Chapultepec. Population den- Estado de Morelos, México. 2 2 Email: [email protected] sity was 0.082 crabs/m , female density was 0.052 crabs/m , and male density was 0.112 crabs/m2; ovigerous females were not observed. Males were more abundant than females; the female: male ratio was 1:2.14. Males and females had similar carapace widths and lengths, left and right chelae lengths, and mass. Individuals of P. dugesi were found mostly under or between rocks and under leaf litter. Individuals were more active at night. An understanding of the biology and population characteristics of P. dugesi will help conservationists to develop protective measures and a conservation strategy for this endangered Mexican freshwater crab species.

KEYWORDS Barranca de Chapultepec, conservation, endemic crab, freshwater, stream

1 | INTRODUCTION it is important to quantify population density, microhabitat use, and size structure of individual crab species. Large decapod crustaceans Freshwater ecosystems around the world are threatened by human are an important component of freshwater ecosystems because activities including pollution, eutrophication, exploitation, and inva- they process organic matter, prey on small invertebrates and fish, sive species (Friberg et al., 2011; Gherardi, Barbaresi, & Salvi, 2000; and are preyed upon by a variety of vertebrates (Lee, 1998; Penha- Smith, 2003). Declines of amphibians (Kupferberg et al., 2012), Lopes et al., 2009; Poon, Chan, & Williams, 2010). fish (Olden, Hogan, & Vander, 2007), and crabs (Dudgeon, 2003; The brachyuran crab Pseudothelphusa dugesi Rathbun 1893 Marijnissen, Michel, Clearly, & McIntyre, 2009) have been reported (cangrejito barranqueño) is endemic to Cuernavaca, Morelos, in worldwide. Native and endemic freshwater crabs are particularly central Mexico (Villalobos, 2005). It inhabits freshwater springs, vulnerable to these threats because of their possible limited distri- some of which have been altered by human impacts, such as water bution (Marijnissen et al., 2009). To fully understand this problem, pollution (drainage of wastewater, solid waste) and non-native

FIGURE 1 Pseudothelphusa dugesi, ventral view. A. Female. B. Male. CL, carapace length; CW, carapace width; CHL, chela length

