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Revista de biología marina y oceanografía

versión On-line ISSN 0718-1957

Rev. biol. mar. oceanogr. vol.55 no.3 Valparaíso dic. 2020  Epub 01-Dic-2020

http://dx.doi.org/10.22370/rbmo.2020.55.3.2589 

Article

Euceramus transversilineatus (Decapoda: Porcellanidae) living in the mantle lobe of the snail Melongena patula (Gastropoda: Melongenidae) in the south eastern Gulf of California: Inference of a biological association

Euceramus transversilineatus (Decapoda: Porcellanidae) viviendo en el lóbulo del manto del caracol de Melongena patula (Gastropoda: Melongenidae) en el sureste del Golfo de California: Inferencia de una asociación biológica

Andrés Martín Góngora-Gómez1 
http://orcid.org/0000-0001-8613-5480

Manuel II García-Ulloa2 
http://orcid.org/0000-0002-6194-9565

Diego García-Ulloa1 
http://orcid.org/0000-0003-1168-9643

Manuel García-Ulloa1  * 
http://orcid.org/0000-0001-5357-8891

José Salgado-Barragán3 
http://orcid.org/0000-0002-3414-4008

Juan Francisco Arzola-González4 
http://orcid.org/0000-0003-3349-1021

Juan Antonio Hernández-Sepúlveda5 
http://orcid.org/0000-0003-4749-3749

1Departamento de Acuacultura, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Instituto Politécnico Nacional, Unidad Sinaloa, Guasave 81101, Sinaloa, México

2Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad de México 04510, México

3Laboratorio de Invertebrados Bentónicos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Unidad Mazatlán, Mazatlán 82040, Sinaloa, México

4Facultad de Ciencias del Mar, Universidad Autónoma de Sinaloa, Mazatlán 82000, Sinaloa, México

5Departamento de Medio Ambiente, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Instituto Politécnico Nacional, Unidad Sinaloa, Guasave 81101, Sinaloa, México

Abstract:

There are abundant reports of symbiosis wherein crustaceans live inside or on mollusks; however, there are few published records of gastropods hosting decapods. This study examines the biological association between fifteen snails (124.86 ± 19.01) from the species Pacific crown conch Melongena patula and the porcelain crab Euceramus transversilineatus. Morphometric relationships of both invertebrates, as well as some sexual characteristics of the crab were conducted. These invertebrates were sampled in the Navachiste Lagoon, in the south eastern Gulf of California, Sinaloa, Mexico. It was found 86.6% of the snails housed at least a female or a male porcelain crab (17.82 ± 3.27 mm total body length) or a pair of them (heterosexual and same sex) with a sexual proportion of 2M:1F. There were no correlations between any of the crab and snail based on their analyzed morphometric relationships. For the crab males, the measurements of both chelae presented relationships with total body length, carapace length, and abdomen width however, no significant differences were observed between the mean width and chelae length of males, females or between sexes. Of the six females collected, four were gravid. Preliminary observations indicated that the porcelain crab E. transversilineatus is a commensal endosymbiont that coexist in short-term association with M. patula. Their population distribution suggests that E. transversilineatus are polygamous with a promiscuous mating pattern.

Key words: Symbiosis; porcelain crab; Pacific Crown conch; morphometry; Sinaloa; Mexico

Resumen:

