Does temperature affect synchronization between reproduction of the bopyrid isopod parasite Probopyrus pandalicola and molting of its grass shrimp host?
Abstract
The bopyrid isopod Probopyrus pandalicola is an ectoparasite that infects palaemonid shrimp, including the 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 and could search for copepod hosts. Temperature affects the length of the molting cycle for shrimp, and therefore may also affect the timing of isopod brood development. The purpose of the present study was to determine the duration of each developmental stage of parasite young as a function of temperature, and to determine fecundity of the parasite. Parasitized shrimp were monitored at 15°C and 23°C within environmental chambers. Brood incubation and shrimp intermolt period were significantly longer at 15°C (34.6 d and 33.1 d, respectively) than at 23°C (11.1 d and 12.1 d, respectively). Epicaridium larvae remained in the parasite marsupium for 3.2 times longer at 15°C (8.7 d) than at 23°C (2.7 d). After brood release, the marsupium remained empty for 15% (3.8 d) of the intermolt period at 15°C, compared to only 5% (0.6 d) at 23°C. This indicates less synchronization between host molting and larval release at 15°C than at 23°C. Brood size ranged from 391 to 4,596 young, and was positively correlated with both parasite and host size. Brood development progressed more rapidly at a higher temperature, suggesting that a potential effect of warming climate could be the increased prevalence of Probopyrus pandalicola and perhaps other arthropod parasites.
... Grass shrimp are easy to collect, handle, and maintain (Kunz et al., 2006) and have been used in many scientific studies (Welsh, 1975;Pung et al., 2002;Chaplin-Ebanks & Curran, 2007;Williamson et al., 2009;Partridge, 2010;Sherman & Curran, 2013, 2015Garcia et al., 2014;Brinton & Curran, 2015a). For example, Kunz et al. (2006) shrimp were observed to determine whether the behavior of the animal was altered by a parasite (Chaplin-Ebanks & Curran, 2005;Brinton, 2014;Brinton & Curran, 2015b), potentially increasing its susceptibility to predators (Brinton, 2014;Brinton & Curran, 2015b). Grass shrimp have also been used in K-12 activities to teach students about marine organisms and scientific research, because they are ideal organisms for young students to observe (Aultman & Curran, 2008;Aultman et al., 2010;Siler & Curran, 2011;Gunzburger & Curran, 2013;Gerido & Curran, 2014). ...
... Grass shrimp are easy to collect, handle, and maintain (Kunz et al., 2006) and have been used in many scientific studies (Welsh, 1975;Pung et al., 2002;Chaplin-Ebanks & Curran, 2007;Williamson et al., 2009;Partridge, 2010;Sherman & Curran, 2013, 2015Garcia et al., 2014;Brinton & Curran, 2015a). For example, Kunz et al. (2006) shrimp were observed to determine whether the behavior of the animal was altered by a parasite (Chaplin-Ebanks & Curran, 2005;Brinton, 2014;Brinton & Curran, 2015b), potentially increasing its susceptibility to predators (Brinton, 2014;Brinton & Curran, 2015b). Grass shrimp have also been used in K-12 activities to teach students about marine organisms and scientific research, because they are ideal organisms for young students to observe (Aultman & Curran, 2008;Aultman et al., 2010;Siler & Curran, 2011;Gunzburger & Curran, 2013;Gerido & Curran, 2014). ...
The process of exploration and the methods that scientists use to conduct research are fundamental to science education. In this activity, authentic scientific practices are used to develop hypotheses to explain the natural world. Students observe grass shrimp in aquaria and construct an ethogram, which is a compilation of the observable behaviors an animal exhibits. They then conduct an experiment, just as real scientists would, to determine how changes in the environment alter shrimp behavior. This activity is designed for a fourth-grade science class and allows students to experience the excitement of observing a live organism while learning about scientific inquiry, and also reinforces quantification and graphing skills. "Do You See What I See" covers Next Generation Science Standards and addresses the science and engineering practices of engaging in argument from evidence. © 2016 National Association of Biology Teachers. All rights reserved.
... 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. ...
... Brood size was estimated with the use of a method that was similar to Beck (1980). In brief, the number of young in a 25% subsample of the brood was counted under a microscope at 30-403 magnification (see Beck, 1980;Brinton, 2014). The accuracy of the modified method was validated by counting the entire brood for half of the selected specimens from each treatment, and the average error was only 62%. ...
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.
... Some authors found that bopyrid isopods also lower the activity level of their shrimp hosts (Bass and Weis, 1999;McGrew and Hultgren, 2011);however, Chaplin-Ebanks and Curran (2005) determined that the activity level of shrimp parasitized by bopyrids was not significantly different from that of unparasitized shrimp. Other effects of bopyrid infection include reduced antipredatory behaviors (Brinton, 2014), increased sensitivity to contaminants (Williamson et al., 2009;Partridge, 2010), and lower survival times during starvation at higher temperatures (Sherman, 2013;Sherman and Curran, 2013). Infection by bopyrid isopods can also result in reduced reproductive potential (Truesdale and Mermilliod, 1976;Van Wyk, 1982;Jarrin and Shanks, 2008;Herna´ez et al., 2010;John, 2011) and sexual sterilization of the definitive host (Morris, 1948;Anderson, 1977;Beck, 1980b;O'Brien and Van Wyk, 1985;Calado et al., 2005Calado et al., , 2008Dumbauld et al., 2011). ...
... Although the reported prevalence of Probopyrus pandalicola in Palaemonetes pugio is ,18% (Campos and Rosa de Campos, -Ebanks and Curran, 2007;Conner and Bauer, 2010), there is a potential for the prevalence of marine parasites to increase at higher temperatures (Chu and La Peyre, 1993;Mouritsen and Jensen, 1997;Cairns et al., 2005;Key et al., 2011). This is perhaps because of faster development rates of the parasites (Kutz et al., 2005;Paull and Johnson, 2011;Brinton, 2014). Key et al. (2011) found that the prevalence of Probopyrus pandalicola increased with temperature across creeks in coastal South Carolina over a 3-yr period; however, many other factors, such as salinity and percent marsh cover, also played a role. ...
Abstract Probopyrus pandalicola is a bopyrid isopod that infects several palaemonid shrimp species, including the daggerblade grass shrimp Palaemonetes pugio. The parasite can have several negative effects on its host, including loss of hemolymph, reduced reproductive potential, and decreased molting frequency and growth. To date, there are conflicting reports on whether Probopyrus pandalicola affects the reproductive capability of both male and female daggerblade grass shrimp. The purpose of this study was to determine whether infection by Probopyrus pandalicola resulted in the sexual sterilization of Palaemonetes pugio, and if the reproductive capability of male and/or female shrimp was restored after the bopyrid was removed. We found that parasitized and deparasitized males were able to successfully fertilize the eggs of unparasitized females, as 18.9±7.1% and 42.7±5.2% of the females paired with them became ovigerous in 4 wk, respectively. Neither parasitized nor deparasitized females became ovigerous when placed with unparasitized males during the 4-wk period. However, 45.4±20.6% of deparasitized females did become ovigerous within 10 wk. Despite the fact that female shrimp are able to reproduce when no longer parasitized, the majority of females remain infected with the bopyrid for their entire lives. Therefore, the sexual sterilization of female shrimp could potentially have a significant impact on estuarine food webs, as grass shrimp are conduits of detrital energy and a food source for many recreationally and commercially important species in estuaries on the East Coast of the U.S.A. and in the Gulf of Mexico.
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