invasive predators such as rainbow trout, Oncorhynchus mykiss 2.2 | Field sampling and morphometric (Walbaum 1792) (unpublished data). Pseudothelphusa dugesi is measurements ranked as “In danger of extinction” on the Mexican list of endangered species (NOM-059;SEMARNAT, -2010). However, because Five sites along the main stream (Site 1, 18°54′44.784′′N, basic knowledge of the ecological characteristics and population 99°12′34.081′′W; Site 2, 18° 54′45.724″N, 99°12′34.041″W; biology of this species are lacking, it is listed as “Data deficient” Site 3, 18°54′58.518″N, 99°12′30.114″W; Site 4, 18°55′6.892″N, on the IUCN Red List (Cumberlidge, 2008). This missing knowl- 99°12′34.898″W; Site 5, 18°55′9.617″N, 99°12′33.224″W) were edge limits the prediction of human impacts on the species and randomly selected on a map of the park, and at each site we sampled its habitats, so its vulnerability to human impacts cannot be a 5-m2 (5 × 1 m) transect five times over a 24-hr period (at 01:00, assessed. 06:00, 11:00, 15:00, and 19:00 hr). Thus, we made a total of 100 Here we evaluate population density (crabs/m2), microhabitat use, sampling surveys: one transect per site, sampled five times during and size characteristics of P. dugesi in the Barranca de Chapultepec a 24-hr period, in each of 4 months, following methods of Taggart, natural protected area, which is a stream in Cuernavaca, Mexico. O´Clair, Shirley, and Mondragon (2004). The activity of the crabs was However, since P. dugesi also inhabits other springs in Cuernavaca, recorded, with a crab considered to be active if found foraging (walk- Mexico, future studies will be required for these other areas. This ing) (Green, 1997). All rocks, leaves, and crevices were searched for is especially important because other streams are affected by even crabs, and the microhabitat in which the crabs were found was re- greater human impacts than the Barranca de Chapultepec study corded. Crabs density was calculated as crabs/m2 for each month area (personal observations). In this first evaluation, we aimed to and time of day (Somers & Nel, 1998). Crabs were collected by provide ecological information to inform the development of a con- hand and placed in a transparent 5-mm mesh container (25 L) that servation strategy for this endangered Mexican freshwater crab allowed spring water to flow through it. Crabs were weighed on a species. digital plate balance (OHAUS, 0.01 mg accuracy). For morphologi- cal measurements, each crab was photographed from above in ventral view in the same position to avoid errors associated with the 2 | METHODS orientation of the crab. The size of each feature was determined with Image J software to reduce the stress on the crab associated 2.1 | Study area and water conditions with making measurements (De La Torre, Arce, Luna-Figueroa, & Córdoba-Aguilar, 2018). Carapace width (CW) and length (CL), and The urban park Barranca de Chapultepec is a natural protected area right and left chela lengths (CHL; Figure 1) of each crab were meas- located in Cuernavaca, central Mexico (between 18°55′09″ and ured in Image J. The sex of the crabs was determined by the shape of 18°54′30″N, and between 99°12′33″ and 99°12′39″W). The park the abdomen (González-Pisani, Barón, & López, 2017; Figure 1). On has a freshwater spring that originates from a stream 1,466 m above completion of morphometric measurements, all crabs were returned sea level (SEMARNAT, 2014). Sampling was conducted during the to the stream. rainy season (May and July of 2018) and the dry season (December of 2018 and March of 2019) (Martínez-Garza, Osorio-Beristain, Valenzuela-Galván, & Nicolás-Medina, 2011). The mean depth of the 2.3 | Statistical analysis water column, water temperature, oxygen concentration, pH, and total dissolved solids at each collection site were recorded using a Data normality was confirmed using Shapiro–Wilk's test. Water multiparameter meter (HANNA, HI 9829). conditions and water depth from each month and each site were PANIAGUA DOMÍNGUEZ et al. | 3 of 6

TABLE 1 Analysis of variance of the physical and chemical and distribution of juveniles (Martinez, 2001), crabs need protection characteristics of the water among sites from hydrodynamic forces that are too strong (Arce & Alcaraz, 2011),