Existen abundantes informes de simbiosis en los que los crustáceos viven dentro o encima de moluscos, sin embargo, hay pocos registros publicados de gasterópodos que alberguen decápodos. Se examinó la asociación biológica entre el caracol corona del Pacífico, Melongena patula, y el cangrejo porcelánido, Euceramus transversilineatus, describiendo las relaciones morfométricas de ambos invertebrados, así como algunas características sexuales del cangrejo. Se muestrearon 15 caracoles (124,86 ± 19,01 mm de altura de concha) en la laguna Navachiste, en el sureste del Golfo de California, Sinaloa, México. El 86,6% de ellos albergaba al menos un cangrejo de porcelana hembra o macho (17,82 ± 3,27 mm de longitud total del cuerpo) o un par (heterosexual y mismo sexo) con una proporción sexual de 2M:1H. No hubo correlaciones entre ninguna de las relaciones morfométricas analizadas entre el cangrejo y caracol. Para los cangrejos, las mediciones de ambas quelas presentaron relaciones con la longitud corporal total, longitud del caparazón y ancho del abdomen en los machos; sin embargo, no se observaron diferencias significativas entre el ancho medio y la longitud de quelas de machos, hembras o entre sexos. De las seis hembras recolectadas, cuatro eran grávidas. Las observaciones preliminares indican que el cangrejo porcelánido E. transversilineatus es un endosimbionte comensal que coexiste en asociación a corto plazo con M. patula. Su distribución poblacional sugiere que E. transversilineatus es polígamo con un patrón de apareamiento promiscuo.

Palabras clave: Simbiosis; cangrejo porcelánido; caracol corona del Pacífico; morfometría; Sinaloa; México

Introduction

Symbiosis is the term generally used to design biological associations between different species, and it refers to a long-term and close interaction between two different organisms or symbionts (Hoffmeister & Martin 2003). Such interactions are classified as commensalistic, parasitic or mutualistic relationships and these interactions can be intra- or inter-specific (Rizzo & Lo-Giudice 2018). Biological associations between marine invertebrates represent strategies of evolutionary adaptation in response to selective pressures exerted by environmental conditions of the ocean, interaction between members of a community and more recently by anthropogenic effects and climate change (Nagelkerken et al. 2016, Baker et al. 2018). Invertebrates such as annelids, bryozoans, crustaceans and mollusks, among others, coexist in order to acquire refuge, food, and/or reproductive niches (Baeza 2007, Beu & Zibrowius 2007, Ocampo et al. 2014, Tenjing 2017).

Examples of symbiotic association between mollusks which serve as hots to crustaceans are well documented for various species thoroughout the world. Baeza et al. (2013) described the sexual and mating system of the shrimp Paranchistus pycnodontae Bruce, 1978, inhabiting the penguin’s wing oyster Pteria penguin Röding, 1798, in Papua New Guinea. On the Pacific coast of Costa Rica, Mena et al. (2014) documented the level of infestation of the pea crab Austinotheres angelicus Lockington, 1877, living in the palmate oyster Saccostrea palmula Carpenter, 1857. Meanwhile, in the Gulf of California, García-Ulloa et al. (2019) detailed the sexual characteristics of the pearl oyster shrimp Pontonia margarita Smith in Verril, 1869, inhabiting the mantle cavity of the rugose pen shell Pinna rugosa Sowerby I,1835.

Although most porcelain crab species are free-living (Rodríguez et al. 2005), many of them have been found in endo or ectosymbiotic relationships (living inside or outside of the host, respectively) living as parasites, commensalistic or mutualistic relationships with a variety of organisms such as anemones (Baeza & Stotz 2003, López-Victoria et al. 2004), sea cucumbers (Werding 1983), different species of molluscs (Boyko & Mikkelsen 2002) and even other crustaceans (Werding 1977, Rocha-Duarte-Alencar et al. 2014). In addition, Baeza & Stotz (2001) documented host-selection by the commensal crab Allopetrolisthes spinifrons, Milne-Edwards, 1837, dependent on the availability of sea anemones as hosts.

The symbiotic association of anomuran crustaceans living inside marine snails is limited. It was reported that the presence of the spotted porcelain crab Porcellana sayana, Leach, 1820, was living inside the shell of the queen conch, Strombus gigas, Linneo, 1758, in Barbados (Telford & Daxboeck 1978). These authors reported the occurrence of up to two crabs in two different snail specimens and the sexual relationship and size of the porcelain crabs. Baeza & Stotz (2001) described for the first time the presence of A. spinifrons between the mantle lobe and foot of the edible gastropod Concholepas concholepas on the north central coast of Chile.

