Research Article |
Corresponding author: Scott Monks ( 1scottmonks@hotmail.com ) Academic editor: Michael Ohl
© 2016 Juan Violante-González, Scott Monks, Guadalupe Quiterio-Rendon, Sergio García-Ibáñez, Edvino Larumbe-Morán, Agustín A. Rojas-Herrera.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Violante-González J, Monks S, Quiterio-Rendon G, García-Ibáñez S, Larumbe-Morán E, Rojas-Herrera AA (2016) Life on the beach for a sand crab (Emerita rathbunae) (Decapoda, Hippidae): parasite-induced mortality of females in populations of the Pacific sand crab caused by Microphallus nicolli (Microphallidae). Zoosystematics and Evolution 92(2): 153-161. https://doi.org/10.3897/zse.92.8256
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Parasites, by definition, can affect mortality of their host, making parasitism an important biotic determinant of animal population dynamics and community structure. Reduction in the number of larger, reproductive age females in populations of the Pacific sand crab, Emerita rathbunae (Decapoda, Hippidae), was observed in studies of the helminth community of this host. The aim of this study was to determine if high abundance of the metacercaria of the trematode, Microphallus nicolli (Microphallidae), causes mortality in this host. Females of E. rathbunae were collected from four sandy beaches in Guerrero State, Mexico, and helminths were collected from each crab. An analysis of variance (Anova) was applied to these data in order to identify differences in abundance between sizes of crabs, and an analysis of covariance (Ancova) was applied to identify differences in the abundance of metacercariae between locations. Parasite-related mortality was inferred by a decrease in abundance in older hosts. Linear and polynomial regressions of mean abundance of helminths (log x+1 transformed data) vs. cephalothorax length of crabs were significant for the four populations of E. rathbunae, indicating increased mortality of older, more heavily infected female crabs and resultant removal from the population. Encapsulation and melanization of cysts by crabs was observed, indicating that an immune response by crabs also killed a portion of the cysts from subsequent exposures. Mortality of hosts through behavioral modification favoring transmission of highly infected crabs was suggested as the driving force behind this process.
helminth parasite, parasite-mediated mortality of hosts, parasite population parameters, Guerrero State, Mexican coast
Parasitism is an important biotic determinant of animal population dynamics and community structure. Parasites can influence host numbers within a population by either decreasing recruitment rate (by reducing host fecundity) or increasing mortality rate. Host mortality attributable to parasites can occur as a reduction in host survival due to the pathological consequences of parasitic infection, or as alterations in a host’s phenotype and/or behavior to facilitate parasite transmission to definitive hosts via predation (
Several approaches based on statistical evidence have been used in a number of studies in an attempt to determine if infection with parasites affects host mortality rates in natural populations (
The Pacific sand crab, or mole crab, Emerita rathbunae Schmitt, 1935 is common in the splash zone of sandy beaches in the intertidal zone (
The Mexican Pacific coastal region experiences two distinct climatic seasons, a rainy period from June to November (precipitation ≈ 430 mm), and a dry season from December to May (precipitation < 70 mm). Adult females of E. rathbunae (Table
Infection parameters of metacercariae of Microphallus nicolli in Emerita rathbunae from four coastal locations in Guerrero, Mexico. Significant values for the relationship between crab size (cephalothorax length) and metacercariae abundance per infected host (rs) are in bold. P (%) = Prevalence of infection (% of infected crabs); Range of Intensity = minimum and maximum number of metacercariae; rs = Spearman’s correlation coefficient.
