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Sexual Sterilization of the Daggerblade Grass Shrimp Palaemonetes pugio (Decapoda: Palaemonidae) by the Bopyrid Isopod Probopyrus pandalicola (Isopoda: Bopyridae)
Abstract
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.
... The species Probopyrus pandalicola (Packard, 1879) is a highly distributed parasitic isopod that is known to infect several species within the family Palaemonidae (Beck 1980b;Conner and Bauer 2010;Sherman and Curran 2015). Although some research demonstrated that the infection by this isopod does no visible harm in the respective hosts (Morris 1948;Calado et al. 2006), other studies showed that it is capable of inducing harmful effects in the vitality of juvenile hosts (Anderson 1990), sexual sterilization (Sherman and Curran 2015), impairment of growth and reproductive traits (Van Wyk 1982) and induce feeding behaviour disturbances (Bass and Weis 1999). ...
... The species Probopyrus pandalicola (Packard, 1879) is a highly distributed parasitic isopod that is known to infect several species within the family Palaemonidae (Beck 1980b;Conner and Bauer 2010;Sherman and Curran 2015). Although some research demonstrated that the infection by this isopod does no visible harm in the respective hosts (Morris 1948;Calado et al. 2006), other studies showed that it is capable of inducing harmful effects in the vitality of juvenile hosts (Anderson 1990), sexual sterilization (Sherman and Curran 2015), impairment of growth and reproductive traits (Van Wyk 1982) and induce feeding behaviour disturbances (Bass and Weis 1999). This highlights even more the necessity of assessing the specific response of each species to this parasite, given the highly diverse nature and the conjoint of factors that are able to influence the interactions between hosts and parasites (Williams and Boiko 2012). ...
... The subsequent loss of nutrients caused by it can disturb and inhibit the synthesis of hormonal compounds that are thought to stimulate maturation processes (Fingerman 1997;Subramoniam 2011;Swetha et al. 2011). Finally, it is likely that the parasitized individual becomes sexually sterile (Sherman and Curran 2015). Although some decapod crustaceans have evolved to be adapted to nutrient loss and even starvation for considerable periods of time (Vinagre and Chung 2016), this can in fact also cause modification of growth patterns, altered survival and body composition in some other species that are not (Wu et al. 2004). ...
In this study, we aimed to record, for the first time, parasitic infestation by the isopod Probopyrus pan-dalicola on the prawn Macrobrachium acanthurus, as well as to register some ecological interactions. We hypothesized that the parasitic infection is able to negatively affect the prawn's nutritional condition and that this interaction can modify growth relationships in male individuals. We collected both parasitized (n = 25) and parasite-free (n = 25) individuals in several locations of the Contas River, state of Bahia, Brazil, which had their morphometric characteristics determined, including of the parasites. Relative growth models were constructed for both groups in order to compare slopes and intercepts and determine if the growth patterns are modified by the parasite. We also determined the body condition of the prawns, which was also compared between the two groups. Our results clearly demonstrated that the parasitic infection is able to induce modifications in relative growth patterns in male individuals and that this isopod is capable of reducing the nutritional condition of the prawns. This study indicates that this parasite can induce deleterious effects in the prawn, but individually. Further studies should be conducted to assess the relevance of our findings in conservation and management.
... Bopyrid isopods are obligate parasites that typically infest the gills or abdomens of decapod crustaceans. This infestation leads to stunted growth and a decrease in the reproductive capacity of the host (Beck, 1980a;O'Brien and Van Wyk, 1985;Calado et al., 2008;Sherman and Curran, 2015;Corral et al., 2019;Corral et al., 2021). Unlike other parasitic isopods, bopyrids have a complex life cycle that involves host changes from a small intermediate host (calanoid copepods) to a larger definitive host (decapod crustaceans) (Schädel et al., 2019). ...
... The carapace length of the host and body length of male female parasites were measured using ImageJ software (Schindelin et al., 2015). Prior to each observation, the developmental stages of the isopod embryo were noted according to the embryonic coloration and morphology described by Beck (1980c), Cash and Bauer (1993), and Sherman and Curran (2015), as follows: egg; translucent or white; embryo I: yellowish, embryo reniform, and tissue around the yolk segmented; embryo II: tan with brown pigmentation, body segmentation well-developed but appendages not free, with little or no yolk; epicaridium larva: dark grey or black, embryo with free appendages, and well-developed eyes. ...
The morphology of female bopyrids is adapted to parasitism, but understanding the function of their thoracic and mouth appendages is hindered by their small size and cryptic lifestyle, limiting detailed examination. This study aimed to clarify the function of the first oostegites and maxillipeds in bopyrid isopods infesting the branchial chamber of caridean shrimp through behavioural observations and morphological examination. We tested whether the movement of these structures was exclusive to ovigerous female parasites during brood ventilation. The results revealed that the beating of the maxillipeds and flapping of the first oostegites were not restricted to ovigerous females. However, the frequency of these movements was significantly higher in ovigerous females than in non-ovigerous females. The frequency of maxilliped beating increased with embryonic development, whereas that of flapping the first oostegites exhibited the opposite trend. Microscopic observation using dye showed that the movements of the maxillipeds and the first oostegites expelled residual dye from the female brood chamber through the dorsal surface or beneath the first oostegites. The dye was then transported by the water current generated by the scaphognathite of the host shrimp. These findings suggest that these structures not only facilitate ventilation but also serve as a grooming mechanism for female parasites, which is critical for embryonic survival. The results of the present study represent the first observation of embryo grooming in bopyrid isopods. This study also provides new information on the functional morphology of bopyrid isopods, which is important for understanding their ecological dynamics and adaptation to parasitism.
... Bopyrid isopods are obligate hematophagous ectoand holoparasites of crustaceans (Chaplin-Ebanks and Curran, 2007;Boyko and Williams, 2009;Williams and Boyko, 2012). They have complex life cycles that require a decapod as a definitive host, and a calanoid copepod as an intermediate host (Anderson, 1990;Lester, 2005;Oliveira and Masunari, 2006;Boyko and Williams, 2009;Sherman and Curran, 2015). An adult female bopyrid is typically found attached to the gills inside the branchial chamber, while the dwarf adult male is often found attached to the ventral side of the female bopyrid (Beck, 1980;Choong et al., 2011;Sherman and Curran, 2015). ...