The incidental capture of Pacific crown conch Melongena patula Broderip & Sowerby, 1829, regionally known as “caracol burro” by the artisanal fishery in the southeastern Gulf of California, revealed a new biological association between this gastropod and the porcelain crab Euceramus transversilineatus Lockington, 1878. Therefore, the objective was to describe this association for the first time, which includes a preliminary description of the morphometric relationships of both invertebrates, as well as some sexual characteristics of the crab. Some studies have suggested that morphometric relationships between two symbiont marine invertebrates are related with their association time (Ocampo et al. 2012, Baeza et al. 2017). If our data are consistent among host-guest measurements then, the biological association will be a long-term. This information can be used for future studies related to biological association.

Materials and methods

Gastropods were collected at Boca de Vasiquilla, in the Navachiste coastal lagoon in September 2018. The sample site was located on the north coast of Sinaloa, Mexico (25°21'31"N-108°47'24"W) (Fig. 1).

Figure 1 Sampling location in Boca de Vasiquilla (black circle), Navachiste Bay, Gulf of California, Mexico / Sitio de muestreo en Boca de Vasiquilla (círculo negro), Bahía de Navachiste, Golfo de California, México 

Local fishermen engaged in the capture of fish and shrimp with the use of boats and bottom nets (15 mm between knots) had previously reported the incidental capture of snails harboring crabs either on their shell or attached to the soft tissue of the snail. The collection site was characterised by a muddy substrate and the environment conditions at the time of the sampling were 31 °C temperature, 35 salinity, strong swell, and 2 m visibility. The sampling method consisted of a fishing net which was placed at a depth of 10 m, where it remained overnight. The net was recovered early the following day (07:00 AM). The Pacific crown conch specimens were carefully untangled and placed individually in plastic bags. Then, specimens were transported to the Laboratory of Malacology at the Interdisciplinary Research Center for Regional Integral Development at the National Polytechnic Institute (CIIDIR-IPN), Sinaloa Unit, following the standard procedures (NOM)1. This research was approved by the Ethic Committee (College of Teachers) at the CIIDIR-IPN.

The following measurements of the Melongena patula shell were obtained with a caliper (± 0.01 mm); the total height (TH) from the apex to the siphon channel; the total width (TW) from the most distal point of the opening parallel to the apex to the most distal part of the outer lip; the height of the opening (HO) from the exhalation channel to the siphonal channel; the width of the opening (WO) or the most distal distance between the inner and outer lips; and the operculum width (OW) or the distance between the points perpendicular to the maximum length of the operculum (Fig. 2).

Figure 2 Body measurements of Melongena patula. A= total height (TH), B= total width (TW), C= height of the opening (HO), D= width of the opening (WO), E= operculum width (OW) / Medidas corporales de Melongena patula. A= altura total (TH), B= anchura total (TW), C= altura de la abertura (HO), D= anchura de la abertura (WO), E= anchura del opérculo (OW) 

The crabs were identified as Euceramus transversilineatus Lockington, 1878 following Hendrickx (1999)2, and the following traits were recorded for each specimen: the total body length (TBL) from the tip of the telson to the tip of the rostrum; the cephalothorax length (LC) from the tip of the rostrum to the posterior end of the carapace; the left (LLCH) and right (RLCH) chela length of the chelae from the end of the dactylum to the most distal edge of each chela; and left (WLCH) and right (WRCH) chelae width or the longest perpendicular distance from the propodium. The sex of the crabs was determined based on the position of the genital pore (base of the third or fifth pair of pereiopods for females and males, respectively) (de Azevedo-Ferreira 2018). The abdomen width (WA), the longest distance perpendicular to the total length of the abdomen, was recorded in males and females. For each ovigerous female, the egg mass (EM) was separated from the abdomen and placed in a Petri dish for counting under microscopic observation. The E. transversilineatus specimens were stored in glass jars and fixed in 70% ethanol stored. The crabs and empty conchs were kept in the Laboratory of Malacology at CIIDIR-IPN, Sinaloa Unit, and labeled as: Malacology/symbiosis-porcelánido/2018(15) and Malacology/symbiosis-snail/2018(15), respectively.