Date (2009) | Locality | No. of crabs | Cephalothorax length (mm) | Total number of parasites | P (%) | Mean abundance of metacercariae | Range of Intensity | rs |
---|---|---|---|---|---|---|---|---|
Sep. | San Andrés | 146 | 37.6 ± 2.9 | 40,3414 | 100 | 2763.1 ± 1235.6 | 300 - 6000 | 0.208 |
Oct. | Revolcadero | 114 | 34.2 ± 1.7 | 107,921 | 100 | 946.7 ± 796.8 | 103 - 4235 | 0.609 |
Nov. | Las Trancas | 173 | 38.2 ± 2.2 | 403,177 | 100 | 2330.5 ± 1076.8 | 1050 - 5800 | 0.444 |
Dec. | Ixtapa | 68 | 32.9 ± 5.6 | 58,241 | 100 | 856.5 ± 597.5 | 15 - 2550 | 0.689 |
Female crabs were captured by hand, placed in labeled plastic bags and transported to the laboratory of the Unidad Académica de Ecología Marina, Universidad Autónoma de Guerrero, Acapulco. Before dissection, cephalothorax length (CL in mm) was measured to the nearest 0.1 millimeter using a digital caliper. This parameter was treated as the standard crab size in the analyses. Crabs were dissected by first removing the carapace, and then examining the internal structures, hepatopancreas, stomach, intestine, and muscle tissue, for helminths. Helminths were collected using standard practices and processed for identification (
Infection parameters included prevalence (percent of infected hosts); abundance (number of parasites per examined host) expressed as the mean ± standard deviation; range of intensity (
Size varied among the encysted metacercariae of M. nicolli, and a number of melanized cysts were found in each infected crab, so samples of cysts were measured (length and maximum width in μm) using an ocular micrometer for two locations (San Andrés and Las Trancas; n = 866). These measurements were used to calculate the volume of live cysts (mm3) using the volume formula for a scalene ellipsoid [V = (4/3) π (a/2) (b/2) (c/2) where a is cyst length, b is cyst width, and c is cyst height]. Melanized cysts were considered to contain dead metacercaria (
Mean parasite load (total number of live metacercariae of all sizes/total number of crabs that were examined) was plotted versus size-class of crabs for the four localities in order to evaluate the affect of this parameter on host mortality; a close relationship was assumed between age and size (
The total sample size was 591 female crabs (E. rathbunae), ranging from 68 individuals at Ixtapa to 173 at Las Trancas (Table
Cephalothorax length was correlated positively with abundance of metacercariae at all locations (P < 0.05), although correlation coefficient values (rs) were low in most cases (Table
Mean length and width measurements and the volume (mm3) of encysted metacercariae of Microphallus nicolli by development stage. Global percentage of melanized cysts corresponds to the sum of the percentages found in the three stages.
Cyst stage | No. of cysts | Length (mm) | Width (mm) | Volume (mm3) | Global percentage of melanized cysts | Mean number of melanized cysts |
---|---|---|---|---|---|---|
Immature | 247 | 0.259 ± 0.040 | 0.221 ± 0.034 | 0.0066 | 37% | 91.4 |
Late immature | 233 | 0.350 ± 0.038 | 0.301 ± 0.035 | 0.0166 | 26% | 86.2 |
Mature | 151 | 0.591 ± 0.046 | 0.393 ± 0.038 | 0.0477 | 16% | 55.9 |
Melanized cyst | 235 | 0.317 ± 0.062 | 0.269 ± 0.044 | 0.0125 | 21% | -- |
Distribution of cysts, based on developmental stage and crab size, did not differ at the two locations where this was analyzed (San Andrés and Las Trancas). The percentage of mature cysts decreased as crab size increased, and the percentage of melanized cysts increased with the increase (small to large) in the size of crabs (Fig.
Percentages of cysts of Microphallus nicolli by development stage of cysts and size-classes of female crabs (Emerita rathbunae). Hatched bars = immature cysts; Shaded bars = late immature cysts; Open bars = mature cysts; Dark bars = melanized cysts. Data are only from San Andrés (A) and Las Trancas beaches (B). Stages of cyst maturity were modified from
Linear and polynomial regressions of the relationship between mean abundance of helminths (log x+1) and cephalothorax length of crabs were significant at all four beaches (Table
Results of the regression analysis used to evaluate the relationship between number of cysts of Microphallus nicolli (log x+1) per crab and the cephalothorax length of crabs from four coastal locations in Guerrero, Mexico. n = number of crabs that were examined; R2 = coefficient of determination; P = significance level. Note: 100% of the crabs examined were infected.