Mean ± SD df F P and also need shelter to hide from predators (Arce & Alcaraz, 2013; Moksnes, Pihl, & Van Montfrans, 1998; Richards, 1992). For P. dug- DO (ppm) 4.8 ± 1.5 4 0.57 .72 esi, it is likely that the leaf litter and rock crevice microhabitats pro- pH 7.9 ± 1.1 4 1.23 .30 vide this protection. The use of these microhabitats is also seen in T (°C) 16.4 ± 0.2 4 1.62 .16 other species, such as Pachygrapsus crassipes (Randal 1840), in which TDS (ppm) 74.4 ± 9.0 4 0.26 .93 crabs use rocks as shelter to protect themselves from hydrodynamic Z (cm) 27.1 ± 16.8 4 20.81 .00 forces (Lau & Martinez, 2003), and Uca mjoebergi Rathbun 1924, in Abbreviations: DO, dissolved oxygen; T, temperature; TDS, total which crabs seek rocks as refuge to avoid predation (Reaney, 2007). dissolved solids; Z, depth. In the urban park Barranca de Chapultepec, we observed non-native rainbow trout, O. mykiss, which can be a predator of P. dugesi compared using ANOVA. Population density was compared among (unpublished data). Thus, refuges are indispensable for the protec- microhabitats, and among months using ANOVA. Population density tion of P. dugesi. The population structure of various crustaceans among sites did not conform to normality assumptions, so we used is determined by the availability of shelters and habitat complexity a Kruskal–Wallis test. Sex ratio was compared using a chi-squared (Beck, 1995, 1997). However, the amount of time that crabs remain test (χ2). Carapace length and width, mass, and chelae sizes were under refuges such as rocks and rock crevices is traded off against compared between sexes using Student's t-test. Statistical analyses foraging time and the loss of opportunities to search for mates were conducted using Statistics®. (Fürtbauer & Fry, 2018; Simonetti, 1984). In addition, the number of refuges is not always sufficient (Beck, 1997), leading to competition between crabs for access to them (Cioni & Gherardi, 2004; Jensen, 3 | RESULTS McDonald, & Armstrong, 2002). In our research, individuals of P. dugesi were more active at The physical and chemical characteristics of the water remained con- night. Indeed, crabs generally have nocturnal activity patterns stant throughout the sampling cycles (P > .05) and among sites (see (Miranda-Anaya, Barrera-Mera, & Ramírez-Lomelí, 2003; Miranda- Table 1). The water was deeper in one of the sites (49.8 ± 14.6 cm; Anaya, Ramírez-Lomelí, Carmona-Alcocer, & Barrera-Mera, 2003; P < .05); however, mean water depth was constant throughout the Ryer, 1987). Nocturnal animals have more opportunities for cam- monthly sampling (27.1 ± 16.8 cm; P > .05). The microhabitat in which ouflage in the environment (Crawford, 1934; Iribarne, Bortolus, & most individuals of P. dugesi were located was under or between Botto, 1997), and the nocturnal activity of P. dugesi may be a re- rocks and in leaf litter: 82% (0.067 crabs/m2) were found under sponse to predation pressure, since potential predators like birds rocks or in crevices along the stream wall and 18% (0.015 crabs/ are highly visually dependent and less active at night (Boujard & m2) were found walking on the substrate. Individuals of P. dugesi of Leatherland, 1992; Hall & Ross, 2007). Rainbow trout, a non-native both sexes were more active at night (Figure 2). Population density predator of P. dugesi, have been observed to be more active at night was similar among all surveys (ANOVA test, F = 3.84; P > .05) and (Brandford & Higgins, 2001; Cooke, Chandroo, Beddow, Moccia, & sites (Kruskal–Wallis test, H = 6.97; P > .05). Population density was McKinley, 2000), and given the coincidence in nocturnal activity, P. 0.082 crabs/m2. Female density was 0.052 crabs/m2, male density dugesi could be severely affected. As rainbow trout might be a threat was 0.112 crabs/m2, and no ovigerous females were observed. Males to P. dugesi, we concludemore studies are necessary to elucidate the were more abundant than females, and the sex ratio was 1:2.14 ecological consequences of this introduced predator. (χ2 test = 32.94; P < .05). Males and females had similar carapace Population density was similarly small at all sampling times and in 2 width (♂ 24.4 ± 7.8 mm; ♀ 23.4 ± 7.2 mm; Student's t-test, t = 1.59, all sites (0.082 crabs/m ). This density does not guarantee a self-sus- P > .05; Figure 3), carapace length (♂ 15.4 ± 4.9 mm; ♀ 14.5 ± 4.6 mm; taining population, and following the IUCN Red List Categories and Student's t-test, t = 1.46, P > .05), mass (♂ 5.14 ± 3.4 g; ♀ 5.06 ± 2.9 g; Criteria document (IUCN, 2012), the population size of P. dugesi is Student's t-test, t = 0.17, P > .05), and left and right chelae lengths consistent with critically endangered species status. The small area (♂18.1 ± 4.7 mm; ♀18.0 ± 5.2 mm; Student's t-test, t = 1.63, P > .05). of occupancy and limited and fragmented distribution (Cuernavaca, Most of the individuals found ranged 11–40 mm in size (carapace central Mexico) puts P. dugesi at risk for extinction (IUCN, 2012). width; Figure 3). Additionally, this crab is an endemic species and we did not observe a clear reproductive period, which makes it still more vulnerable. Males frequently compete with other males to copulate with 4 | DISCUSSION females (Goshima & Murai, 1988). This is often associated with a male-biased sex ratio in crabs, such as in the crab Potamonautes perla-

The microhabitat in which individuals of P. dugesi are found is mostly tus (H. Milne Edwards 1837) (Somers & Nel, 1998), or in the mangrove under or between rocks and leaf litter. While the movement of the crab Aratus pisonii (H. Milne Edwards 1837) (Díaz & Conde, 1989). water provides services to the crabs, such as the transport of nutrients In our study, the female–male ratio was approximately one female 4 of 6 | PANIAGUA DOMÍNGUEZ et al.

