ABSTRACT

Caridean shrimps are often infested by ectoparasites from the isopod family Bopyridae. Urobopyrus processae is a widespread species of bopyrid parasitizing the branchial (gill) chambers of members of the caridean family Processidae, including Ambidexter symmetricus. We examined hypotheses on differential infestation based on gender, castration of the host by the parasite, correlation between host and parasite size, and the fecundity of female parasites. Infestation rates varied from 1.3 to 32.1% between 2010 and 2011. Infested shrimps ranged from 1.26 mm to 6.24 mm carapace length (CL) between 2010 and 2011. Female shrimps were infested at a higher rate than males (2010 P = 0.0376; 2011 P = 0.0023). We report for the first time the differential selection between left and right branchial chambers in a caridean shrimp by a bopyrid parasite (P = 0.0209). Female parasite total length (TL) increased with host size (CL) in both years of sampling (2010 R² _adj = 0.6863; 2011 R² _adj= 0.8206). The size of male parasite TL was explained by both host CL (2010 R² _adj = 0.4591; 2011 R² _adj = 0.5490) and parasite female TL (2010 R² _adj = 0.5606; 2011 R² _adj = 0.6195). The number of embryos in a brood of the female parasite (85-3096) was varied positively with female TL (R² _adj = 0.625). Our results show that the bopyrid-shrimp host relationship in processids is typical of those studied in other carideans, indicating similar selective pressures act on bopyrids infesting the branchial chambers of shrimps.

Key words
Parasitic castration; Parasitism; Reproduction; St. Joseph Bay

Introduction

Decapod crustaceans are often infested by isopod parasites from the family Bopyridae. The majority of the members of this family are ectoparasites attaching within the branchial (gill) chamber or on the abdomens of their hosts (O'Brien and Van Wyk, 1985O'Brien, J. and Van Wyk, P. 1985. Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on growth of crustacean hosts. p. 191-218. In: A.M. Wenner (ed) Factors in adult growth. Crustacean Issues, Vol. 3. Rotterdam, A.A. Balkema.; Markham, 1986Markham, J.C. 1986. Evolution and zoogeography of the Isopoda Bopyridae, parasites of Crustacea Decapoda. p. 143-164. In: R.H. Gore and K.L. Heck (eds), Crustacean biogeography. Crustacean Issues, Vol. 4. Rotterdam, A.A. Balkema.). These parasites do not kill their hosts as a requirement for development but instead depend on them for nutrition and as their habitat (Anderson and May, 1978Anderson, R.M. and May, R.M. 1978. Regulation and stability of host-parasite population interactions I. Regulatory processes. Journal of Animal Ecology, 47(1): 219-247.). Most species are also usually parasitic castrators (Baudoin, 1975Baudoin, M. 1975. Host Castration as a Parasitic Strategy. Evolution, 29(2): 335-352.; Beck, 1979Beck, J.T. 1979. Population interactions between a parasitic castrator, Probopyrus pandalicola (Isopoda: Bopyridae), and one of its freshwater shrimp hosts, Palaemonetes paludosus (Decapoda: Caridea). Parasitology, 79(3): 431-449.; O'Brien and Van Wyk, 1985O'Brien, J. and Van Wyk, P. 1985. Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on growth of crustacean hosts. p. 191-218. In: A.M. Wenner (ed) Factors in adult growth. Crustacean Issues, Vol. 3. Rotterdam, A.A. Balkema.; Romero-Rodríguez and Román-Contreras, 2013Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650.), although this is not always the case (Calado et al., 2006Calado, R.; Vitorino, A. and Dinis, M.T. 2006. Bopyrid isopods do not castrate the simultaneously hermaphroditic shrimp Lysmata amboinensis (Decapoda: Hippolytidae). Diseases of Aquatic Organisms, 73(1): 73-76.). It has been shown that in some cases the host may recover its reproductive ability if it outlives the parasite (Kuris, 1974Kuris, A.M. 1974. Trophic interactions: similarity of parasitic castrators to parasitoids. The Quarterly Review of Biology, 49(2): 129-148.; Oliveira and Masunari, 1998Oliveira, E. and Masunari, S. 1998. Population relationships between the parasite Aporobopyrus curtatus (Richardson, 1904) (Isopoda: Bopyridae) and one of its porcelain crab hosts Petrolisthes armatus(Gibbes, 1850) (Decapoda: Porcellanidae) from Farol Island, southern Brazil. Journal of Natural History, 32(10-11): 1707-1717.). Thus, bopyrid parasites play an important part in the population biology and regulation of their definitive host species (Kuris, 1974Kuris, A.M. 1974. Trophic interactions: similarity of parasitic castrators to parasitoids. The Quarterly Review of Biology, 49(2): 129-148.; Beck, 1979Beck, J.T. 1979. Population interactions between a parasitic castrator, Probopyrus pandalicola (Isopoda: Bopyridae), and one of its freshwater shrimp hosts, Palaemonetes paludosus (Decapoda: Caridea). Parasitology, 79(3): 431-449.; Jay, 1989Jay, C.V. 1989. Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. American Midland Naturalist, 121(1): 68-77.). The relationships between populations of hosts and their parasites may follow classical predator-prey interactions (Anderson and May, 1978Anderson, R.M. and May, R.M. 1978. Regulation and stability of host-parasite population interactions I. Regulatory processes. Journal of Animal Ecology, 47(1): 219-247.; Romero-Rodríguez and Román-Contreras, 2013Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650.) and cause sex ratio distortion in their hosts (Hatcher et al., 1999Hatcher, M.J.; Taneyhill, D.E. and Dunn, A.M. 1999. Population dynamics under parasitic sex ratio distortion. Theoretical Population Biology, 56(1): 11-28.).

