Behavioral changes in the grass shrimp, Palaemonetes pugio (Holthuis), induced by the parasitic isopod, Probopyrus pandalicola (Packard)

Department of Biological Sciences, Rutgers University, Newark, NJ 07102, USA
Journal of Experimental Marine Biology and Ecology (Impact Factor: 1.87). 08/1999; 241(2):223-233. DOI: 10.1016/S0022-0981(99)00084-2


Preliminary observations indicated that the grass shrimp, Palaemonetes pugio, parasitized by the isopod, Probopyrus pandalicola, captured significantly fewer prey items (Daphnia) and exhibited reduced activity compared to unparasitized conspecifics. Further research focused on elucidating the factors involved in altering the shrimp’s behavior. When viewed from above in an opaque container, activity levels of parasitized shrimp were considerably lower than unparasitized shrimp; however, when viewed from the side in a glass container, differences in activity were also seen, but not under all circumstances. In response to the observer above, the parasitized shrimp reduced their activity disproportionately. When (in the opaque tank) prey capture of Artemia was examined, there was no difference between parasitized and unparasitized shrimp’s capture rate. This is attributable to the greater activity of Artemia, which makes them more likely than Daphnia to encounter a relatively inactive predator. There was not a significant difference in prey capture when Cyprinodon larvae were used as prey and tanks were not observed from above. When predator avoidance was studied using mummichogs (Fundulus heteroclitus), we expected that the more conspicuous parasitized shrimp would be preyed upon more, but this was not the case. Their lowered activity in the presence of a predator apparently reduced their conspicuousness, so that they were not preyed on more than the unparasitized shrimp.

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Available from: Judith Weis
    • "A female-male pair of isopods is usually present within the branchial chamber of each parasitized shrimp (Kensley & Schotte, 1989), which typically remains with the host until its death (Beck, 1980a). Research on this parasite has included its life history (Beck, 1980a; Anderson & Dale, 1981, 1989; Anderson, 1990), prevalence (Chaplin-Ebanks & Curran, 2007; Key et al., 2011), and relationship with its shrimp hosts (Beck, 1980b, c; Anderson, 1990; Cash & Bauer, 1993; Bass & Weis, 1999; Chaplin-Ebanks & Curran, 2005; Sherman & Curran, 2013). Consumption of hemolymph by P. pandalicola can reach 10% of the total energy intake (Anderson, 1977) and up to 25% of total hemolymph volume of the shrimp on a daily basis (Walker, 1977). "
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    ABSTRACT: The bopyrid isopod Probopyrus pandalicola (Packard, 1879) is a large, noticeable, hematophagous ectoparasite of palaemonid shrimps, including the daggerblade grass shrimp Palaemonetes pugio Holthuis, 1949. Bopyrids affect grass shrimp physiology and may also affect predator-prey dynamics. The purpose of this study was to determine whether the isopod affected the behavior and/or camouflage of grass shrimp, thereby altering the predation preferences of the mummichog Fundulus heteroclitus (Linnaeus, 1766). To determine whether the isopod affected predator preference through behavioral and/or camouflage alterations, paired combinations of unparasitized, parasitized, and marked shrimp were presented to mummichogs. One branchiostegite of some of the unparasitized shrimp was marked with black paint to mimic the bopyrid parasite. Mummichog predation preference and shrimp behavior immediately prior to predation events were recorded. All shrimp behavior was classified as motionless, walking, swimming, or backward thrusting. Immediately prior to predation, parasitized shrimp swam more (p = 0.0477) and backward thrusted less (p = 0.0272) than unparasitized shrimp. Mummichogs exhibited a preference for the more active shrimp (80.7% of shrimp; p<0.0001), and also for the less camouflaged (parasitized or marked) shrimp (81.5% of shrimp; p = 0.0011) if there was no difference in shrimp behavior. Parasitized shrimp were preferentially consumed (51/85 shrimp) when paired with unparasitized shrimp (p = 0.0089), but not with marked shrimp (p = 0.0837). A 30-min activity budget was created for each type of shrimp both in the presence and absence of predators; neither the parasite nor marking affected their behavior over 30 min (p = 0.1005). The major finding of this study was that P. pandalicola affected the predation preferences of F. heteroclitus by altering the behavior and/or camouflage of the grass shrimp. Parasitization alters predator-prey dynamics by decreasing the camouflage and the frequency of backward-thrusting behavior by the host when it is threatened by predation, which thereby decreases the ability of shrimp to escape from predators.
    No preview · Article · Dec 2015 · Crustaceana
    • "Physiological effects of the parasite include sexual sterilization (Beck, 1980; John, 2011; Sherman and Curran, 2015), increased caloric intake (Anderson, 1977), decreased oxygen consumption and metabolic rate (Anderson, 1975a), and decreased growth (Ludwig, 2009). It has also been reported that this parasite affects host behavior (Bass and Weis, 1999; Brinton, 2014). However, Chaplin-Ebanks and Curran (2005) reported no difference in activity level between parasitized and unparasitized shrimp. "
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    ABSTRACT: The bopyrid isopod Probopyrus pandalicola is a hematophagous ectoparasite that sexually sterilizes some palaemonid shrimps, including female daggerblade grass shrimp Palaemonetes pugio. The reproduction of parasitic isopods is thought to occur synchronously with host molting because the brood would be unsuccessful if molting occurred before the larvae were free swimming. Temperature affects the length of the molting cycle of shrimp, and therefore may also affect the incubation time of isopod broods. The purpose of the present study was to determine the effect of temperature on brood development of the parasite and on synchronization with the molting of its host. Parasitized P. pugio were monitored daily at 2 experimental temperatures, 23 C and 15 C, in temperature-controlled chambers for the duration of a full parasite reproductive cycle. Developmental stage was determined by the visible coloration of the brood through the exoskeleton of the host, and was designated as egg, embryo I, embryo II, or epicaridium larvae. Temperature significantly affected median brood incubation time, which was only 11 days at 23 C, as compared to 35 days at 15 C. The final developmental stage (epicaridium larvae) was 3 times shorter at 23 C (median 3 days; n=45) than at 15 C (median 9 days; n=15). Temperature significantly affected the intermolt period of parasitized shrimp, which was shorter at 23 C (median 12 days) than at 15 C (median 37 days). A smaller percentage of the intermolt period elapsed between larval release and shrimp molting at 23 C (0.0%) than at 15 C (3.1%), indicating closer synchronization between host molting and parasite reproduction at the warmer temperature. At 15 C the isopods utilized a smaller proportion of the time that was available for brood incubation during the intermolt period of their host. Brood size ranged from 391 to 4,596 young and was positively correlated with parasite and host size. Since development progressed more rapidly at 23 C, warmer temperatures could increase the prevalence of P. pandalicola. The corresponding reduction in the abundance of ovigerous grass shrimp as a result of sexual sterilization by bopyrids could adversely impact estuarine ecosystems, as grass shrimp are a crucial link in transferring energy from detritus to secondary consumers.
    No preview · Article · Aug 2015 · Journal of Parasitology
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    • "). This could indirectly influence mortality by changing the host's susceptibility to predation, if, for example, males are more likely to leave their burrows and/or fight to mate with females (Bass and Weis 1999). While Griffen (2009) hypothesizes that this could be an important factor in the O. griffenis–U. "

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