FIGURE 2 Density of active individuals of Pseudothelphusa dugesi. Crabs were considered active if found foraging. A. Females. B. Males. Night and day hours are shown

FIGURE 3 Size frequency (carapace width) of females (A) and males (B) of Pseudothelphusa dugesi

for every two males; however, the lack of ovigerous females in our & Pinheiro, 2019; Sanvicente-Añorve, Lemus-Santana, & Solís- sample suggests that females do not live in the streams when bear- Weiss, 2016). There could be advantages to variation in male chela ing eggs. Ovigerous females may congregate in particular locations size; however, further studies should explore relationships between to incubate their eggs, as occurs in Cancer pagurus (Linnaeus 1758) chela size and male–male competition, foraging, and female prefer- (Howard, 1982). In the case of P. dugesi, this is likely out of water. In ence in P. dugesi. other species, such as Pseudothelphusa garmani Rathbun 1898 and We would expect the population of P. dugesi living in a protected

Pseudothelphusa chacei Crane 1949, ovigerous females are found natural area to increase if relevant action measures are taken for walking along the damp forest floor, out of the water (Crane, 1949). their protection. This is the first study to investigate populations of

Ovigerous females of Pseudothelphusa belliana Rathbun 1898 P. dugesi; our study highlights the vulnerability of this endemic crab also leave the water (García-Madrigal & Bastida-Zavala, 1998). species due to its limited distribution, small population, and habitat