A sample size of fifteen individuals, considering an alpha significance criterion of 0.05, maintains a sufficient statistical power of 0.8, according to Cohen (1988, 1992) in correlations of r ≥ 0.65 (and r ≤ -0.65). Therefore, although in this study it is not possible to validate subtle correlations, the strong significant correlations, that is, when r ≥ 0.65 and r ≤ -0.65, are statistically valid (Fig. 3). Calculations were made with the pwr.r.test function from the pwr v1.3-0 R package (Champely 2020). Command used: pwr.r.test (n= NULL, r= values from 0.1 to 0.95 in increments of 0.05, sig. level= 0.05, power= 0.8). Vignette of pwr v1.3-0 in Champely (2020) 3.

Figure 3 Sample size required (Y axis) to obtain a statistical power of 0.8, considering an alpha of 0.05, given the hypothetical correlation between 2 variables (X axis) / Tamaño de muestra requerido (eje Y) para obtener un poder estadístico de 0,8, considerando un alfa de 0,05, dada la hipotética correlación entre 2 variables (eje X) 

The normality and homoscedasticity (Lilliefors & Bartlett’s tests, respectively) of data were evaluated before applying the appropriate statistical tests (Zar 1996). Pearson's correlation coefficient (r P ) was calculated between all measurements of male and female E. transversilineatus against each other, and separately against all measurements of M. patula using R-base. R-base was used to perform t-tests on the LLCH, LRCH, WLCH, WRCH of males, females, and between sexes of E. transversilineatus. The correlation heatmap was generated using R libraries reshape2 (Wickham 2007) and ggplot2 (Wickham 2016). Statgraphics Centurion (ver. 14.0, Softonic International S.A., Spain) was used to perform the statistical tests (P ≤ 0.05).

Results

Fifteen snails were collected from the Navachiste Lagoon. The TH fluctuated from 101.55 to 174.23 mm. The coefficients of variation for all measurements (TH, TW, HO, WO, and OW) were ˂23% (Table 1). All snail measurements were correlated with each other (Pearson’s correlation r P = 0.93, P = 0.0001, mean value).

Table 1 Body measurements (mm) of Melongena patula (n= 15) / Medidas corporales de Melongena patula (n= 15) 

Thirteen of the gastropods (86.6%) housed at least one porcelain crab (female or male) or pair (heterosexual and same sex) distributed as follows: four snails with a solitary male, one snail with a solitary non-gravid female, three snails with a solitary gravid female, one snail with a heterosexual pair (non-gravid female), one snail with a heterosexual pair (gravid female), and three snails with one male pair each. The crabs had a pearly white color and were strongly attached to the mantle lobe with the propodium and dactyl of each cephalothorax appendage (Fig. 4). Of the eighteen crabs observed, twelve (66%) were male and six (33%) were female for a sex ratio of 2M:1F.

Figure 4 Porcelanid crabs Euceramus transversilineatus (yellow circles) living in the mantle lobe of the Pacific crown conch Melongena patula / Cangrejos porcelánidos Euceramus transversilineatus (círculos amarillos) viviendo en el lóbulo del manto del caracol concha del Pacífico Melongena patula 

The correlations between the crab TBL and LC with the metric characteristics (TH, TW, HO, WO and OW) of Melongena patula are respectively shown in Figures 5 and 6.