Linear | Polynomial | |||||
---|---|---|---|---|---|---|
Locality | n | R2 | P | R2 | P | Curve type |
San Andrés | 146 | 0.297 | 0.0001 | 0.330 | 0.0001 | Convex |
Revolcadero | 114 | 0.393 | 0.0001 | 0.395 | 0.0001 | Concave |
Las Trancas | 173 | 0.235 | 0.0001 | 0.300 | 0.0001 | Concave |
Ixtapa | 68 | 0.508 | 0.0001 | 0.588 | 0.0001 | Convex |
Species of Microphallus infect several species of marine crustaceans that function as second intermediate hosts; adult worms mature mainly in coastal birds (
Although prevalence of M. nicolli did not differ between the four locations, mean abundance was significantly higher at San Andrés and Las Trancas (Table
It is possible that variation in the abundance of M. nicolli between the four locations is the result of a factor or process related to the size of the crabs that might influence this infection parameter (
Metacercaria of M. nicolli continue to grow post-encystment (
A high percentage of cysts had been encapsulated and melanized (Table
The overall percentage of mature (large) cysts was lower than the percentage of the two earlier stages (Table
Ample evidence exists of parasite-induced mortality in marine crustacean populations under field conditions (
If an infrapopulation of a species of parasite does not induce host mortality, then a positive linear relationship can be expected between host size and parasite abundance due to parasite accumulation in the host over time (
In some studies of host mortality induced by helminth parasites, differences have been reported in the effect of parasites between host species and locations (
The most plausible explanation for the lower abundance of metacercaria in larger size crabs is the regulation of the population of E. rathbunae through elimination of a high proportion of metacercariae cysts, directly by mortality of crabs or by favoring the capture of the more highly-infected crabs (the larger, older hosts) (
Parasite-induced mortality in populations of a marine crustacean (E. rathbunae) under field conditions by infrapopulations of the metacercaria of M. nicolli is documented in four populations of sand crabs in Guerrero, Mexico. These results are consistent with previous studies of other Crustacea-Digenea host-parasite systems. Evidence that the population of E. rathbunae is affected, and possibly regulated, by the infrapopulations of M. nicolli consists of five factors: 1. Mean volumetric abundance of metacercariae generally decreased as crabs aged (grew larger), but the proportion of mature cysts decreased, suggesting that the metacercariae were growing, but that crabs with a higher proportion of more mature cysts had been removed (preferentially?) from the population of crabs; 2. Linear and polynomial regressions of mean abundance of helminths (log x+1) vs. cephalothorax length of crabs were significant for the four populations of E. rathbunae (Table
Funds for this study were provided to the authors by the Programa de Mejoramiento del Profesorado (PROMEP) as part of the collaborative project “Calidad ambiental y desarrollo sustentable: evaluación del impacto ambiental por actividades antropogénicas- alternativas de mitigación” (third year). Other funds (to JV-G) were provided by the project “Parásitos de rayas de importancia económica y ecológica en la Bahía de Acapulco, Gro.”, financed by the Universidad Autónoma de Guerrero, and the project “Fortalecimiento del Doctorado en Ciencias Ambientales de la Universidad Autónoma de Guerrero”, financed by Fondos Mixtos-Consejo Nacional de Ciencia y Tecnología (CONACyT)-Guerrero (2015). Guadalupe Quiterio-Rendón assisted with the processing of much of the material as part of her MS thesis project; she received a scholarship (No. 247514) from CONACyT during this study. The authors wish to thank students of the Marine Ecology Academic Unit (UAG) for their assistance with field and laboratory work, and the local residents who assisted with collection of the crabs.