Pseudothelphusa garmani garmani (Rathbun 1898) is adapted for aerial fragmentation. We suggest that further studies explore abundance, gas exchange, and adults may be encountered far from water (Innes, habitat, size structure, and other factors, such as reproductive rate, Haj, & Gobin, 1986). Further studies into the reproductive behav- growth, and ecological function of the crab. Our study indicates that ior of P. dugesi are needed to determine basic information, such as P. dugesi could be at risk of extinction if an adequate conservation where they incubate. strategy is not put in place. This strategy should include manage- In some crab species, large males have advantages over smaller ment of the springs were P. dugesi is found and constant monitoring males in accessing females (Jivoff, 1997; Jivoff & Hines, 1998). In to better characterize the status of the population in all their habi- our study, males and females had similar carapace width and length tats. More studies are also needed to understand the biology of this and body mass. Chela size increases proportionally with body size, species. These steps must be carried out before P. dugesi populations such that larger males have larger chelae than smaller males. This decline to levels from which they cannot recover. may provide them an advantage in aggressive interactions for females, especially if the abundance of males is high (Abelló, Pertierra, ACKNOWLEDGMENTS & Reid, 1990; Jivoff, 1997). Studies of chela size have focused on the The authors all declare that they have no conflict of interests. All ap- use of chelae in foraging and in male–male competition (Elner, 1980; plicable international, national, and/or institutional guidelines for the Paul & Paul, 1996; Sneddon, Huntingford, & Taylor, 1997). However, care and use of animals were followed. The authors thank Cristina males and females had similar left and right chela lengths in our Martínez-Garza and José Figueroa for their helpful comments. They study. Crabs with larger chelae can feed on a wider range of prey thank Marco Franco, Yuritzi Castillo, Moises Mejia-Mejia, Olivia De and have fitness advantages through increased success in mating los Santos, Osmara Oliván, Viridiana Pérez, Verónica Jacobo, and competition and intraspecific agonistic interactions (Rio, Hernáez, Betsabe Salas for technical assistance. They also thank Lynna Kyere PANIAGUA DOMÍNGUEZ et al. | 5 of 6 for editing the English text and Jorge Andere González for editing Dudgeon, D. (2003). The contribution of scientific information to the conservation and management of freshwater biodiversity the figures. in tropical Asia. Aquatic Biodiversity, 500, 295–314. https://doi. org/10.1007/978-94-007-1084-9_21 ORCID Elner, R. W. (1980). The influence of temperature, sex and chela size Domínguez Emmanuel Carlos Paniagua https://orcid. in the foraging strategy of the shore crab, Carcinus maenas (L.). org/0000-0003-4212-3271 Marine & Freshwater Behaviour & Physiology, 7, 15–24. https://doi. org/10.1080/10236248009386968 Uribe Elsah Arce https://orcid.org/0000-0002-9815-2525 Friberg, N., Bonada, N., Bradley, D. C., Dunbar, M. J., Edwards, F. K., Diego Alfonso Viveros-Guardado https://orcid. Grey, J., … Woodward, G. (2011). Biomonitoring of human impacts org/0000-0002-3704-4766 in freshwater ecosystems: The good, the bad and the ugly. Advances in Ecological Research, 44, 1–68. https://doi.org/10.1016/B978-0-12- 374794-5.00001-8 REFERENCES Fürtbauer, I., & Fry, A. (2018). Social conformity in solitary crabs, Carcinus Abelló, P., Pertierra, J. P., & Reid, D. G. (1990). Sexual size dimorphism, maenas, is driven by individual differences in behavioural plasticity. relative growth and handedness in Liocarcinus depurator and Animal Behaviour, 135, 131–137. https://doi.org/10.1016/j.anbeh Macropipus tuberculatus (Brachyura: Portunidae). Scientia Marina, av.2017.11.010 54(2), 195–202. https://www.icm.csic.es/scimar/index.php/ García-Madrigal, M. S., & Bastida-Zavala, J. R. (1998). Variaciones morfo- secId/6/IdArt/2464/ metricas de Pseudothelphusa belliana (Decapoda: Pseudothelphusidae) Arce, E., & Alcaraz, G. (2011). Shell use by the hermit crab Calcinus cali- en Michoacán, México. Revista De Biología Tropical, 46(4), 921–927. forniensisat different levels of the intertidal zone. Scientia Marina, 75, Gherardi, F., Barbaresi, S., & Salvi, G. (2000). Spatial and temporal pat- 121–128. https://doi.org/10.3989/scimar.2011.75n1121 terns in the movement of Procambarus clarkii, an invasive crayfish. Arce, E., & Alcaraz, G. (2013). Plasticity of shell preference and its an- Aquatic Sciences, 62(2), 179–193. https://doi.org/10.1007/PL000 tipredatory advantages in the hermit crab Calcinus californiensis. 