... They have complex life cycles that require a decapod as a definitive host, and a calanoid copepod as an intermediate host (Anderson, 1990;Lester, 2005;Oliveira and Masunari, 2006;Boyko and Williams, 2009;Sherman and Curran, 2015). An adult female bopyrid is typically found attached to the gills inside the branchial chamber, while the dwarf adult male is often found attached to the ventral side of the female bopyrid (Beck, 1980;Choong et al., 2011;Sherman and Curran, 2015). Parasites induce visible lateral swellings on the carapace of the host and this deformation on the branchiostegite region characterizes the host-parasite relationship (Choong et al., 2011). ...
We determined the infestation rate of Probopyrus sp. in populations of Palaemon pandaliformis (Stimpson, 1871) and P. northropi (Rankin, 1898) in the Ubatumirim River, localized in a mangrove ecosystem on Ubatumirim Beach, northern coast of the state of São Paulo, Brazil. Samplings were carried out monthly from April 2003 to March 2004. Monthly prevalence varied from 0 to 4.94 % for P. pandaliformis, and from 0 to 4.54 % for P. northropi. This is the first record of Probopyrus sp. infesting the studied species in this region. Species of Probopyrus (Giard and Bonnier, 1888) seem to have a high plasticity with regard to palaemonid hosts, as they can be parasites of shrimps in both Palaemon (Fabricius, 1798) and Macrobrachium (Spence Bate, 1868). The linear relationships between the parasite and host sizes suggest that the parasite infests both hosts early in their development. We concluded that the infestation of Probopyrus sp. has little impact on Palaemon populations, mostly due to the low prevalence of infestation.
... The loss of nutrients through parasite action can disrupt and hinder the production of hormonal compounds that are believed to trigger growth processes and reproduction (Fingerman, 1997;Subramoniam, 2011;Swetha et al., 2011). A study conducted by Sherman & Curran (2015) revealed that prawns infested by Probopyrus experienced sexual sterilization. In the present study, none of the M. amazonicum females infested by Probopyrus were ovigerous. ...
The Amazon prawn or Macrobrachium amazonicum (Heller, 1862) is widely distributed in South America, occurring in the Orinoco and Amazon rivers, and forms an important source of income for riverside families. This prawn hosts crustacean ectoparasites of the genus Probopyrus (Giard & Bonnier, 1888) (Bopyridae) that infest its gill cavity. The aim of the present study was to report new occurrences of Probopyrus in Amazon prawns caught in the Amazon River. Macrobrachium amazonicum prawns were collected between May 2017 and April 2018, and again from July 2021 to May 2022 in the regions of Ilha de Santana and Rio Mazagão, state of Amapá, Brazil. Among the 5,179 prawn specimens caught, 133 were parasitized by the ectoparasites Probopyrus pandalicola (Packard, 1879), Probopyrus bithynis (Richardson, 1904), Probopyrus floridensis (Richardson, 1904) and Probopyrus palaemoni (Lemos de Castro & Brasil Lima, 1974). These occurrences of P. floridensis and P. palaemoni in M. amazonicum were the first records of this on the northern coast of Brazil. These four ectoparasites are not limited to specific host species or genera, as observed in this study, which reports four species of Probopyrus infesting M. amazonicum.
... The female isopod feeds on host hemolymph, consuming 1-10% of the total energy intake of the shrimp, reducing shrimp respiration, metabolism, and growth (Anderson, 1975(Anderson, , 1977Ludwig, 2009). These parasites also castrate shrimp hosts and have been known to negatively influence host population size (Chaplin-Ebanks and Curran, 2007;Calado et al., 2008;Sherman and Curran, 2015). In addition to the direct effects that Pr. pandalicola have on grass shrimp, they also may influence shrimp behavior, resulting in altered movements and more conspicuous hosts, with possible implications for predatorprey dynamics (Bass and Weiss, 1999;Brinton and Curran, 2015a). ...
In salt marsh ecosystems, daggerblade grass shrimp, Palaemon (Palaemonetes) pugio, play a crucial role in food webs and serve as the definitive host for the bopyrid isopod Probopyrus pandalicola. These ectoparasites infest the branchial chambers of grass shrimp, which can lead to decreased energy availability and sterilization of infected hosts. Although bopyrid isopod infestation of daggerblade grass shrimp has been frequently reported in literature from coastal marshes of the southeastern United States, the prevalence of this parasite has not been recently documented in daggerblade grass shrimp from marshes of the northeastern United States. The goal of this project was to quantify the prevalence of Pr. pandalicola infestations in Pa. pugio across Cape Cod, Massachusetts. We evaluated bopyrid isopod prevalence from shrimp collected from 5 different salt marsh habitats along Cape Cod in August 2021. Bopyrid isopod infestations were found in shrimp at 4 of 5 salt marshes, with prevalence ranging from 0.04 to 14.1%. Seasonal resampling of one of the salt marshes revealed the highest average infestation prevalence in spring (<17.1%) and an isolated high of 30.3% prevalence in a single salt panne. A series of linear and multivariate models showed that panne area, shrimp abundance, and distance to shoreline were related to Pr. pandalicola shrimp infestations in salt pannes in summer. This study describes the prevalence of the bopyrid isopod infesting daggerblade grass shrimp in salt marshes in New England, with implications for how parasitized shrimp influence salt marsh food webs in which they are found.
... Bopyrid isopods are obligate ectoparasites that infest decapod crustaceans such as shrimp, crabs, and anomurans (Markham, 1986;Williams and Boyko, 2012). Infestation causes alterations in the morphology, behaviour, and reproductive capacity of their host (Yoshida, 1952;Beck, 1980a;Ito and Watanabe, 1992;Bass and Weis, 1999;Calado et al., 2008;McGrew and Hultgren, 2011;Sherman and Curran, 2015;Corral et al., 2019;Golin et al., 2022). Bopyrids have a complex life cycle that requires two hosts: an intermediate host (calanoid copepod) and a definitive host (decapod crustacean). ...
The reproduction of bopyrid isopod parasites is thought to occur immediately following host ecdysis, but direct observations supporting this hypothesis are limited. The aim of this study was to describe the reproductive behaviour of the bopyrid isopod Bopyrus crangorum relative to host ecdysis based on video recordings. Several hours after host ecdysis, biphasic moulting of female parasites was observed. The cuticle of the posterior body was shed before that of the anterior body at an interval of 1 h. Two hours after female moulting, the male repeatedly moved from its initial position between the female pleopods and stopped at the anterior end of the fifth oostegite, immediately above the gonopore. To our knowledge, this repeated visiting behaviour by males has not been previously observed in bopyrid isopods. Oviposition through the female gonopore occurred 33 min later. The male-removal experiment showed that females with their males removed after visits to the gonopore oviposited eggs, whereas females with their males removed before visits did not. We propose that repeated visits by males to the gonopore are attempts to inseminate the female. We hypothesised that sperm are released onto the external surface of each gonopore and that the eggs are fertilised as they pass through the opening, which would explain the synchronous development of fertilised eggs inside the marsupium. The present study provides new information on the life history of bopyrid isopods, which allows for a better understanding of the host–parasite relationship.