When bopyrids castrate their hosts, two changes in host biology tend to occur: female ovaries do not mature, and males become feminized (Baudoin, 1975Baudoin, M. 1975. Host Castration as a Parasitic Strategy. Evolution, 29(2): 335-352.; Beck, 1980cBeck, J.T. 1980c. The effects of an isopod castrator, Probopyrus pandalicola, on the sex characters of one of its caridean shrimp hosts, Palaemonetes paludosus. Biological Bulletin, 158(1): 1-15.; O'Brien and Van Wyk, 1985O'Brien, J. and Van Wyk, P. 1985. Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on growth of crustacean hosts. p. 191-218. In: A.M. Wenner (ed) Factors in adult growth. Crustacean Issues, Vol. 3. Rotterdam, A.A. Balkema.; Ayub and Ahmed, 2004Ayub, Z. and Ahmed, M. 2004. Study on the host-parasite relationship of Parapenaeopsis stylifera (H. Milne Edwards) (Decapoda: Penaeidae) and Parapenaeon japonica (Thielemann) (Isopoda: Bopyridae). Hydrobiologia, 523(1-3): 225-228.). Bopyrid parasites often infest young shrimps and grow with the hosts in marine and brackish ecosystems (Pike, 1960Pike, R.B. 1960. The biology and post larval development of the bopyrid parasites Pseudione affinis G. O. Sars and Hemiarthus abdominalis (Kröyer) (= Phryxus abdominalis (Kroyer)). Journal of the Linnean Society of London, Zoology, 44(297): 239-251.; Kuris, 1974Kuris, A.M. 1974. Trophic interactions: similarity of parasitic castrators to parasitoids. The Quarterly Review of Biology, 49(2): 129-148.; Owens, 1983Owens, L. 1983. Bopyrid parasite Epipenaeon ingensNobili as a biological marker for the banana prawn, Penaeus merguiensis de Man. Australian Journal of Marine and Freshwater Research, 34(3): 477-481.; Cash and Bauer, 1993Cash, C.E. and Bauer, R.T. 1993. Adaptations of the branchial ectoparasite Probopyrus pandalicola (Isopoda: Bopyridae) for survival and reproduction related to ecdysis of the host, Palaemonetes pugio (Caridea: Palaemonidae). Journal of Crustacean Biology, 13 (1): 111-124.; Roccatagliata and Lovrich, 1999Roccatagliata, D. and Lovrich, G.A. 1999. Infestation of the false king crab Paralomis granulosa (Decapoda: Lithodidae) by Pseudione tuberculata (Isopoda: Bopyridae) in the Beagle Channel, Argentina. Journal of Crustacean Biology, 19(4): 720-729.; Romero-Rodríguez and Román-Contreras, 2013Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650.). However, in rare cases, parasites may infest older and larger host shrimps, e.g., in amphidromous shrimps which may be infested during reproductive migrations to estuaries (Conner and Bauer, 2010Conner, S.L. and Bauer, R.T. 2010. Infection of adult migratory river shrimps, Macrobrachium ohione, by the branchial bopyrid isopod Probopyrus pandalicola. Invertebrate Biology, 129(4): 344-352.). Another possible side effect of a parasite on a host is gigantism. Not only do parasites often castrate their hosts, but they can also cause the host to grow larger than they would without the parasite (Baudoin, 1975Baudoin, M. 1975. Host Castration as a Parasitic Strategy. Evolution, 29(2): 335-352.). This process has been documented in the snail host Lymnaea Lamark, 1799 infested with the trematode parasite Echinostoma revolutum (Fröhlich, 1802) (Sorensen and Minchella, 1998Sorensen, R.E. and Minchell, D.J. 1998. Parasite influences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails. Oecologia, 115(12): 188-195.), as well as in the water flea host Daphnia Müller, 1785 infected with the bacterial parasite Pasteuria ramosa Metchnikoff, 1888 (Ebert et al., 2004Ebert, D.; Carius, H.J.; Little, T. and Decaestecker, E. 2004. The evolution of virulence when parasites cause host castration and gigantism. The American Naturalist, 164(S5): S19-S32.).

Bopyrid parasites also exhibit various patterns of infestation within decapod hosts. For example, the host sex with the larger body size tends to have a higher infestation rate in host species with sexual dimorphism in body size (Beck, 1979Beck, J.T. 1979. Population interactions between a parasitic castrator, Probopyrus pandalicola (Isopoda: Bopyridae), and one of its freshwater shrimp hosts, Palaemonetes paludosus (Decapoda: Caridea). Parasitology, 79(3): 431-449.; Jay, 1989Jay, C.V. 1989. Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. American Midland Naturalist, 121(1): 68-77.; Jordá and Roccatagliata, 2002Jordá, M.T. and Roccatagliata, D. 2002. Population dynamics of Leidya distorta (Isopoda: Bopyridae) infesting the fiddler crab Uca uruguayensis at the Río de la Plata estuary, Argentina. Journal of Crustacean Biology, 22(4): 719-727.). When there is no difference in size between male and female hosts, parasites tend to infest sexes equally (Beck, 1979Beck, J.T. 1979. Population interactions between a parasitic castrator, Probopyrus pandalicola (Isopoda: Bopyridae), and one of its freshwater shrimp hosts, Palaemonetes paludosus (Decapoda: Caridea). Parasitology, 79(3): 431-449.; Miranda and Mantelatto, 2010Miranda, I. and Mantelatto, F. 2010. Temporal dynamic of the relationship between the parasitic isopod Aporobopyrus curtatus(Crustacea: Isopoda: Bopyridae) and the anomuran crab Petrolisthes armatus (Crustacea: Decapoda: Porcellanidae) in southern Brazil. Latin American Journal of Aquatic Research, 38(2): 210-217.).

Urobopyrus processaeRichardson, 1904Richardson, H. 1904. Contributions to the Natural History of the Isopoda. Proceedings of the United States National Museum, 27(1350): 1-89. (Peracarida: Epicaridea: Bopyridae) is a parasitic isopod with a distribution including the Atlantic Ocean, Caribbean Sea, Gulf of Mexico, and Mediterranean Sea (Markham, 1986Markham, J.C. 1986. Evolution and zoogeography of the Isopoda Bopyridae, parasites of Crustacea Decapoda. p. 143-164. In: R.H. Gore and K.L. Heck (eds), Crustacean biogeography. Crustacean Issues, Vol. 4. Rotterdam, A.A. Balkema.). This parasite infests members of the family Processidae, including Processa fimbriata Manning and Chace, 1971, the shrimp from which Richardson (1904)Richardson, H. 1904. Contributions to the Natural History of the Isopoda. Proceedings of the United States National Museum, 27(1350): 1-89. described the parasite; Processa canaliculata Leach, 1815 (Bourdon, 1968Bourdon, R. 1968. Les Bopyridae des mers Européennes. Mémoires du Muséum National D'Histoire Naturelle de Paris, Nouvel Série A, Zoologie, 50(2): 75-424.); Processa edulis edulis (Risso, 1816) (Bourdon, 1968Bourdon, R. 1968. Les Bopyridae des mers Européennes. Mémoires du Muséum National D'Histoire Naturelle de Paris, Nouvel Série A, Zoologie, 50(2): 75-424.); Processa acutirostris Nouvel and Holthuis, 1957 (Bourdon, 1968Bourdon, R. 1968. Les Bopyridae des mers Européennes. Mémoires du Muséum National D'Histoire Naturelle de Paris, Nouvel Série A, Zoologie, 50(2): 75-424.); Processa robusta Nouvel and Holthuis, 1957 (Bourdon, 1968Bourdon, R. 1968. Les Bopyridae des mers Européennes. Mémoires du Muséum National D'Histoire Naturelle de Paris, Nouvel Série A, Zoologie, 50(2): 75-424.); and Ambidexter symmetricus Manning and Chace, 1971 (Markham, 1985Markham, J.C. 1985. A review of the bopyrid isopods infesting shrimps in the northwestern Atlantic Ocean, with special reference to those collected during the Hourglass Cruises in the Gulf of Mexico. Memoirs of the Hourglass Cruises, 7(3): 1-156.). Previous work by Bourdon (1968)Bourdon, R. 1968. Les Bopyridae des mers Européennes. Mémoires du Muséum National D'Histoire Naturelle de Paris, Nouvel Série A, Zoologie, 50(2): 75-424. suggested that European processids are infested at smaller size classes with the host and parasite growing together, and that infestation rates varied from May through November. Rasch and Bauer (in press) showed that infestation of A. symmetricus by U. processae causes gigantism in the host, which has been seen in other animal species infested by parasites (Ebert et al., 2004Ebert, D.; Carius, H.J.; Little, T. and Decaestecker, E. 2004. The evolution of virulence when parasites cause host castration and gigantism. The American Naturalist, 164(S5): S19-S32.; Hall et al., 2007Hall, S.R.; Becker, C. and Cáceres, C.E. 2007. Parasitic castration: a perspective from a model of dynamic energy budgets. Integrative and Comparative Biology, 47(2): 295-309.). A taxonomic re-examination of this parasite may be necessary given the wide distribution and the supposed breadth of infestation across members of the family Processidae.