01330 Canadian Journal of Zoology, 91, 321–327. https://doi.org/10.1139/ González-Pisani, X., Barón, P. J., & López, G. L. S. (2017). Integrated cjz-2012-0310 analysis of sexual maturation through successive growth instars Beck, M. W. (1995). Size-specific shelter limitation in stone crabs: A test in the spider crab Leurocyclus tuberculosis (Decapoda: Majoidea). of the demographic bottleneck hypothesis. Ecology, 76, 968–980. Canadian Journal of Zoology, 95(7), 473–783. https://doi.org/10.1139/ https://doi.org/10.2307/1939360 cjz-2016-0034 Beck, M. W. (1997). A test of the generality of the effects of shelter Goshima, S., & Murai, M. (1988). Mating investment of male fiddler bottlenecks in four stone crab populations. Ecology, 78, 2487– crabs, Uca lacteal. Animal Behaviour, 36, 1249–1251. https://doi. 2503. https://doi.org/10.1890/0012-9658(1997)078[2487:ATOTG org/10.1016/S0003-3472(88)80091-5 O]2.0.CO;2 Green, P. T. (1997). Red crabs in rain forest on Christmas Island, Indian Boujard, T., & Leatherland, J. F. (1992). Circadian rhythms and feeding Ocean: Activity patterns, density and biomass. Journal of Tropical time in fishes. Environmental Biology of Fishes, 35, 109–131. https:// Ecology, 13, 17–38. https://doi.org/10.1017/S0266467400010221 doi.org/10.1007/BF00002186 Hall, M. I., & Ross, C. F. (2007). Eye shape and activity pat- Brandford, M. J., & Higgins, P. S. (2001). Habitat-, season-, and size-spe- tern in birds. Journal of Zoology, 271, 437–444. https://doi. cific variation in diel activity patterns of juvenile chinook salmon org/10.1111/j.1469-7998.2006.00227.x (Oncorhynchus tshawytscha) and steelhead trout (Oncorhynchus my- Howard, A. E. (1982). The distribution and behaviour of ovigerous edible kiss). Canadian Journal of Fisheries and Aquatic Sciences, 58(2), 365– crabs (Cancer pagurus), and consequent sampling bias. ICES Journal 374. https://doi.org/10.1139/f00-253 of Marine Science, 40(3), 259–261. https://doi.org/10.1093/icesj Cioni, A., & Gherardi, F. (2004). Agonism and interference competition ms/40.3.259 in freshwater decapods. Behaviour, 141, 1297–1324. https://doi. Innes, A. J., Haj, A. J. E., & Gobin, J. F. (1986). Scaling of the respiratory, car- org/10.1163/15685 3 9 0 4 2 7 2 9 7 0 2 dio-vascular and skeletal muscle systems of the freshwater/terrestrial Cooke, S. J., Chandroo, K. P., Beddow, T. A., Moccia, R. D., & McKinley, mountain crab, Pseudothelphusa garmani garmani. Journal of Zoology, R. S. (2000). Swimming activity and energetic expenditure of captive 209(4), 595–606. https://doi.org/10.1111/j.1469-7998.1986.tb036 rainbow trout Oncorhynchus mykiss (Walbaum) estimated by electro- 14.x myogram telemetry. Aquaculture Research, 31, 495–505. https://doi. Iribarne, O., Bortolus, A., & Botto, F. (1997). Between-habitat differences org/10.1046/j.1365-2109.2000.00470.x in burrow characteristics and trophic modes in the southwestern Crane, J. (1949). Fresh-water crabs of the genus Pseudothelphusa from Atlantic burrowing crab Chasmagnathus granulata. Marine Ecology Rancho Grande, Venezuela. Zoologica, 34(1), 24–30. Progress Series, 155, 137–145. https://doi.org/10.3354/meps155137 Crawford, S. C. (1934). The habits and characteristics of nocturnal IUCN (2012). IUCN red list categories and criteria: Version 3.1, 2nd edn. animals. The Quarterly Review of Biology, 9, 201–214. https://doi. Gland, Switzerland and Cambridge, UK: IUCN. 32 p. org/10.1086/394460 Jensen, G. C., McDonald, P. S., & Armstrong, D. A. (2002). East meets Cumberlidge, N. (2008). Pseudothelphusa dugesti. The IUCN Red list of west: Competitive interactions between green crab Carcinus mae- threatened species 2008: e.T134196A3917805. doi: 10.2305/IUCN. nas, and native and introduced shore crab Hemigrapsus spp. Marine UK.2008.RLTS.T134196A3917805.en. Ecology Progress Series, 225, 251–262. https://doi.org/10.3354/ De La Torre, Z. A. M., Arce, E., Luna-Figueroa, J., & Córdoba-Aguilar, A. meps225251 (2018). Native fish, Cichlasoma istlanum, hide for longer, move and Jivoff, P. (1997). Sexual competition among male blue crab, Callinectes eat less in the presence of a non-native fish, Amatitlania nigrofasci- sapidus. The Biological Bulletin, 193(3), 368–380. https://doi. ata. Environmental Biology of Fishes, 101, 1077–1082. https://doi. org/10.2307/1542939 org/10.1007/s10641-018-0761-z Jivoff, P., & Hines, A. H. (1998). Female behavior, sexual competition and Díaz, H., & Conde, J. E. (1989). Population dynamics and life history of mate guarding in the blue crab, Callinectes sapidus. Animal Behaviour, the mangrove crab Aratus pisonii (Brachyura, Grapsidae) in a marine 55(3), 589–603. https://doi.org/10.1006/anbe.1997.0646 environment. Bulletin of Marine Science, 45(1), 148–163. 6 of 6 | PANIAGUA DOMÍNGUEZ et al.