... It presents a useful model due to its relatively high prevalence, ease in identification of the swollen branchial chamber, and ease of host maintenance; thus, several studies have examined the effect of the parasite on the survival of the shrimp, parasite and host seasonality, as well as the host-parasite relationship (e.g. Beck 1980a, b;Anderson 1990;Sherman and Curran 2015). ...
As with all animals, crustaceans serve as hosts to a very diverse taxa of parasites. These parasites range from unusual dinoflagellates that parasitise the hemocoels or eggs of their hosts, to classical helminths that use crustaceans as intermediate hosts, and to the bizarrely adapted tantulocarid and rhizocephalan crustaceans with their highly derived life styles. Here, I review the major parasitic taxa that use Crustacea as hosts. The parasites of decapods, particularly those in shrimps, crabs, and lobsters are the best known, primarily because of their impact on populations of their commercially important hosts. Several of these parasites are outright pathogens that cause widespread mortality, feminisation, and stunting in their host populations. Other parasites, particularly those in copepods, cladocerans, and amphipods have also received attention because of the ecological importance of these hosts in food webs. They have received notable studies on vertical transmission, the influence of cryptic species complexes (both host and parasite), as well as the emergence of new pathogens in these hosts. A few parasites are also known from brine shrimp (Anostraca) and barnacles (Cirripedia) which have served as laboratory or ecological models, respectively, but few of these parasites have received much study other than their initial taxonomic descriptions and systematic placement. Although molecular tools have revealed the systematics of many of the parasitic taxa, their biology and ecology remain poorly known.
... Host castration by bopyrid isopods is a well-known phenomenon (Van Wyk 1982;Oliveira and Masunari 1998;McDermott 2002;Sherman and Curran 2015), but it does not always occur, in some host species reproduction is only partially or not affected at all (Calado et al. 2006;Hernáez et al. 2010). We recorded ovigerous females of A. cristulifrons, A. estuariensis and S. curacaoensis parasitised by bopyrids and their fecundity and embryo volume were within the ranges reported for unparasitized alpheids (see Corey and Reid 1991;Hernáez et al. 2010;Oliveira et al. 2018). ...
Based on the examination of alpheid shrimps from the SW Gulf of Mexico and the Mexican Caribbean, deposited in two scientific collections housed in the Universidad Nacional Autónoma de México, we document for the first time Synalpheus curacaoensis, Alpheus cristulifrons and A. estuariensis as hosts of bopyrid isopods, and for the latter alpheid species is confirmed their distribution in Mexican coasts. Similarly, the bopyrids Capitetragonia alphei and Parabopyrella lata are recorded for the first time along coasts of Mexico. New hosts are reported for Bopyrione synalphei, on Synalpheus elizabethae; Parabopyrella mortenseni, on Alpheus normanni and A. cristulifrons; and Eophryxus subcaudalis on Synalpheus anasimus. The distribution range of Bopyrella harmopleon is extended and new localities are reported for B. synalphei, P. mortenseni and E. subcaudalis. Morphological remarks for the six bopyrid species are provided and reproductive data (fecundity and embryo size) are given for five of them.
... Bopyrid isopods exhibit a complex life cycle in which calanoid copepods serve as intermediate hosts and decapod crustaceans as the final hosts (Sherman and Curran 2014). This complex life cycle likely further decreases the chances of locating a suitable final host, especially if that host is not abundant. ...
Knowledge of marine host–parasite relationships has been increasing, but little is known about the reproductive strategies of the parasites. Theoretically, parasitic crustaceans inhabiting relatively small and scarce hosts should be monogamous. Parasites are also expected to exhibit higher reproductive performance (RP) than their free-living relatives, a strategy thought to have evolved to increase host-to-host transmission, or to be the outcome of living in a ‘stable, nutrient-rich environment’. Here, the parasitic isopod Parabopyrella lata and its shrimp host Lysmata boggessi were used to test for monogamy and augmented RP, and to examine whether or not P. lata castrates its host. Prevalence, population distribution, and reproductive performance were examined in P. lata over 1 year (2012–2013) off Homosassa Springs, Florida USA (28.8037° N, 82.5761° W). Prevalence of P. lata on L. boggessi was greater during the warmer months of the year and infested shrimps were almost exclusively males. P. lata lives in male–female pairs within the gill chamber of infested shrimps more frequently than expected by chance alone. The sizes of paired males and females were tightly and positively correlated with each other and with host size. Average fecundity (3660 ± 1146 eggs female⁻¹) and reproductive output (61 ± 19%) in P. lata, as with other bopyrid parasites, was much greater than those reported for free-living isopods. This evidence supports the hypotheses that parasites such as P. lata are adapted to be monogamous, display augmented RP, and reproductively castrate their host.
... They may also increase host susceptibility to predation, particularly at higher temperatures (Sherman and Curran, 2013). Many bopyrid species act as parasitic castrators that may partly or completely shut down host reproduction (Williams and Boyko, 2012;Sherman and Curran, 2015). The energy drained from the host may affect the development and function of reproductive organs (Lafferty and Kuris, 2009), sometimes causing male hosts to become feminized and leaving female hosts with immature gonads (Calado et al., 2005). ...
Caridean shrimp are critical components of seagrass communities and occasionally harbor parasitic bopyrid isopods, which can negatively impact their hosts. However, the ecological factors that drive infection rates of parasitic bopyrid isopods in host carideans are poorly known. We examined 43,785 carideans belonging to 6 families and 11 genera from 19 shallow-water localities throughout south Florida. Of these, only 114 shrimp (belonging to 5 genera) were found to be infested with bopyrids (an additional 251 had deformed carapaces consistent with recent infestation). We identified 13 bopyrid species (Bopyrina abbreviata; Bopyrinella thorii; Eophrixus subcaudalis; Loki circumsaltanus; Metaphrixus carolii; Ovobopyrus alphezemiotes; Parabopyrella lata; Parabopyrella richardsonae; Parabopyriscus stellatus; Capitetragonia alphei; Probopyrus pandalicola; Schizobopyrina urocaridis; and an unidentified Diplophryxus sp.). Bopyrid infection rates were very low throughout the study area, with mean prevalence of 0.26% (range 0.04-1.48%). Furthermore, each isopod species was only ever recovered from a single host genus, suggesting a high degree of genus-level specificity. At the community level, multivariate analyses (RELATE and BVSTEP) indicated that bopyrid community composition was correlated with host community structure, latitude and temperature, as well as the relative coverage of the seagrasses Thalassia sp. and Syringodium sp. and the alga Penicillus sp. Only 4 parasite taxa were sufficiently abundant to warrant further analysis at the individual taxon level: B. abbreviata, B. thorii, Diplophryxus sp., and P. pandalicola; stepwise regression indicated that bopyrid infection rates were primarily driven by the abundance of their specific hosts, and secondarily by environmental variables such as temperature and depth, as well as algal and seagrass community composition.