Figure 5 Relationships between Euceramus trasnversilineatus (TBL, mm) and Melongena patula (TH, TW, HO, WO, and OW, mm) measurements. Males= empty circles, females= full circles / Relaciones entre las medidas de Euceramus transversilineatus (TBL, mm) y Melongena patula (TH, TW, HO, WO y OW, mm). Machos= círculos vacíos, hembras= círculos llenos 

Figure 6 Relationships between Euceramus trasnversilineatus (LC, mm) and Melongena patula (TH, TW, HO, WO, and OW, mm) measurements. Males= empty circles, females= full circles / Relaciones entre las medidas de Euceramus transversilineatus (LC, mm) y Melongena patula (TH, TW, HO, WO y OW, mm). Machos= círculos vacíos, hembras= círculos llenos 

There was no correlation between any of the crab and snail measurements analyzed; r P varied from 0.17 to 0.30 (Pearson’s correlation). Negative and positive r P values were obtained when comparing the relationships between snails and crabs by sex (Table 2).

Table 2 Regression equations, correlation coefficients (r P ), standard error of slope and P-value by sexes between Euceramus transversilineatus and Melongena patula measurements taken as indicated in Figure 2 / Ecuaciones de regresión, coeficientes de correlación (r P ), error estándar de la pendiente y valor de P por sexos entre Euceramus transversilineatus y Melongena patula tomadas como se indica en la Figura 2  

The r P values (Pearson’s correlation) for females and males ranged from -0.02 to 0.18 and -0.19 to 0.15, respectively. No correlations were found between the snail measurements and the TBL and LC of Euceramus transversilineatus by sex.

Porcelain crabs had a minimum and maximum TBL of 7.66 and 19.79 mm, respectively, meanwhile the LC ranged from 4.95 to 12 mm (Table 3). The LLCH and WLCH presented the highest coefficients of variation (28.68 and 33.54%, respectively).

Table 3 Body measurements (mm) of Euceramus transversilineatus (n= 18) / Medidas corporales de Euceramus transversilineatus (n= 18) 

There were significant correlations among several measurements of males E. transversilineatus (Fig. 7). Notably, the measurements of both chelae presented relationships (Pearson’s correlation) with TBL, LC, and WA in males; their carapace length was highly correlated with the length of both chelae (LC vs. LLCH: r P = 0.99, P = 0.01 and LC vs. LRCH: r P = 0.95, P = 0.05) and the WRCH (r P = 0.99, P = 0.01). For females, LC was correlated with the LLCH (r P = 1, P = 0.001).

Figure 7 Correlation heatmap comparing Euceramus transversilineatus measurements between sexes. Measurements with initial “m” or “f” belong to males and females, respectively. EM, egg mass; LC, carapace length; LLCH, length of left chela; RLCH, length of right chela; TBL, total body length; WA, width of abdomen; WLCH, width of left chela; WRCH, width of right chela. Upper value= r P value; lower value= P - value. *Significant correlation at 95% / Correlación (heartmap) comparando las medidas de Euceramus transversilineatus entre sexos. Las medidas con letra inicial “m” o “f” pertenecen a machos y hembras, respectivamente. EM, masa de huevos; LC, longitud de caparazón; LLCH, longitud de quela izquierda; RLCH, longitud de quela derecha; TBL, longitud corporal total; WA, anchura del abdomen; WLCH, anchura de la quela izquierda; WRCH, anchura de la quela derecha. Valor superior= valor de r P ; valor inferior= valor de P. *Correlación significativa a 95% 

There were no significant differences (Unpaired t - test) between the mean LLCH, RLCH, WLCH, and RLCH of males, females, or between sexes (Table 4).

Table 4 Unpaired t-tests of width and length for the right and left chelae of Euceramus transversilineatus males, females and between sexes / Pruebas de t no pareadas de la anchura y longitudes de las quelas derecho e izquierda de machos, hembras y entre sexos de Euceramus transversilineatus 

Of the six females collected, four were gravid (three solitary and one in a pair). The number of eggs per female ranged from 181 (13.78 mm TBL) to 565 (17.82 mm TBL) with an average of 304 ± 177.15. No correlation (Pearson’s correlation) was observed between the number of eggs and the abdomen width (r P = -0.68, P = 0.32); however, larger females contained more eggs (r P = 0.9, P = 0.10).