Kupferberg, S. J., Palen, W. J., Lind, A. J., Bobzien, S., Catenazzi, A., Richards, A. R. (1992). Habitat selection and predator avoidance: Drennan, J., & Power, M. E. (2012). Effects of flow regimes altered Ontogenetic shifts in habitat use by the Jonah crab Cancer borealis by dams on survival, population declines, and range-wide losses of (Stimpson). Journal of Experimental Marine Biology and Ecology, 156(2), California river-breeding frogs. Conservation Biology, 26(3), 513–524. 187–197. https://doi.org/10.1016/0022-0981(92)90245-6 https://doi.org/10.1111/j.1523-1739.2012.01837.x Rio, J. P. P., Hernáez, P., & Pinheiro, M. A. A. (2019). Relative growth, Lau, W. W. Y., & Martinez, M. M. (2003). Getting a grip on the intertidal: sexual maturity and handedness in the ghost shrimp Callichirus major Flow microhabitat and substratum type determine the dislodgement (Decapoda: Callianassidae) from the southwestern Atlantic. Scientia of the crab Pachygrapsus crassipes (Randall) on rocky shores and in Marina, 83(2), 167–175. https://doi.org/10.3989/scimar.04869.28A estuaries. Journal of Experimental Marine Biology and Ecology, 295(1), Ryer, C. H. (1987). Temporal patterns of feeding by blue crabs (Callinectes 1–21. https://doi.org/10.1016/S0022-0981(03)00276-4 sapidus) in a tidal-marsh creek and adjacent seagrass meadow in Lee, S. Y. (1998). Ecological role of grapsid crabs in mangrove ecosys- the lower Chesapeake Bay. Estuaries, 10(2), 136–140. https://doi. tems: A review. Marine and Freshwater Research, 49(4), 335–343. org/10.2307/1352178 https://doi.org/10.1071/MF97179 Sanvicente-Añorve, L., Lemus-Santana, E., & Solís-Weiss, V. (2016). Body Marijnissen, S. A. E., Michel, E., Clearly, D. F. R., & McIntyre, P. B. (2009). growth pattern of an isolated land crab species (Johngarthia planata) Ecology and conservation status of endemic freshwater crabs in Lake (Decapoda, Gercarcinidae) from the Eastern Tropical Pacific: An Tanganyika, Africa. Biodiversity and Conservation, 18(6), 1555–1573. ecological approach. Crustaceana, 89(13), 1525–1539. https://doi. https://doi.org/10.1007/s10531-008-9543-9 org/10.1163/15685403-00003602 Martinez, M. M. (2001). Running in the surf: Hydrodynamics of the shore SEMARNAT. (2014). Plan de manejo SEMARNAT-UMA-INT-079- crab Grapsus tenuicrustatus. Journal of Experimental Biology, 204, MOR/14. México. 66 pp. 3097–3112. SEMARNAT. (2010). Norma Oficial Mexicana NOM-059- Martínez-Garza, C., Osorio-Beristain, M., Valenzuela-Galván, D., & SEMARNAT-2010, Protección ambiental-Especies nativas de México Nicolás-Medina, A. (2011). Intra and inter-annual variation in seed de flora y fauna silvestres-Categorías de riesgo y especificaciones rain in a secondary dry tropical forest excluded from chronic distur- para su inclusión, exclusión o cambio-Lista de especies en riesgo. bance. Forest Ecology and Management, 262, 2207–2218. https://doi. México. 68 p. org/10.1016/j.foreco.2011.08.013 Simonetti, J. (1984). Utilización de refugio por Lialaemus nigromacula- Miranda-Anaya, M., Barrera-Mera, B., & Ramírez-Lomelí, E. (2003). tus entre riesgos de predación y necesidades termorregulatorias. Circadian locomotor activity rhythm in the freshwater crab Studies on Neotropical Fauna and Enviroment, 19, 47–51. https://doi. Pseudothelphusa americana (DeSaussure, 1857): Effect of eyestalk org/10.1080/01650528409360643 ablation. Biological Rhythm Research, 34(2), 167–177. https://doi. Smith, V. H. (2003). Eutrophication