... They can be collected from marshes using dip nets or can be found at some major chain pet stores or bait shops. 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). ...
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.
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.
A total of 16,692 specimens of Paralomis granulosa was collected in the Beagle Channel. Tierra del Fuego, Argentina, between July 1996 and July 1997. This lithodid was parasitized by a bopyrid isopod identified as Pseudione tuberculata. Infested crabs exhibited a conspicuous bulge on their carapaces, which accommodated the parasite housed in the branchial chamber. The prevalence of infestation by P. tuberculata decreased with crab size, from 45.6% at 10-19.9-mm to 0% at 90-99.9-mm carapace length. Bopyrids were found on 251 occasions in the left branchial chamber and only once in the right branchial chamber. Except for two immature female parasites found in the branchial chamber of a small crab, all parasites were mature females, each usually carrying a dwarf male attached to its abdomen. The length of the female isopods and that of their hosts were positively correlated. These two observations suggest that the parasites infest P. granulosa early in the life of the host, and remain on, and grow up with the host throughout its life. The finding of crabs without bopyrids, but with distended branchial chambers, shows that some crabs survive the infestation. While breeding is inhibited in parasitized hosts, the prevalence of the parasite is already low (about 1.2%) at the size of host maturity. Therefore, we suggest that the reproductive potential of the crab population is not seriously affected by the sterilizing effect of the parasite. Finally, the cooccurrence of this bopyrid and a second parasite, the rhizocephalan Briarosaccus callosus, was recorded, but the prevalence of double infestations was low.
ABSTRACT Of 558 Palaemonetes spp. exposed to infective cryptoniscus larvae of Probopyrus pandalicola, 364 became infected (most within 24 h after exposure). Larvae of Probopyrus pandalicola are host specific (permanent infections leading to parasite maturation resulted when Palaemonetes pugio was exposed but only temporary infections or host death resulted when Palaemonetes vulgaris was used). Parasite success was also dependent on host age: young hosts of both species became infected more readily than older ones. Parasites typically are endoparasitic for up to 2 weeks after infection, later becoming ectoparasitic in the branchial chamber. However, the endoparasitic stage is unnecessary for parasite larvae infecting hosts already harboring a female bopyridium within the branchial chamber. Often, loss of parasites from hosts or movements of parasites after infection (i.e., during the transition from endoparasitism to ectoparasitism or during movement from one branchial chamber to the other) occurred at host ecdysis. The mortality rate of experimentally infected hosts is high during the parasite's endoparasitic stage which lasts from 1-2 weeks. However, the mortality rate 5 weeks after infection is near that of uninfected shrimp. Although my results suggest that parasites were distributed at random among shrimp in exposure vessels, further studies of parasite distribution using larger experimental host populations are warranted.
The burrowing mud shrimp, Upogebia pugettensis, is an important ecosystem engineer throughout bays and estuaries along the Pacific coast of North America. Populations of U. pugettensis have recently declined throughout its range. A likely reason for this decline is the arrival of an invasive bopyrid isopod parasite, Orthione griffenis, which has colonised the system and increased in prevalence. We tested the following three hypotheses regarding this host–parasite system: (1) parasite infection is correlated with the volume of water processed by the host; (2) infection negatively affects host’s energetic state; and (3) infection causes feminisation in male hosts. We used several physiological and morphological measures to quantify the effects of this parasite infection on U. pugettensis. The parasite appears to have different physiological effects on male and female hosts. Our study provides mixed support for the previous theory that predicted the mechanistic interactions between this host and its new parasite. Recent examples from other systems have demonstrated that invasive parasites can have far-reaching influences when they infect ecosystem engineers. Given the negative effects of O. griffenis on U. pugettensis, this invasive parasite may have similarly large impacts on Pacific North-west estuaries throughout its invaded range.
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.
High summer water temperatures can adversely affect stream salmonids in numerous ways. The direct effects of temperature associated with increased metabolic demand can be exacerbated by other factors, including decreased resistance to disease and increased susceptibility to parasites. We quantified the occurrence of black spot infestation caused by a neascus-type trematode (family Diplostomidae) of juvenile salmonids in Oregon's West Fork Smith River stream network during summer 2002 through fall 2003. The highest 7-d average of the daily maximum (ADM) temperatures was positively correlated with infestation rates in both years. We summarized the frequency and infestation severity of juvenile coho salmon Oncorhynchus kisutch by location within the network and summarized temperatures for 19 study reaches. Summer ADMs ranged from approximately 24°C near the watershed mouth to approximately 17°C in the upper reaches, while tributary ADMs ranged from approximately 16–18°C in the lower reaches to 12–17°C in the upper reaches. Temperatures were consistently higher in summer 2003 than in summer 2002. The presence of black spot infestation was more frequently noted in warm main-stem reaches than in adjacent cooler tributary reaches, and infestation rates were generally higher in 2003 than in 2002 in the same reach. Movements of coho salmon juveniles within the stream network also appeared to influence observed infestation rates.
Circumstantial evidence has suggested that marine microphallid trematodes using gastropods Hydrobia spp. as first intermediate hosts, amphipods Corophium spp, as second intermediate hosts, and various waterbirds as final hosts, may cause temperature-dependent epizootics and eventually local extinction of intermediate host populations. Therefore, we examined experimentally the impact of the microphallid trematode Maritrema subdolum on Corophium volutator with special reference to the influence of temperature, during the parasites' transmission from snail to amphipod. Trematode infected snails and amphipods were established together in experimental aquaria at temperatures of 15, 22 and 24 degrees C for 9 d. Amphipod surface activity, survival rate, parasite prevalence, infection rate, and parasite distribution both within and between amphipod individuals were recorded during, or at the end of, the experiment. The snails' shedding rate of larval trematodes as a function of temperature was also examined. Increasing temperature resulted in higher infection levels and parasite-induced mortality in the amphipods, most likely governed by a similar temperature-dependent emergence of larval trematodes from the snails. No transmission occurred at 15 degrees C, whereas at 24 degrees C the parasite prevalence approached 100 % and the parasite-induced mortality exceeded 50 % in relation to controls. As assessed by the transparency of the amphipods' gills, infestation inflicted anaemia was the likely mechanism behind the increased surface activity observed among infected specimens. This parasite-induced behavioural change may facilitate transmission of infective stages to shorebird hosts feeding on C. volutator. The results demonstrate that microphallid trematodes are able to induce a significant additive mortality in C. volutator populations. The temperature mediated mortality emphasizes the potential significance of a density-independent process in controlling the impact of parasites on host organisms and thereby host population dynamics.