Discussion

Compared with other marine invertebrates such as bivalves (Salas-Moya et al. 2014) and ascidians (Levitt-Barmats & Shenkar 2018) that host endosymbiotic crustaceans, the snail M. patula is a large and morphologically complex host which is capable of housing up to two porcelain crabs in the mantle cavity. Our observations coincide with those of Telford and Daxboeck (1978) who found up to two specimens of the crab Porcellana gayana on the inner surface of the operculum of the snail Strombus gigas. They reported that the porcellanids move inside the snail mantle cavity when these are disturbed by external factors (e.g., predators) and, when the foot is retracted, the crabs remain immovable and hidden between the foot and operculum. This behavior also was observed in this study (Fig. 4). The movement of the crabs inside M. patula would be subject to the displacement or retraction of the structures inside the snail (mantle, foot, and operculum; Telford & Daxboeck 1978), which could explain the state of apparent immobility of crabs when they were discovered at the edge of the foot and operculum.

Different endosymbiont porcellanids receive protection from their hosts in various ways. For example, P. sayana has been found living on the shell of the brachyuran crab Stratiolibinia bellicosa Oliveira, 1934, which offer protection in the form of camouflage provided by its shell and displaces the guest without exposing the crab to the marine substratum (Rocha-Duarte- Alencar et al. 2014). The snail shell represents a difficult barrier to be breached by a variety of predators (Němec & Horsák 2019); thus, the size, thickness, and color of the M. patula shell guarantees the protection of E. transversilineatus against small predators such as fish and other crustaceans.

Although there is evidence that some porcelain crabs parasitize their host (Bierbaum & Shumway 1988, Sun et al. 2006), the data collected in our study are not sufficient to explore a possible symbiotic effect the crab may confer on M. patula; further studies should address this question. For now, considering exclusively the protection granted by the snail, E. transversilineatus may be defined as an endocommensal. In fact, E. transversilineatus exhibits body characteristics typical of an endosymbiotic species, such as a flattened but corpulent body, with a small face, strong pereopods adapted for climbing and thick abdomen (Ross 1983, Bauer 2004). Its pearly white color would represent a disadvantage since it contrasts sharply against the dark muddy bottom (Carbajal Enzian et al. 2018), which highlights the importance of a protective service acquired when this porcelain crab is living associated with M. patula.

Corey & Reid (1991), Góngora-Gómez et al. (2015) and García-Ulloa et al. (2019) correlated the volume of bivalve shells with morphometric measurements of endosymbiotic crustaceans in terms of the space available for their accommodation. However, in the present study, no correlation was found between snail and crab measurements by crab pool and sex. Specimens of M. patula with HO and WO ranging from 91.86 to 141.45 and from 34.60 to 60.02 mm, respectively, accommodated up to two crabs measuring between 7.66 and 19.79 mm TBL. However, considering their mean size (124.86 ± 19.01 mm), a given snail could accommodate more than two crabs; a hypothesis that warrants further investigation. Baeza et al. (2017) found up to four palemonid shrimp Periclimenes paivai Costa, 1844, located in the inner region of the umbrella and tentacles of the Lychnorhiza lucerna Haeckel, 1880, jellyfish, a morphologically complex and large host (89-220 mm in diameter). In our study, the lack of correlation between snail and crab measurements suggests that these invertebrates do not grow together. Thus, their symbiotic association could be considered a short-term commensal relationship benefitting the guest E. transversilineatus, specifically, ensuring the survival and reproduction of the porcellanid crab in the shelter provided by the morphology of the snail. Similar observations were noted by Baeza et al. (2013) and García-Ulloa et al. (2019) for pontonid shrimps reproducing inside mollusks.