In this study, we tested several hypotheses about parasite biology and its effects on the host: that infestation rate of this parasite varied through time in A. symmetricus; that infestation of A. symmetricus differs between the sexes; and that this parasite castrates its hosts (Kuris, 1974Kuris, A.M. 1974. Trophic interactions: similarity of parasitic castrators to parasitoids. The Quarterly Review of Biology, 49(2): 129-148.; O'Brien and Van Wyk, 1985O'Brien, J. and Van Wyk, P. 1985. Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on growth of crustacean hosts. p. 191-218. In: A.M. Wenner (ed) Factors in adult growth. Crustacean Issues, Vol. 3. Rotterdam, A.A. Balkema.; Ayub and Ahmed, 2004Ayub, Z. and Ahmed, M. 2004. Study on the host-parasite relationship of Parapenaeopsis stylifera (H. Milne Edwards) (Decapoda: Penaeidae) and Parapenaeon japonica (Thielemann) (Isopoda: Bopyridae). Hydrobiologia, 523(1-3): 225-228.). We predicted that parasites infest their shrimp hosts when both species are young, thereafter growing together with time (Kuris, 1974Kuris, A.M. 1974. Trophic interactions: similarity of parasitic castrators to parasitoids. The Quarterly Review of Biology, 49(2): 129-148.; Baudoin, 1975Baudoin, M. 1975. Host Castration as a Parasitic Strategy. Evolution, 29(2): 335-352.; O'Brien and Van Wyk, 1985O'Brien, J. and Van Wyk, P. 1985. Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on growth of crustacean hosts. p. 191-218. In: A.M. Wenner (ed) Factors in adult growth. Crustacean Issues, Vol. 3. Rotterdam, A.A. Balkema.; Hall et al., 2007Hall, S.R.; Becker, C. and Cáceres, C.E. 2007. Parasitic castration: a perspective from a model of dynamic energy budgets. Integrative and Comparative Biology, 47(2): 295-309.). We also describe parasite fecundity. This study is the first to examine the population biology of U. processae infesting any shrimp species. This study also allows further insight into how bopyrid parasites affect the growth and reproduction of caridean shrimps over their lifetimes.

Materials and Methods

Study Area and Sampling

A sampling site was established in the northeastern Gulf of Mexico in Eagle Harbor of St. Joseph Bay, Florida within T.H. Stone Memorial St. Joseph Peninsula State Park (29°46'3.94"N 85°24'12.22"W). Processid shrimps were collected in May-August 2010 and in April-October 2011, weather and low-tide permitting. Sampling focused on areas primarily covered by the seagrass Thalassia testudinum Banks ex König, 1805. The depth sampled at this site ranged from 0.5 to 1.3 m and samples were taken at night using a pushnet with a mouth size of 45 x 23 cm, with a 1 mm mesh (Bauer, 1985Bauer, R.T. 1985. Penaeoid shrimp fauna from tropical seagrass meadows: Species composition, diurnal, and seasonal variation in abundance. Proceedings of the Biological Society of Washington, 98(1): 177-190.). The pushnet was pushed over the bottom and through the seagrass for a haphazard distance, with material collected then sorted by hand using headlamps; this was repeated for up to three hours. Any processid shrimps were separated and maintained in a bucket of ambient seawater until later preservation in a solution of 10% seawater formalin (10% formaldehyde, 90% ambient seawater) and later washed with tapwater before transfer to 70% ethanol for permanent storage. Species name, carapace length, gender, ovigerous condition, and embryonic condition and presence of parasite(s) were recorded. Species were identified using keys from Manning and Chace (1971)Manning, R.B. and Chace Jr., F.A. 1971. Shrimps of the family Processidae from the northwestern Atlantic Ocean (Crustacea: Decapoda: Caridea). Smithsonian Contributions to Zoology, 89: 1-41. and Abele and Kim (1986)Abele, L.G. and Kim, W. 1986. An illustrated guide to the marine decapod crustaceans of Florida. State of Florida, Department of Environmental Regulation, 8, 1-760..

Measurements and Counts

Body size in shrimps was measured as carapace length (CL ± 0.01 mm), defined as the distance from the posterior edge of the orbit to the posterior lateral edge of the carapace and measured with an ocular micrometer. We examined the second pleopods for the presence (male) or absence (female) of an appendix masculina, the secondary male sexual character used to determine sex in carideans shrimps (Bauer, 2004Bauer, R.T. 2004. Remarkable shrimps: Adaptations and natural history of the carideans. Animal Natural History Series, Vol. 7. Norman, University of Oklahoma Press, 282p.). If an individual had damaged second pleopods, they were not included in the study. The degree of ovarian and embryonic condition of female shrimps was measured as in Bauer (1986Bauer, R.T. 1986. Sex change and life history pattern in the shrimp Thor manningi (Decapoda: Caridea): a novel case of partial protandric hermaphroditism. Biological Bulletin, 170(1): 11-31.; 1989Bauer, R.T. 1989. Continuous reproduction and episodic recruitment in nine shrimp species inhabiting a tropical seagrass meadow. Journal of Experimental Marine Biology and Ecology, 127(2): 175-187.; 1991)Bauer, R.T. 1991. Analysis of embryo production in a caridean shrimp guild from a tropical seagrass meadow. p. 181-192. In: A. Wenner & A. Kuris (eds), Crustacean Egg Production. Crustacean Issues, Vol. 7. Rotterdam, A.A. Balkema Press..