This species profile summarizes much of the literature published about the biology of grass shrimp, Palaemonetes spp. Five species (P. pugio, P. vulgaris, intermedius, P. paludosus, and P. kadiakensis) are common in coastal waters of the northern Gulf of Mexico, although the last two are primarily freshwater forms. The brackish-water species are among the most abundant shallow-water benthic decopods in estuaries and play important roles as food for fishes and as transporters of nutrients among various trophic levels. They spawn from spring to autumn and the growth of planktonic larvae is normally completed n 7 to 12 molts. Postlarvae of 7-10 mm are 1.5 to 2 months old. The life span of grass shrimp is 6 to 13 months (maximum size rarely exceeds 50 mm). Palaemonetes spp. are eurythermal, euryhaline, and are relatively tolerant to hypoxia and a variety of pollutants. Grass shrimp feed on detritus, epiphytes,and meiofauna. They tend to concentrate near underwater structures and plants, especially in dense stands of underwater macrophytes. (Author)
The pattern of brood production was analyzed in the grass shrimp Palaemonetes pugio. Determination of patterns of brood production as successive (spawning after each molt) or alternate (spawning after every other molt) was made by observations on individual females paired with males in the laboratory over a four-month period. A pattern of successive parturial (spawning) molts was the most common pattern. However, in a majority of these successive parturials, the ovary of the female was not mature at hatching of embryos from a previous brood. There was a delay of 10–11 days, during which ovarian maturation took place, between embryo hatching and the next (parturial) molt. This pattern of “slow successive” parturials does not result in the truly continuous brood production which occurs in many caridean species, i.e., spawning of a new brood within 1–2 days after hatching of a previous brood. However, there was a relatively low percentage of females in which the ovary was mature at embryo hatching. These latter females did have a parturial molt after only 2 days (“fast successive” parturial). In the “alternate” pattern, more frequent later in the 4-month observation period, hatching of embryos was followed by a non-parturial (without spawning) molt within 2 days, followed by an intermolt period of 10 days during which ovarian maturation occurred prior to the next (parturial) molt. The interval between spawns was similar in the “slow successive” and “alternate” parturial molt patterns (22–23 days) compared to a much shorter one (14–15 days) in the “fast successive” parturials. Examination of reproductive females from field samples indicated that the spawning pattern observed in the laboratory was that which occurs in natural populations in southern Louisiana. Although brood production in P. pugio is not truly continuous, the relatively short interspawn intervals observed still allow production of several broods during the breeding season.
Several Synalpheus species have been reported as hosts of bopyrid parasites; however, the impact of infestation on egg production is still unknown. Therefore, the present work studied reproductive aspects and the effect of parasitism on fecundity of the alpheid shrimp Synalpheus yano from Bocas del Toro, Caribbean coast of Panama. Un-infested females (N = 84) ranging from 3.7 to 9.6 mm carapace length, produced between 5 and 246 eggs (average: 98±64.6), and egg number increased significantly with female size. The eggs were relatively large (0.6–1.3 mm in diameter), but within the range of other Synalpheus species, and egg size did not differ significantly between un-infested and infested females. Despite these large eggs, the morphological characteristics of hatching larvae indicate a planktotrophic development. During the incubation period, the egg volume increased from 0.100 to 0.218 mm3, representing an overall increase of 118%. A total of 18 females (16% of all ovigerous individuals) were infested, and the occurrence of parasitic infestation was more pronounced in larger females. Infested females ranging from 4.6 to 9.4 mm carapace length, produced between 22 and 166 eggs (average: 81±44.4). Egg-bearing females infested by parasitic bopyrids carried on average 41% fewer eggs than similar-sized females without parasites. The co-occurrence of parasites and developing eggs, however, indicates that the bopyrid parasite does not necessarily castrate its host. Therefore, we encourage more comparative intraspecific studies on egg production in infested and un-infested females to assess the impact of infestation on fecundity in caridean shrimp.
The present work reports the existence of parasitic castration induced by the bopyrid isopod Argeiopsis inhacae parasitizing the branchial chamber of female Stenopus hispidus. Parasitized and unparasitized females of S. hispidus displayed similar intermoult periods (14 +/- 2 d) and exhibited similar mating behaviours. However, despite exhibiting typical mating behaviour, parasitized females were never able to produce any egg clutch when paired with unparasitized males; neither displayed the typical 'dorsal bright green spot' evidencing the presence of large vitellogenic oocytes. The idea that bopyrid infections generally lead to the 'reproductive death' of the decapod host is reinforced and the apparent existence of a heavily sex-biased infection towards females in S. hispidus may just be a consequence of the still limited number of surveyed specimens.
I quantified the effects of parasitism by the isopod Probopyrus pandalicola on energy flow through the host Palaemonetes pugio by comparing secondary production, metabolism, ingestion, and egestion by unparasitized laboratory shrimp populations to the same parameters for parasitized groups during 10 months. The effects of parasitism on host growth and metabolism vary from month to month. Temperature, season, host age, sex, and reproductive condition affect energetics for host-parasite systems. Probopyrus pandalicola has little effect on host assimilation efficiency. However, tissue growth efficiences during most study months were higher for control shrimp than parasitized shrimp. These differences between groups were of lesser magnitude when parasite production was considered in the calculations. Trophic level energy intake efficiency for parasites was of the order of 6 to 10% throughout much of the study—the highest values were calculated during the parasites' reproductive months. Through parasitic castration, P. pandalicola significantly affects host energetics. Significantly, parasite reproduction was often of the same magnitude as reproduction by unparasitized hosts, although parasite biomass accounts for only about 4% of the total host-parasite system biomass.