The reproductive advantage conferred on the guest by the host is strongly related to the concept of protection. Grafen & Ridley (1983) and Thiel et al. (2003a) concluded that monogamy between symbiont hosts is related to a sexual proportion without bias toward either sex, so that it would be common to find heterosexual pairs of symbionts in each host (Baeza et al. 2015). Our study does not support this hypothesis for at least two reasons: (1) the presence of twice the number of males as females suggests that the mating and reproduction system of E. transversilineatus is polygamous, as reported by Thiel et al. (2003b) for A. spinifrons inhabiting the anemone Phymanthea pluvia, Drayton in Dana, 1846; and (2) the sexual distribution of the crab in M. patula (solitary males, solitary females, heterosexual pairs with gravid or non-gravid females and pairs of males) indicates that both males and females move between hosts in search of reproductive partners, reflecting polygamous and promiscuous reproductive behavior (Baeza 2008, Baeza et al. 2016). This would result in the crab having low fidelity to the host snail, where it would remain exclusively for reproductive purposes (Ocampo et al. 2012). The presence of E. transversilineatus in 86.6% of the snails captured indicates a high degree of symbiotic occupation; however, the results obtained are based on data from a single sample (September, summer) and patterns may vary during other seasons or at other sites with different environmental conditions. This hypothesis should be verified though ongoing research (Puente-Tapia et al. 2018).

Unlike pontonid shrimp in which the male is smaller than the female (Baeza 2008, Aucoin & Himmelman 2010, Góngora-Gómez et al. 2015), E. transversilineatus showed no sexual dimorphism (r P = -0.34, P = 0.66). Moreover, the chelae dimensions among males, females, and between the two sexes were not significantly different. This pattern suggests that pregnant females do not need the protection of a male during the egg incubation. Proportionally, larger chela in males indicates that this appendix is used as a weapon for defense, attack, or protection in monogamous species (Baeza & Thiel 2007); this was not the case in our study.

Among crustaceans, females of greater body length have a larger abdomen to contain more eggs (Salas-Moya et al. 2014); however, in our study no significant correlation was observed between female body dimensions and number of eggs. This pattern has been reported by García-Ulloa et al. (2019) for females of the pearl oyster shrimp Pontonia margarita in symbiosis with the rugose pen shell Pinna rugosa.

In our study, (1) the porcelanid crab E. transversilineatus was found in the mantle cavity and edge of the operculum of the snail M. patula, and thus can be considered an endosymbiont; (2) the measurements of both invertebrates were not correlated, suggesting a short-term association; (3) E. transversilineatus is a commensal endosymbiont that is favored by snail protection without offering any apparent benefit in return; (4) the lack of correlation between the morphometry of female and male crabs suggests that females can fend for themselves regardless of their reproductive status; (5) the population distribution of E. transversilineatus presumes that both females and males leave their gastropod hosts to look for reproductive partners in other snails, reflecting a polygamous and promiscuous mating pattern; (6) at the same time, suggesting low fidelity to the host snail by porcellanids, as found by Thiel et al. (2003b); and finally, (7) the mantle cavity of M. patula is a comfortable and safe environment that favors the reproduction and temporary housing of ovigerous females of E. transversilineatus.

Our results are in accordance with reports of other species of symbiotic crustaceans. However, further research is needed to develop generalizations regarding the mechanisms of social and reproductive behavior of E. transversilineatus in symbiotic association with M. patula. Future studies should also focus on the conditions that favor or force the association between these invertebrates as an evolutionary strategy.

Acknowledgements

The authors thank the Instituto Politécnico Nacional for the logistical and economic support provided for the development of this research through the projects: “Morfometría y fisiología de la almeja venus Chione undatella de Bahía La Paz, y el puerto minero de Santa Rosalía, Baja California Sur, México” (IPNSIP 20195442), and “Incidencia estacional de nematodos y Perkinsus marinus de la almeja venus Chione undatella de bahía de La Paz y del puerto minero de Santa Rosalía, Baja California Sur, México” (IPNSIP 20190071). We thank Biol. Javier Quiñónez Gutiérrez for his invaluable help in the work of collecting organisms. Thanks to Dr. Kristin Sullivan for the English edition.

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Received: December 10, 2019; Accepted: October 28, 2020

*Corresponding author: turbotuag@hotmail.com

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