of freshwater and coastal marine org/10.1076/brhm.34.2.167.14486 ecosystems a global problem. Environmental Science and Pollution Miranda-Anaya, M., Ramírez-Lomelí, E., Carmona-Alcocer, V. P., & Research, 10(2), 126–139. https://doi.org/10.1065/espr2002.12.142 Barrera-Mera, B. (2003). Circadian locomotor activity under ar- Sneddon, L. U., Huntingford, F. A., & Taylor, A. C. (1997). Weapon size tificial light in the freshwater crab Pseudothelphusa americana. versus body size as a predictor of winning in fights between shore Biological Rhythm Research, 34(5), 447–458. https://doi.org/10.1076/ crabs, Carcinus maenas (L.). Behavioral Ecology and Sociobiology, 41(4), brhm.34.5.447.27847 237–242. https://doi.org/10.1007/s002650050384 Moksnes, P. O., Pihl, L., & Van Montfrans, J. (1998). Predation on post- Somers, M. J., & Nel, J. A. J. (1998). Dominance and population struc- larvae and juveniles of the shore crab Carcinus maenas: Importance ture of freshwater crabs (Potamonautes perlatus Milne Edwards). of shelter, size and cannibalism. Marine Ecology Progress Series, 166, South African Journal of Zoology, 33(1), 31–36. https://doi. 211–225. https://doi.org/10.3354/meps166211 org/10.1080/02541858.1998.11448450 Olden, J. D., Hogan, Z. S., & Vander, Z. M. J. (2007). Small fish, big fish, red Taggart, S. J., O´Clair, C. E.,Shirley, T. C., & Mondragon, J. (2004). fish, blue fish: Size-biased extinction risk of the world´s freshwater Estimating Dungeness crab (Cancer magister) abundance: Crab pots and marine fishes. Global Ecology and Biogeography, 16(6), 694–701. and transects compared. Fishery Bulletin, 102(3), 488–497. http:// https://doi.org/10.1111/j.1466-8238.2007.00337.x fishbull.noaa.gov/1023/tagga rt.pdf Paul, A. J., & Paul, J. M. (1996). Observations on mating of multiparous Villalobos, J. L. (2005). Sistemática de los cangrejos de agua dulce de Chionoecetes bairdi Rathbun (Decapoda: Majidae) held with different México, Tribu Pseudethelphusini Ortmann, 1897 (Crustacea: sizes of males and one-clawed males. Journal of Crustacean Biology, Decapoda: Brachyura: Pseudothelphusidae). Análisis filogenético, 16(2), 295–299. https://doi.org/10.1163/193724096X00090 biogeográfico y descripción de especies nuevas. Tesis Doctoral, Penha-Lopes, G., Bartolini, F., Limbu, S., Cannici, S., Kristemsen, E., Universidad Nacional Autónoma de México. 407 p. & Paula, J. (2009). Are fiddler crabs potentially useful ecosystem engineers in mangrove wastewater wetlands? Marine Pollution Bulletin, 58(11), 1694–1703. https://doi.org/10.1016/j.marpo How to cite this article: PaniaguaDEC, Arce UE, Viveros- lbul.2009.06.015 Guardado DA. Population density, microhabitat use, and size Poon, D. Y. N., Chan, B. K. K., & Williams, G. A. (2010). Spatial and temporal variation in diets of the crabs Metopograpsus frontalis (Grapsidae) characteristics of Pseudothelphusa dugesi, a threatened and Perisesarma bidens (Sesarmidae): Implications for mangrove food species of freshwater crab from Mexico (Brachyura: webs. Hydrobiologia, 638, 29–40. https://doi.org/10.1007/s1075 Pseudothelphusidae). Invertebr Biol. 2020;00:e12295. https:// 0-009-0005-5 doi.org/10.1111/ivb.12295 Reaney, L. T. (2007). Foraging and mating opportunities influence refuge use in the fiddler crab, Uca mjoebergi. Animal Behaviour, 73, 711–716. https://doi.org/10.1016/j.anbehav.2006.05.022

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