A dramatic increase in prevalence of the recently discovered bopyrid isopod parasite, Orthione griffenis, likely introduced in the 1980s from Asia to the Pacific coast of North America, coincided with the 2002 collapse of a population
of its burrowing mud shrimp host, Upogebia pugettensis, in Willapa Bay, Washington that had been stable since monitoring began in 1988. An examination of whether O. griffenis infections were sufficient to cause this decline and other recently noted U. pugettensis population collapses in Pacific Coast estuaries was conducted. O. griffenis prevalence was the highest in large reproductive-sized female shrimp and caused an estimated average 68% loss of U. pugettensis reproduction in Yaquina Bay, Oregon over a 5-year period. O. griffenis prevalence fluctuated from year to year, but trends were similar in all estuaries sampled. Uninfected shrimp transplanted
back into locations from which they had disappeared acquired the parasite, suggesting that O. griffenis is extremely effective at finding its host even in estuaries with very low host density. Since both U. pugettensis and O. griffenis have pelagic larval stages, their population dynamics are also influenced by coastal nearshore oceanography and estuarine
recruitment success. Coastwide lack of estuarine recruitment appears to coincide with declines in density of a co-occurring
thalassinid shrimp, Neotrypaea californiensis, but cannot alone explain U. pugettensis population collapses. Although patterns observed to date could be explained by the presence of either a native or introduced
parasitic castrator, assumptions of a resilient co-evolved host–parasite relationship do not apply for introduced species,
so continued efforts to follow the spatial extent and consequences of the O. griffenis–U. pugettensis host–parasite relationship are warranted.
KeywordsParasitic castrator–Local extinctions–Introduced species–
Neotrypaea californiensis
–Thalassinidea
The grass shrimp, Palaemonetes pugio, plays a large role in the marine ecosystem, serving as a vital link in the food web between many other species. Marine parasites such as the bopyrid isopod, Probopyrus pandalicola, reduce shrimp growth and reproductive output and may also cause P. pugio to be more vulnerable to the lethal effects of contaminants. The purpose of this study was to determine the toxicity of resmethrin and bifenthrin on the grass shrimp, P. pugio, infected with the bopyrid isopod, Probopyrus pandalicola. A 96-h static renewal test was conducted to determine the toxicity of the pyrethroid insecticides resmethrin and bifenthrin to grass shrimp, Palaemonetes pugio, parasitized with the bopyrid isopod, Probopyrus pandalicola. The results were then compared to similar tests utilizing unparasitized P. pugio. Parasitized P. pugio had lower 24-h LC(50) (1.08 microg/L) and 96-h LC(50) (0.43 microg/L) values for resmethrin than unparasitized P. pugio. However, LC(50) ratio tests found that there was no significant difference between parasitized and unparasitized shrimp when affected by resmethrin (p = 0.1751 and 0.1108, respectively). In contrast, an LC(10) ratio test indicated that there was a significant difference between parasitized and unparasitized P. pugio after 96 h (p < 0.0001). When subjected to bifenthrin, parasitized P. pugio had a higher 24-h LC(50) (0.049 microg/L6) than unparasitized P. pugio. The LC(50) ratio test established that the effects of bifenthrin on parasitized P. pugio when compared to unparasitized P. pugio were significantly different at 24 h (p = 0.0065). However, there were no significant differences between parasitized and unparasitized after 96 h (p = 0.4229). In conclusion, both resmethrin and bifenthrin are toxic to the grass shrimp, P. pugio, regardless of parasite presence, and parasitized shrimp may be more susceptible to lower doses of resmethrin (when exposed in the field).
The daggerblade grass shrimp Palaemonetes pugio Holthuis, 1949 is prevalent in estuaries along the East and Gulf coasts of the United States, and is an integral part of the estuarine food web. Probopyrus pandalicola (Packard, 1879) is a bopyrid isopod that parasitizes P. pugio and decreases the energy available to its host by feeding on the hemolymph of the shrimp. The parasite also causes female shrimp to be castrated. The purpose of this study was to determine the effect of Probopyrus pandalicola on the survival time of P. pugio during starvation at two different temperatures. The experiment was conducted between September 2009 and June 2012 at 20.0 +/- 0.11 degrees C and 25.0 +/- 0.10 degrees C. Three trials at each temperature were performed. For each trial, parasitized, deparasitized and unparasitized shrimp were randomly placed into individual aquaria in a temperature-controlled chamber. All trials lasted until 100% shrimp mortality occurred. The bopyrid isopod did have a significant effect on shrimp survival times, but only at the higher temperature during which parasitized shrimp survived a significantly shorter amount of time (21.8 +/- 6.93 days) than unparasitized shrimp (25.2 +/- 8.25 days). In contrast, the bopyrid did not have a significant effect on shrimp survival times at the lower temperature, with shrimp surviving an average of 26.9-27.5 days. The results of this study have implications related to potential climate change, specifically higher temperatures, as we found that a small increase in temperature significantly affected the response of P. pugio to the isopod parasite. This supports prior research on other host-parasite interactions that are affected by increased temperature.
Sponge-dwelling snapping shrimps are often more heavily parasitized by bopyrid isopods than their free-living relatives, but little is known about how parasitism influences the behavior and morphology of these shrimps. In this study, we measured parasitism rates in the eusocial snapping shrimp Synalpheus elizabethae and tested whether parasitism by bopyrid isopods (Bopyrione sp.) affects shrimp activity levels and morphology. Using field surveys, we found that S. elizabethae suffer higher parasitism rates when inhabiting the sponge Lissodendoryx colombiensis than do co-occurring pair-forming congeners (S. yano and S. dardeaui) in the same host. In laboratory behavioral assays, parasitized S. elizabethae showed 50% lower activity levels than unparasitized colony members, suggesting that infection by bopyrids decreases shrimp activity. Finally, parasitism influenced shrimp morphology; parasitized S. elizabethae individuals were larger, but had relatively smaller major chelae (25% reduction) than unparasitized individuals. Parasites comprised similar to 5% of the entire body weight of an individual shrimp. Together these data suggest that parasitism by bopyrid isopods may incur significant energetic costs for commensal sponge-dwelling shrimps such as Synalpheus, and may be especially severe for social species such as S. elizabethae.