Shrimps were considered infested if an isopod bopyrid parasite was present within a branchial chamber (Fig. 1A). If one side of the carapace was deformed (bulged outward) but empty, it was assumed that the shrimp had been infested recently, and these shrimps were still used in analysis of overall infestation rate, gender of infested shrimps, and side of infestation (Jay, 1989Jay, C.V. 1989. Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. American Midland Naturalist, 121(1): 68-77.; Oliveira and Masunari, 1998Oliveira, E. and Masunari, S. 1998. Population relationships between the parasite Aporobopyrus curtatus (Richardson, 1904) (Isopoda: Bopyridae) and one of its porcelain crab hosts Petrolisthes armatus(Gibbes, 1850) (Decapoda: Porcellanidae) from Farol Island, southern Brazil. Journal of Natural History, 32(10-11): 1707-1717.; Miranda and Mantelatto, 2010Miranda, I. and Mantelatto, F. 2010. Temporal dynamic of the relationship between the parasitic isopod Aporobopyrus curtatus(Crustacea: Isopoda: Bopyridae) and the anomuran crab Petrolisthes armatus (Crustacea: Decapoda: Porcellanidae) in southern Brazil. Latin American Journal of Aquatic Research, 38(2): 210-217.). Some bopyrids were encountered loose in samples, presumably due to dislodgement during sampling and preservation; these were not used in any analyses since they could not be definitively matched to a host shrimp. All branchial parasites of the host shrimps were identified, using Markham (1985)Markham, J.C. 1985. A review of the bopyrid isopods infesting shrimps in the northwestern Atlantic Ocean, with special reference to those collected during the Hourglass Cruises in the Gulf of Mexico. Memoirs of the Hourglass Cruises, 7(3): 1-156., as Urobopyrus processae (Fig. 1B-E). The total length (TL ± 0.01 mm) of parasites found within branchial chambers was measured using a stereomicroscope with ocular micrometer, from the anterior edge of the cephalon to the posterior edge of the pleotelson in males (Fig. 1E) and in juvenile females (Fig. 1C), both of which are symmetrical in shape. However, female parasites are asymmetrical in shape (Fig. 1B, D) and were measured along the longest line from the anterior end to the end of the pleotelson (Cash and Bauer, 1993Cash, C.E. and Bauer, R.T. 1993. Adaptations of the branchial ectoparasite Probopyrus pandalicola (Isopoda: Bopyridae) for survival and reproduction related to ecdysis of the host, Palaemonetes pugio (Caridea: Palaemonidae). Journal of Crustacean Biology, 13 (1): 111-124.; Conner and Bauer, 2010Conner, S.L. and Bauer, R.T. 2010. Infection of adult migratory river shrimps, Macrobrachium ohione, by the branchial bopyrid isopod Probopyrus pandalicola. Invertebrate Biology, 129(4): 344-352.). Development of embryos within the marsupium was divided into four successive stages: stage I, which is spherical in shape, whitish; stage II, which is oblong in shape and yellowish; stage III, which is oblong in shape and yellowish in color with brown pigments; and epicaridium larva, with external appendages and visible eyespots (Beck, 1980aBeck, J.T. 1980a. Life history relationships between the bopyrid isopod Probopyrus pandalicola and one of its freshwater shrimp hosts Palaemonetes paludosus. American Midland Naturalist, 104(1): 135-154.; Romero-Rodríguez and Román-Contreras, 2013Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650.).

Data Analysis

A goodness of fit chi-square test was used to determine if there was an infestation preference by the parasites for female or male host shrimps as well as for infestation of the host's left or right branchial chamber. A full-cross ANOVA was used to address the question or whether parasite size was affected by month of sampling and/or sex of parasite. We used a Tukey-Kramer posthoc to determine interactions between Least Square Means (SAS Institute Inc. 2013SAS Institute Inc. 2013. SAS Enterprise Guide 6.1 for SAS OnDemand, Cary, NC: SAS Institute Inc.). A linear regression compared female parasite TL with CL of the host shrimp, as female parasite length may be constrained by host size. We also used a linear regression to compare male parasite TL with both female parasite TL as well as, for completeness, the host shrimp CL. We used an analysis of covariance to test the hypothesis of no difference between the slopes of the regressions, using year and parasite gender as covariates (SAS Institute Inc. 2013SAS Institute Inc. 2013. SAS Enterprise Guide 6.1 for SAS OnDemand, Cary, NC: SAS Institute Inc.). If there was only one parasite in a branchial chamber, it was considered female for analysis even if it was still in the cryptoniscus stage, as the first parasite larva that infests the branchial chamber becomes female (Reinhard, 1949Reinhard, E.G. 1949. Experiments on the determination and differentiation of sex in the bopyrid Stegophryxus hyptius Thompson. Biological Bulletin, 96(1): 17-31.).

If a cryptoniscus was found in the branchial chamber with a female parasite, it was considered a male (Reinhard, 1949Reinhard, E.G. 1949. Experiments on the determination and differentiation of sex in the bopyrid Stegophryxus hyptius Thompson. Biological Bulletin, 96(1): 17-31.). If there was a cryptoniscus larva on opposite sides of the branchial chamber (N = 3), these parasites were not included in any analysis as it could not be determined which was the first infester. In shrimps with three or more parasites, only paired individuals (male and female or cryptoniscus and female) were used in the various analyses (N = 5).

The variation in brood size (number of embryos) with female parasite size (TL) was examined using linear regression (SAS Institute Inc., 2013SAS Institute Inc. 2013. SAS Enterprise Guide 6.1 for SAS OnDemand, Cary, NC: SAS Institute Inc.). We also analyzed the variation of embryo size (volume) with developmental stage. The greater (d₂) and lesser (d₁) diameters of 10 embryos chosen haphazardly from each brood were measured. The mean volume of embryos brooded by female parasites were calculated using the formula v = (π*(d₁)2*d₂)/6 (Turner and Lawrence, 1979Turner, R.L. and Lawrence, J.M. 1979. Volume and composition of echinoderm eggs: implications for use of egg size in life-history models. p. 25-40. In: S.E. Stancky (ed), Reproductive Ecology of Marine Invertebrates. Columbia, University of South Carolina Press.; Romero-Rodríguez and Román-Contreras, 2013Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650.).