During a faunal survey of the intertidal mud flat of Shinhama Lagoon on the northern coast of Tokyo Bay, parasitic bopyrid isopods, Ione cornuta Spence Bate, were found attached to the inner walls of the branchial chambers of ghost shrimps, Nihonotrypaea japonica (Ortmann). In this isopod, the females are parasites of N. japonica whereas dwarf males attach to conspecific females. To investigate the prevalence of the parasite I. cornuta, sampling of ghost shrimps was conducted every 2 to 4 weeks at the Shinhama Lagoon during the periods from August, 1994, to October, 1995, and January, 1998, to May, 1999. A total of 328 individuals (253 females, 62 males, and 13 of unknown sex) of N. japonica was collected, and 22 individuals among them (6.7%) were infected with I. cornuta. Among the infected shrimps, females accounted for 21 individuals, and only one male was infected. This skewed sex ratio is considered to simply reflect the female-biased sex ratio of this species in the field. In most cases, one individual of the parasite I. cornuta was attached within the left or the right branchial chamber of each host shrimp. No significant relationship was detected between the handedness of the major cheliped of the host shrimps and the attachment position of I. cornuta. A significant positive correlation was found between the size of the host shrimps and the size of mature females (i.e., those with brood chambers) of the parasite; however, the size of immature parasites was not correlated with the size of their host shrimp. In spite of the long sampling periods during this study, no ovigerous shrimp infected by I. cornuta was collected. This strongly suggests that infection by I. cornuta negatively affects the reproduction of the host female shrimps.
The grass shrimp, Palaemonetes pugio, is a dominant species uniquely adapted to a highly stressed tidal marsh embayment. Monthly sampling of length and dry weight revealed that its life cycle was a single year, with spawning in May, June, and July and most rapid growth in late summer and fall. Mark and recapture estimates conducted quarterly and quadrat net estimates calculated monthly indicated that shrimp were present throughout the year and that densities peaked in the fall (over 1.2 million in 0.01 km2 in October). Production of biomass (growth) equated loss to predation (including decomposition) over the annual cycle, averaging 0.2 kcal@?m^-^2@?day^-^1. Respiration averaged 1.1 kcal 1.1 kcal@?m^-^2@?day^-^1. Average daily production per square meter of "total consumables" (fecal pellets = 0.8 kcal, dissolved organic matter [DOM] = 0.7 kcal, biomass = 0.2 kcal) was 60% of total ingestion (2.9 kcal); production of feces and DOM thus outweighed biomass production 15:2. Microcosm studies and observations by scanning electron microscope revealed that shrimp macerated detritus into a heterogeneous assortment of uneaten particles by plucking away the cellular matrix from surfaces of large detrital fragments. This action provided cavities that became heavily invaded by pennate diatoms, and particles that became suspended in the water column and populated by bacteria. Nutrient analyses indicated the shrimp excreted large quantities of ammonia and phosphate which together with DOM release was presumably responsible for heavy growth of microflora and increased protein fraction in both feces and large and small uneaten detrital fragments. Palaemonetes pugio, while supporting its own trophic requirements, accelerated breakdown of detritus, preventing blockages or accumulations that might have occurred from pulses of emergent grass and macroalgal detritus in the embayment. This repackaging into feces, heterogeneous fragments, DOM, and shrimp biomass made detrital energy available at a variety of trophic levels, smoothing out organic pulses over time and space, and raising the efficiency of transfer to the food web. The special adaptation of P. pugio to the low-oxygen environment of the decomposer system appeared to limit predation and competition, allowing the shrimp to develop large populations necessary to carry out its role effectively.
Data are provided on the reproduction, attachment, postlarval development and population structure of the parasitic isopod, Probopyrus pandalicola, on its shrimp host, Palaemonetes paludosus, collected monthly for 2 years from a site in the Wakulla River and a tributary, McBride's Slough, Wakulla Co., Florida. Ovigerous P. pandalicola occurred from January to October, whereas ovigerous hosts occurred only from January to September. Brood size, which ranged from 350-11,850 young, increased exponentially with length of the female, and was independent of host sex. Mean brood size and length of ovigerous P. pandalicola increased from late winter to a peak in March. There was a second smaller peak in June with a subsequent decline to low levels for the remainder of the breeding season. Cryptoniscus larvae occurred on shrimp 9-39 mm long from April-October. Growth of body width in relation to body length in male and female isopods was positively allometric. The length of female and male parasites was positively correlated with the length of the host and female parasite, respectively. Host and parasite longevity was ca. 1 year. Death of the parasite rarely preceded host death. These data are compared with that for other epicaridean isopods.
Monthly samples of shrimp, Crangon spp., were collected from Hookton Channel in South Humboldt Bay, California, from April 1983 through April 1984. A total of 5790 Crangon franciscorum and 9741 C. nigricauda and C. nigromaculata (in combination) were collected. Crangon nigromaculata was collected only occasionally. Of the total shrimp collected, 169 C. franciscorum and one C. nigromaculata were infested with the bopyrid isopod Argeia pugettensis. Infestation of A. pugettensis on C. nigricauda in other localities has been recorded; however, no C. nigricauda were found infested in this study. Parasite prevalence on C. franciscorum ranged from 0% to 34%. Prevalence fluctuations apparently resulted from shrimp migration. Frequency of infestation did not differ significantly between the right and the left branchial chambers of the host shrimp and no shrimp had multiple infestations. Female shrimp were infested more frequently (85%) than males (15%) even though females were often less abundant. Infested female shrimp were significantly smaller than noninfested females. Ovigerous isopods occurred whenever isopods were collected (April through January). Female isopods apparently become reproductively mature between 3.0 and 4.0 mm long. Isopod brood sizes ranged from 1600 to 38,300 eggs and increased with female length. Male isopod length increased with female isopod length, which increased with host shrimp length. Host shrimp were probably infested early in their life.
The diet of the Atlantic croaker from Mississippi Sound has been examined for the first time. Over 83 taxa were encountered, or more than were reported from croaker in any other region. We also found 60 taxa, 36 of which overlapped with the above, in croaker from various offshore stations in the Gulf of Mexico. In Mississippi Sound the frequency of occurrcnce of items revealed primarily crustaceans followed by polychaetes, molluscs, fishes, and less common items, and, in the open Gulf, molluscs appeared slightly more often than in inshore croaker and than polychaetes in offshore fish. The diets were assessed according to length of fish, season, depth of water, and locality.
The bopyrid, Probopyrus pandalicola, infects grass shrimp, Palaemonetes pugio, and negatively affects shrimp respiration and metabolic activity, prevents reproductive output, and reduces shrimp activity. Our objective was to determine whether grass shrimp maintained tidal rhythmicity in the laboratory and whether the bopyrid parasite affected tide-related grass shrimp activity levels. Five bopyrid-parasitized and five unparasitized shrimp were selected, and examined for sex, length, and for number of trematode cysts (to exclude any effect of that parasite). The shrimp were randomly placed in individual static aquaria with sand substrate and filtered seawater, and tanks were separated by opaque dividers. Shrimp were maintained on an ambient photoperiod (14.5-h day) and observed for activity every three hours (corresponding with high, ebb, low, and flood water) for two tidal cycles. Tidal stage had a significant effect on shrimp activity with the maximum number of shrimp (71%) resting at flood and the minimum (16%) at ebb (n = 10 trials). There was a significant effect of light and tide-light interaction on shrimp activity with the greatest activity at night, particularly during nighttime-ebb. Because shrimp were most active during ebb, they may be more susceptible to predation by visual predators in the water column at that time. Bopyrid infection did not significantly influence shrimp activity, and thus was not the primary factor affecting shrimp activity in the first 30 h after collection.