The size at sexual maturity of female parasites is an important reproductive parameter of populations. To estimate this parameter, we first plotted the relative proportion of female parasites in 0.3 mm size classes. The logistic function y =1/(1+e^-r(TL-TL50)) was then fitted to the data, where TL_50%corresponds to the size at which 50% of the individuals are considered sexually mature and r stands for the slope of the curve (King, 1995King, M. 1995. Fisheries Biology, Assessment and Management. Fishing News Books. Oxford, Blackwell Science Ltd., 352p.). We only included first infester parasites that had begun to show female differentiation for this analysis. We used maximum likelihood estimates for fitting (R Core Team, 2014R Core Team. 2014. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org
http://www.R-project.org... ). We used a Wilcoxon-Mann-Whitney test to determine if the distributions were different between years (SAS Institute Inc., 2013SAS Institute Inc. 2013. SAS Enterprise Guide 6.1 for SAS OnDemand, Cary, NC: SAS Institute Inc.). We followed this test with a boot-strap analysis to test for differences in the shape of the distributions between 2010 and 2011. To do this we pooled data for all years and drew 1000 random samples. For each sample we drew 69 samples to represent 2010 and 53 samples to represent the 2011 data. In our analysis the shape of the distributions is summarized by the model parameters r and TL_50%. To perform this analysis we considered a modified version of the model:

where year is coded as either 0 for 2010 or 1 for 2011. In our expanded model ∆r gives the change in r for the 2011 individuals relative to the 2010 individuals. Our expanded model also has ∆T giving the change in TL_50% for the 2011 individuals relative to the 2010 individuals. For each of the 1000 replicates we recorded ∆r and ∆T to establish the distributions for these parameters under the null hypothesis of no differences between the 2010 and 2011 populations. We then compared the values for ∆r and ∆T computed from the observed data to the distributions. To compare the observed ∆r to its distribution we found the number of replicates that had a value equal to or more extreme that the observed ∆r and divided this by the total number of replicates. This value can be interpreted as a p-value in this analysis. This process was repeated for ∆T. To determine if host CL of sexually mature female parasites was different between years, we used a two-sample t-test comparing host CL for 2010 and 2011 (SAS Institute Inc., 2013SAS Institute Inc. 2013. SAS Enterprise Guide 6.1 for SAS OnDemand, Cary, NC: SAS Institute Inc.).

Results

We collected a total of 1309 Ambidexter symmetricus in 2010 and 1177 in 2011, which was the only processid shrimp species collected infested with Urobopyrus processae. Monthly infestation rates in 2010 varied from 2.1% to 17.8% with a mean infestation rate of 8.6%, while in 2011 infestation rates varied from 1.3% to 32.1% with a mean of 8.2%, not including the July data (n = 2, infestation rate = 50%) because of its small sample size (Fig. 2). Shrimps ranged in size (CL) from 0.79 mm to 6.50 mm. The size range of infested shrimps was from 1.56 mm to 6.24 mm CL in 2010, and 1.26 mm to 5.88 mm CL in 2011 (Fig. 3). Parasite size (TL) ranged from 0.72 mm to 3.60 mm in 2010, and 0.83 mm to 3.90 mm in 2011. Female parasite size (TL) was larger earlier in the year (April, May) but declined later in the year, while male parasites were consistent in TL across samples (Tabs. 1 and 2).

There were only 3 shrimps collected during the two years that had a cryptoniscus larva on both sides of the branchial chamber; these were not used in analyses. There were five shrimps collected with more than two parasites. All shrimps with three or four parasites were female, and collected between June 14th and June 17th in 2010 or 2011. No shrimp had more than four parasites in their branchial chamber. In these multiple infestations, only one female bopyrid was present, accompanied by a male, with the second infestation being either a cryptoniscus larva, a pair of cryptoniscus larvae, or in one case another male bopyrid (supernumerary male) all found in the opposite branchial chamber from the female-male pair.

Parasite infestation differed between male and female shrimps. In 2010, more female shrimps (N = 67) were infested with U. processae than males (N = 45) (χ² ₁ = 4.32, P = 0.0376). In the 2011 samples, 64 females and 33 males were infested (χ² ₁ = 9.28, P = 0.0023). Infestation also differed between right and left branchial chambers. In 2010 and 2011, there were 112 shrimps infested on the right branchial chamber, and 80 infested on the left branchial chamber (χ² ₁ = 5.33, P = 0.0209). Out of 131 parasitized female shrimps, only four were brooding embryos, including one which showed a developing ovary, indicating a possible future spawn. In all four cases, the parasites were cryptoniscus larvae, indicating a recent infestation.

The variation in female and male parasite TL was significantly explained by host CL in both 2010 and 2011 (Fig. 4). There was no combined effect of year*parasite gender*host CL on parasite TL, but there was an effect of parasite gender*host CL and an effect of host CL*year on parasite TL (Fig. 4). However, the variation in male parasite TL was better explained by female parasite TL in both years (Fig. 5). There was no interaction between female TL*year or effect of year on male TL (Fig. 5).

Brood size of the parasites ranged from 85 to 3096 embryos, and the volume of an embryo ranged from 0.00145-0.00238 mm³ depending on embryo stage (Tab. 3). Within a brood the size and developmental stage of the eggs did not vary. There was variation among broods between similarly sized female parasites when broken down into 0.5 mm size classes (Tab. 4); however there was a positive relationship present between number of parasite embryos brooded and female parasite TL (Fig. 6).

Female parasites differed in the size of sexual maturity between 2010 and 2011. The TL_50% was 1.09 mm in 2010 and 1.63 mm in 2011 (Fig. 7), and these differences were statistically significant. We found the value for ∆r and ∆T for the observed data were -0.937 and 0.565, respectively. When we compared the observed value for ∆r to its distribution we found that only a 1.8% of the replicates where equal to or more extreme that observing ∆r value. This value indicates that the observed ∆r was significantly different that zero at the P = 0.018 level. When we compared the observed value for ∆T to its distribution we found that only a < 0.001% of the replicates where equal to or more extreme that observing ∆T value. This value indicates that the observed ∆T was significantly different that zero at the P < 0.0001 level. We found that the mean host length for shrimps (CL ± SD in mm) infested by female parasites was 3.017 mm ± 1.030 in 2010 and 3.471 mm ± 0.966 in 2011. There was a significant difference between these host CLs between years (T = -2.47, P = 0.0151, df = 119).

Discussion

Our results showed that the incidence of infestation by the bopyrid Urobopyrus processae of the processid shrimp Ambidexter symmetricuswas higher than that found previously in other processid shrimps. Bourdon (1968)Bourdon, R. 1968. Les Bopyridae des mers Européennes. Mémoires du Muséum National D'Histoire Naturelle de Paris, Nouvel Série A, Zoologie, 50(2): 75-424. reported an overall infestation rate of 6.4% in Processa edulis edulis, ranging from a low of 5.3% in October/November and a high of 8.9% in August; however more detailed data on monthly infestations were not provided. The percentage of A. symmetricusinfested overall in both 2010 (8.6%) and 2011 (8.2%), ranging from a low of 1.4% in October of 2011, to a high of 32.1% in June of 2011. Bourdon (1968)Bourdon, R. 1968. Les Bopyridae des mers Européennes. Mémoires du Muséum National D'Histoire Naturelle de Paris, Nouvel Série A, Zoologie, 50(2): 75-424. did not report gender of hosts infested by U. processae for us to compare our data. However, a higher infestation rate of females is consistent with other bopyrid parasites known to infest sexually dimorphic carideans in which females are the larger sex (Romero-Rodríguez and Román-Contreras, 2013Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650.). Noël (1976)Noël, P. 1976. L'évolution des caractères sexuals chez Processa edulis (Risso) (Décapode, Natantia). Vie et Milieu, 26: 65-104. found a much lower incidence of infestation of processids by U. processae in his study, with only ~0.1% of P. edulis edulis infested overall, 4% of Processa robusta Nouvel and Holthuis, 1957, and 2.8% of Processa acutirostris. There is considerable variation in the infestation rates of U. processae within and across host processids, and the factors causing this variation should be a point of further study.

Bourdon (1968)Bourdon, R. 1968. Les Bopyridae des mers Européennes. Mémoires du Muséum National D'Histoire Naturelle de Paris, Nouvel Série A, Zoologie, 50(2): 75-424. found three individual shrimps which were infested with three or more parasites, similar to our study, and he suggested that Processa spp. may be unable to survive multiple infestations. However, it has been suggested that the first-established female parasite may inhibit the ability of other females to develop, this preventing bilateral infestations most of the time (Reinhard, 1949Reinhard, E.G. 1949. Experiments on the determination and differentiation of sex in the bopyrid Stegophryxus hyptius Thompson. Biological Bulletin, 96(1): 17-31.; Beck, 1979Beck, J.T. 1979. Population interactions between a parasitic castrator, Probopyrus pandalicola (Isopoda: Bopyridae), and one of its freshwater shrimp hosts, Palaemonetes paludosus (Decapoda: Caridea). Parasitology, 79(3): 431-449.; Jay, 1989Jay, C.V. 1989. Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. American Midland Naturalist, 121(1): 68-77.). Previous experiments also showed that when an immature female bopyrid is added to a host with an established adult female parasite, it later leaves (Reinhard, 1949Reinhard, E.G. 1949. Experiments on the determination and differentiation of sex in the bopyrid Stegophryxus hyptius Thompson. Biological Bulletin, 96(1): 17-31.). This would account for the small number of multiple infestations found in our study (five), and that multiple infestations never have more than one female bopyrid and usually involve cryptoniscus larvae. This is consistent with other studies reporting multiple infestations in caridean shrimps (Jay, 1989Jay, C.V. 1989. Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. American Midland Naturalist, 121(1): 68-77.; Romero-Rodríguez and Román-Contreras, 2013Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650.). In our samples only one supernumerary male was present (in the opposite branchial chamber), and it was larger than the male paired with the female bopyrid as seen previously in Probopyrus pandalicola (Packard, 1879) infesting Palaemonetes paludosus (Gibbes, 1850) (Beck, 1980bBeck, J.T. 1980b. Larval and adult habitats of a branchial bopyrid Probopyrus pandalicola on one of its freshwater shrimp hosts Palaemonetes paludosus. Crustaceana, 38(3): 265-270.).

Previous studies show branchial bopyrids generally occur equally in both the left and right gill chambers of their definitive hosts (Jay, 1989Jay, C.V. 1989. Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. American Midland Naturalist, 121(1): 68-77.; Miranda and Mantelatto, 2010Miranda, I. and Mantelatto, F. 2010. Temporal dynamic of the relationship between the parasitic isopod Aporobopyrus curtatus(Crustacea: Isopoda: Bopyridae) and the anomuran crab Petrolisthes armatus (Crustacea: Decapoda: Porcellanidae) in southern Brazil. Latin American Journal of Aquatic Research, 38(2): 210-217.). Bourdon (1968)Bourdon, R. 1968. Les Bopyridae des mers Européennes. Mémoires du Muséum National D'Histoire Naturelle de Paris, Nouvel Série A, Zoologie, 50(2): 75-424. did report the percentage of left (48.4%) and right side (51.6%) infestations, but analysis was not conducted to determine if there was a statistical difference. Some bopyrids are known to show preferential branchial chamber side infestation in non-natantian decapod crustaceans. These differential infestations all have all been by members of the bopyrid subfamily Pseudioninae and the hosts are hermit crabs in Diogenidae and Paguridae (Markham, 1986Markham, J.C. 1986. Evolution and zoogeography of the Isopoda Bopyridae, parasites of Crustacea Decapoda. p. 143-164. In: R.H. Gore and K.L. Heck (eds), Crustacean biogeography. Crustacean Issues, Vol. 4. Rotterdam, A.A. Balkema.) and in the false king crab Paralomis granulosa (Hombron & Jacquinot, 1846) which is a member of Lithodidae (Roccatagliata and Lovrich, 1999Roccatagliata, D. and Lovrich, G.A. 1999. Infestation of the false king crab Paralomis granulosa (Decapoda: Lithodidae) by Pseudione tuberculata (Isopoda: Bopyridae) in the Beagle Channel, Argentina. Journal of Crustacean Biology, 19(4): 720-729.). These three families belong to the infraorder Anomura and all are characterized by some degree of body asymmetry. Processid shrimps show some asymmetry of thoracic appendages in the six currently described genera. In five genera, only the right first pereopod is chelate, and in some species, the left second pereopod (cheliped) is longer than right (Manning and Chace, 1971Manning, R.B. and Chace Jr., F.A. 1971. Shrimps of the family Processidae from the northwestern Atlantic Ocean (Crustacea: Decapoda: Caridea). Smithsonian Contributions to Zoology, 89: 1-41.; Hayashi, 1975Hayashi, K. 1975. The Indo-West Pacific Processidae (Crustacea, Decapoda, Caridea). The Journal of the Shimoneseki University of Fisheries, 24(1): 47-145.). The possible differential selection of a branchial chamber by U. processae infesting A. symmetricus is the first such case in a caridean shrimp, and the first by a non-Pseudioninae bopyrid in any decapod (UrobopyrusRichardson, 1904 is in subfamily Bopyrinae).

Urobopyrus processae appears to castrate most female A. symmetricus that they infest. Of the 131 female shrimps with parasites, only 3 carried embryos, and only one showed ovarian development. Given the small size and early developmental stage of the parasites on these latter four shrimps, it is likely they were new infestations and did not have enough time yet to influence the reproductive capabilities of these host females. The ovary probably would have degenerated as the young parasite transitioned into a reproductive female (Baudoin, 1975Baudoin, M. 1975. Host Castration as a Parasitic Strategy. Evolution, 29(2): 335-352.; Beck, 1980cBeck, J.T. 1980c. The effects of an isopod castrator, Probopyrus pandalicola, on the sex characters of one of its caridean shrimp hosts, Palaemonetes paludosus. Biological Bulletin, 158(1): 1-15.; Masunari et al., 2000Masunari, S.; Castagini, A.S. and Oliveira, E. 2000. The population structure of Probopyrus floridensis (Isopoda, Bopyridae), a parasite of Macrobrachium potiuna (Decapoda, Palaemonidae) from the Perequê River, Paranaguá Basin, Southern Brazil. Crustaceana, 73(9): 1095-1108.). The castration of decapod hosts by bopyrids is a well known phenomenon (Baudoin, 1975Baudoin, M. 1975. Host Castration as a Parasitic Strategy. Evolution, 29(2): 335-352.; Beck, 1979Beck, J.T. 1979. Population interactions between a parasitic castrator, Probopyrus pandalicola (Isopoda: Bopyridae), and one of its freshwater shrimp hosts, Palaemonetes paludosus (Decapoda: Caridea). Parasitology, 79(3): 431-449.; O'Brien and Van Wyk, 1985O'Brien, J. and Van Wyk, P. 1985. Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on growth of crustacean hosts. p. 191-218. In: A.M. Wenner (ed) Factors in adult growth. Crustacean Issues, Vol. 3. Rotterdam, A.A. Balkema.; Oliveira and Masunari, 1998Oliveira, E. and Masunari, S. 1998. Population relationships between the parasite Aporobopyrus curtatus (Richardson, 1904) (Isopoda: Bopyridae) and one of its porcelain crab hosts Petrolisthes armatus(Gibbes, 1850) (Decapoda: Porcellanidae) from Farol Island, southern Brazil. Journal of Natural History, 32(10-11): 1707-1717.; Masunari et al., 2000Masunari, S.; Castagini, A.S. and Oliveira, E. 2000. The population structure of Probopyrus floridensis (Isopoda, Bopyridae), a parasite of Macrobrachium potiuna (Decapoda, Palaemonidae) from the Perequê River, Paranaguá Basin, Southern Brazil. Crustaceana, 73(9): 1095-1108.; Romero-Rodríguez and Román-Contreras, 2013Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650.). The most likely explanation is that the energy resources needed for host reproduction are taken up by the bopyrid female to produce its own broods of embryos. Additionally, the bopyrid may disrupt the host endocrine system affecting reproduction (Calado et al., 2005Calado R.; Bartilotti, C. and Narciso, L. 2005. Short report on the effect of a parasitic isopod on the reproductive performance of a shrimp. Journal of Experimental Marine Biology and Ecology, 321: 13-18.). Males of A. symmetricus and other carideans might also be castrated by bopyrids, but Calado et al.(2005)Calado R.; Bartilotti, C. and Narciso, L. 2005. Short report on the effect of a parasitic isopod on the reproductive performance of a shrimp. Journal of Experimental Marine Biology and Ecology, 321: 13-18. found that parasitized individuals of the shrimp Lysmata seticaudata (Risso, 1816) in the simultaneous hermaphrodite stage could mate and inseminate as males although they were unable to produce embryos. Thus, the lower energetic needs of sperm production may allow males to mate and inseminate normally, a hypothesis which needs to be tested with bopyridized male carideans.

We found that female parasites are smaller in size as the year progresses, which is consistent with other data (Rasch and Bauer, in press) showing that the host shrimps are larger in size in the population sampled earlier in the year (April/May), and smaller in size later in the summer (July, August, September). This change in the host population most likely is due to recruitment of shrimp postlarvae and death of larger older individuals during the summer. Female parasite TL increases with host size, and thus smaller newly recruited hosts as the summer progresses would result in smaller female parasites more recently infesting the younger, smaller shrimps. Male parasites appear to be limited in TL because they are constrained by the size of the female parasite, as males fit into a space on the female pleotelson. As noted, female parasite size is constrained by host size (the size of the branchial chamber, which the female fills). Positive correlation of female parasite TL is commonly reported in bopyrid parasite-host relationships, suggesting that the host is infested when very young, and the host and parasite then grow together (Roccatagliata and Lovrich, 1999Roccatagliata, D. and Lovrich, G.A. 1999. Infestation of the false king crab Paralomis granulosa (Decapoda: Lithodidae) by Pseudione tuberculata (Isopoda: Bopyridae) in the Beagle Channel, Argentina. Journal of Crustacean Biology, 19(4): 720-729.; Romero-Rodríguez and Román-Contreras, 2013Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650.). Anderson (1990)Anderson, G. 1990. Postinfection mortality of Palaemonetes spp. (Decapoda: Palaemonidae) following experimental exposure to the bopyrid isopod Probopyrus pandalicola (Packard) (Isopoda: Epicaridea). Journal of Crustacean Biology, 10(2): 284-292. showed experimentally that infestation of the shrimp Palaemonetes pugioHolthuis, 1949 by Probopyrus pandalicola occurs mainly in the shrimp's zoeal or young postlarval stages. Our data show that growth of the female bopyrid is strongly linked to host size; however some temporal variation also existed and needs to be further examined. Male parasites begin association with the female parasite soon after the latter becomes established in the host branchial chamber, consistent with male bopyrids of other species, and the two grow together to maturity (Beck, 1980aBeck, J.T. 1980a. Life history relationships between the bopyrid isopod Probopyrus pandalicola and one of its freshwater shrimp hosts Palaemonetes paludosus. American Midland Naturalist, 104(1): 135-154.; Jay, 1989Jay, C.V. 1989. Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. American Midland Naturalist, 121(1): 68-77.; Cash and Bauer, 1993Cash, C.E. and Bauer, R.T. 1993. Adaptations of the branchial ectoparasite Probopyrus pandalicola (Isopoda: Bopyridae) for survival and reproduction related to ecdysis of the host, Palaemonetes pugio (Caridea: Palaemonidae). Journal of Crustacean Biology, 13 (1): 111-124.).

The size of broods incubated by female U. processae is positively correlated with female parasite size (TL) (Beck, 1980aBeck, J.T. 1980a. Life history relationships between the bopyrid isopod Probopyrus pandalicola and one of its freshwater shrimp hosts Palaemonetes paludosus. American Midland Naturalist, 104(1): 135-154.; Romero-Rodríguez and Román-Contreras, 2008Romero-Rodríguez, J. and Román-Contreras, R. 2008. Aspects of the reproduction of Bopyrinella thorii (Richardson, 1904) (Isopoda, Bopyridae), a branchial parasite of Thor floridanus Kingsley, 1878 (Decapoda, Hippolytidae) in Bahía de la Ascensión, Mexican Caribbean. Crustaceana, 81(10): 1201-1210.; 2013Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650.). Thus, larger hosts which suffer gigantism (Rasch and Bauer, in press) would have larger parasites within their branchial chambers, and these larger female parasites would be able to produce larger broods. The slight variation in brood size among similarly sized female parasites, but high variation among differently sized female parasites is consistent with observations in broods of other bopyrids parasitizing caridean shrimps, such as Probopyrus pandalicola infesting Palaemonetes paludosus (Beck, 1980bBeck, J.T. 1980b. Larval and adult habitats of a branchial bopyrid Probopyrus pandalicola on one of its freshwater shrimp hosts Palaemonetes paludosus. Crustaceana, 38(3): 265-270.), Bopyrinella thorii(Richardson, 1904Richardson, H. 1904. Contributions to the Natural History of the Isopoda. Proceedings of the United States National Museum, 27(1350): 1-89.) on Thor floridanus Kingsley, 1878 (Romero-Rodríguez and Román-Contreras, 2008Romero-Rodríguez, J. and Román-Contreras, R. 2008. Aspects of the reproduction of Bopyrinella thorii (Richardson, 1904) (Isopoda, Bopyridae), a branchial parasite of Thor floridanus Kingsley, 1878 (Decapoda, Hippolytidae) in Bahía de la Ascensión, Mexican Caribbean. Crustaceana, 81(10): 1201-1210.), Bopyrina abbreviata Richardson, 1904Richardson, H. 1904. Contributions to the Natural History of the Isopoda. Proceedings of the United States National Museum, 27(1350): 1-89. on Hippolyte zostericola (Smith, 1873) (Romero-Rodríguez and Román-Contreras, 2013Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650.), and Argeia pugettensis Dana, 1853 on Crangon francisorum francisorum Stimpson, 1856 (Jay, 1989Jay, C.V. 1989. Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. American Midland Naturalist, 121(1): 68-77.).

The higher incidence of infestation reported here in female A. symmetricus is consistent with that reported in other bopyrid parasites infesting caridean shrimps where females are the larger host (Beck, 1979Beck, J.T. 1979. Population interactions between a parasitic castrator, Probopyrus pandalicola (Isopoda: Bopyridae), and one of its freshwater shrimp hosts, Palaemonetes paludosus (Decapoda: Caridea). Parasitology, 79(3): 431-449.; Jay, 1989Jay, C.V. 1989. Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. American Midland Naturalist, 121(1): 68-77.). This parasite adaptation enables parasite females to produce larger broods and maximize fecundity, as the female parasite is limited by host size, and brood size is also limited by host size as mentioned above (Beck, 1979Beck, J.T. 1979. Population interactions between a parasitic castrator, Probopyrus pandalicola (Isopoda: Bopyridae), and one of its freshwater shrimp hosts, Palaemonetes paludosus (Decapoda: Caridea). Parasitology, 79(3): 431-449.; Jay, 1989Jay, C.V. 1989. Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. American Midland Naturalist, 121(1): 68-77.; Miranda and Mantelatto, 2010Miranda, I. and Mantelatto, F. 2010. Temporal dynamic of the relationship between the parasitic isopod Aporobopyrus curtatus(Crustacea: Isopoda: Bopyridae) and the anomuran crab Petrolisthes armatus (Crustacea: Decapoda: Porcellanidae) in southern Brazil. Latin American Journal of Aquatic Research, 38(2): 210-217.). The range of brood size and embryo size seen in U. processae is consistent with the values reported for a variety of bopyrid parasites infesting caridean shrimps as reported by Romero-Rodríguez and Román-Contreras (2013)Romero-Rodríguez, J. and Román-Contreras, R. 2013. Prevalence and reproduction of Bopyrina abbreviata (Isopoda, Bopyridae) in Laguna de Términos, SW Gulf of Mexico. Journal of Crustacean Biology, 33(5): 641-650..

The size at sexual maturity, L_50% (in this study parasite TL_50%), is an important population parameter for comparing reproductive maturity within and across taxa (King, 1995King, M. 1995. Fisheries Biology, Assessment and Management. Fishing News Books. Oxford, Blackwell Science Ltd., 352p.) that may vary among and between populations (Pardo et al., 2009Pardo, L.M.; Fuentes, J.P.; Olguín, A. and Orensanz, J.M. 2009. Reproductive maturity in the edible Chilean crab Cancer edwarsii: methodological and management considerations. Journal of the Marine Biological Association of the United Kingdom, 89(8): 1627-1634.). The TL_50% for U. processae indicated that approximately 50% of female parasites reached sexual maturity between 1.10-1.63 mm TL, with a significant difference between years for both the slope and the y-intercept of the lines. This suggests that some abiotic or biotic factors may be influencing sexual development in this parasite from year to year and warrants further study. One factor may be host CL. Our data showed that shrimps with female parasites in 2011 were larger than those in 2010, and this could influence sexual maturity in the parasites.

Urobopyrus processae is known to occur in several Processa species (Bourdon, 1968Bourdon, R. 1968. Les Bopyridae des mers Européennes. Mémoires du Muséum National D'Histoire Naturelle de Paris, Nouvel Série A, Zoologie, 50(2): 75-424.; Markham, 1985Markham, J.C. 1985. A review of the bopyrid isopods infesting shrimps in the northwestern Atlantic Ocean, with special reference to those collected during the Hourglass Cruises in the Gulf of Mexico. Memoirs of the Hourglass Cruises, 7(3): 1-156.; 1986Markham, J.C. 1986. Evolution and zoogeography of the Isopoda Bopyridae, parasites of Crustacea Decapoda. p. 143-164. In: R.H. Gore and K.L. Heck (eds), Crustacean biogeography. Crustacean Issues, Vol. 4. Rotterdam, A.A. Balkema.), but only infested A. symmetricus we collected, and not any other member of the family Processidae that were taken in the same collections [Processa bermudensis (Rankin, 1900), Processa hemphilli Manning and Chace, 1971Manning, R.B. and Chace Jr., F.A. 1971. Shrimps of the family Processidae from the northwestern Atlantic Ocean (Crustacea: Decapoda: Caridea). Smithsonian Contributions to Zoology, 89: 1-41., Processa riveroi Manning and Chace, 1971Manning, R.B. and Chace Jr., F.A. 1971. Shrimps of the family Processidae from the northwestern Atlantic Ocean (Crustacea: Decapoda: Caridea). Smithsonian Contributions to Zoology, 89: 1-41.]. This speciesspecific host infestation could suggest this parasite may be a different species, or subspecies. Very little is known about parasitic development during the infestation of the host, since most of the focus is on the fully developed adult parasite morphology (Anderson, 1990Anderson, G. 1990. Postinfection mortality of Palaemonetes spp. (Decapoda: Palaemonidae) following experimental exposure to the bopyrid isopod Probopyrus pandalicola (Packard) (Isopoda: Epicaridea). Journal of Crustacean Biology, 10(2): 284-292.). Parasites and hosts coevolve with each other, so that understanding the biology of the parasite is critical to understanding the ecology of the host and vice versa. The relationship between U. processae and its host A. symmetricus warrants further investigation to determine if the patterns reported from our data are consistent among different locations and other processid host species.

Acknowledgements

We thank the Florida Fish and Wildlife Conservation Committee and the Florida Department of Environmental Protection for allowing us to collect samples in T.H. Stone Memorial St. Joseph Peninsula State Park, Florida. We would like to acknowledge support of the St. Joseph Bay Buffer Preserve and the Friends of St. Joseph's Bay for lodging. We thank S.M. Duke-Sylvester for statistical assistance and B.E. Felgenhauer for useful comments on this manuscript. We thank numerous graduate students from the University of Louisiana at Lafayette who participated in the field work, for which we would not have been able to do this research. Funding was provided by a Louisiana Board of Regents Fellowship and by the University of Louisiana at Lafayette Graduate Student Organization to the first author. This is Contribution No. 173 of the Laboratory for Crustacean Research.

References

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