Während des Studium der externen (Universität zu Liverpool) und der internen (Freie Universität, Amsterdam) Faktoren, welche auf die Zwischenhäutungsperiode von Palaemonetes varians (Leach) einwirken, wurden die Fortpflanzungseigenschaften dieser Art näher untersucht, beschrieben und verglichen mit denen von Palaemon elegans Rathke (cf. Höglund, 1943, als Leander squilla), die einzige andere Garnele, die in dieser Hinsicht ausführlich untersucht wurde. Die Resultate dieses Vergleiches zeigen deutlich, daß das Brutkleid von Palaemonetes varians dem von Palaemon elegans in hohem Maße ähnlich ist mit Ausnahme der folgenden Unterschiede: 1, zusätzliche Setae an der Innenseite der abdominalen Epimera von Palaemonetes varians; 2, während der Brutperiode erhält Palaemonetes varians ein zusätzliches Chromatophorenmuster; 3, die Vergrößerung der Abdominalpleuriten erweist sich als permanentes sekundäres weibliches Geschlechtsmerkmal von Palaemonetes varians und unterliegt nicht wie bei Palaemon elegans einer periodischen Vergrößerung während der Brutperiode. Ferner ergab sich aus den individuellen Häutungsprotokollen einer Anzahl Palaemonetes varians während der Fortpflanzungszeit, daß die Brutzwischenhäutungsperiode reichlich zweimal so lang ist wie die normale Zwischenhäutungsperiode. Schließlich werden im Zusammenhang mit der aufgezeigten Hemmung des Häutungsrhythmus während der Brutperiode einige Aspekte des Fortpflanzungsprozesses besprochen.
Survival of the branchial ectoparasite Probopyrus pandalicola through ecdysis of the host, Palaemonetes pugio, was studied by observing infected shrimps before and after ecdysis and directly with time-lapse video. The parasite pair retained its position through 97.3% of 112 host ecdyses. This observation and positive correlations between parasite and host size support the hypothesis that bopyrid isopods remain on and grow together with their host. Video recordings of shrimp ecdysis showed that the female and male maintain their position rather than being cast off and reentering the host branchial chamber. Observations on exuviae from parasitized shrimps and from video recordings suggest that the female parasite avoids being discarded with the molt skin by immediately attaching to the newly exposed inner lining of the gill cover as the shrimp backs out of its exuviae. Reproductive activities of the parasite relative to host molting were studied. Epicaridium larvae were released from the host branchial chamber several hours to 5 days before the host molt. Spawning by the parasite female took place within several hours (median = 12 h) after host ecdysis. Expulsion of exuvial fragments of female parasites from the host branchial chamber was observed in 2 video recordings prior to spawning. In several video recordings, the usually inactive male moved from its site on the female abdomen up to and inside the female marsupium after the host molt and before female spawning, presumably to inseminate the female. Females from which males had been removed failed to produce a brood after the next host molt, tentatively supporting the hypothesis that females must be inseminated prior to each spawning.
Although infestation of Penaeus semisulcatus by Epipenaeon elegans does not inhibit growth of the host, there is a drastic effect on reproduction. The gona-dosomatic index is ≤ 0.5 in both infected male and female shrimps. The petasma is not formed in the infected male shrimps. The ovaries remain small in infected females and the oocytes do not develop beyond primary vitellogenesis. If the parasite is lost the ovary of the host is activated and oocytes in vitellogenesis are observed. The testes in infected males are also reduced and few spermatozoa are formed. These findings are compared with other studies on parasitic castration in Crustacea.
The bopyrid parasite Orbione halipori was recorded for the first time from Metapenaeus joyneri. Morphometric analysis indicated that infested male and female shrimp have slightly, but significantly, lower body weight than uninfested shrimp of the same carapace length. While the parasites sterilize their hosts, the low infestation rate (0·53%) appears not to pose a threat to the shrimp fisheries in the Zhujiang estuary.
The relationships between mean intensity and prevalence of infestation of Pseudione humboldtensis and the size and sex of the hosts, the squat lobsters Cervimunidia johni and Pleuroncodes monodon, from three fishing grounds in northern Chile are described. The prevalences were 13.6% and 6.8% for C. johni in Coquimbo and Huasco, respectively, while in P. monodon they were 18.2% and 0.6% in Coquimbo and Caldera, respectively. Between fishing grounds, no significant differences were found in the prevalence of infestation between male and female C. johni, but in Coquimbo, the prevalence of infestation in P. monodon was significantly higher in females. The sizes of infested squat lobsters were significantly lower than those of uninfested hosts. Males and females parasitized by P. monodon showed significantly lower body weights than uninfested hosts. Parasitized males of C. johni showed lower body weight than uninfested males. Only 0.6% of ovigerous females of C. johni and none of P. monodon were infested. The near absence of infested ovigerous females suggests castration process in females. A nonlinear relationship was detected between host size and parasite size for both females and males. Multiple infestations of P. humboldtensis were found in both host species, but they were more common in P. monodon. Given the high prevalence of multiple infestations (50%) and the significantly lower body weights of infested P. monodon, we suggest that this host is more vulnerable to P. humboldtensis than is C. johni.
The smooth bay shrimp, Lissocrangon stylirostris, was sampled using a beach seine and a hyperbenthic sledge in the summer of 2006 at a dissipative sandy beach in southern Oregon. We investigated possible variations in the population structure due to environmental variables, preferred prey, sexual system employed, impacts due to parasitism by the bopyrid isopod Argeia pugettensis, and possible predators. The population was 63% female, and females were generally larger than males. The density of L. stylirostris varied significantly with the time of day. A cohort of small shrimp was observed from July to September while large adult shrimps were rare during the same months. The net effect was that shrimp densities were stable over the summer. The shrimps fed mostly at night on the mysid Archaeomysis grebnitzkii. The differences in female to male ratio, the larger size of females relative to males, and the relatively little overlap in size frequency distribution between males and females could be because this species exhibits a type of protandry. Both male and female shrimps supported an equal, high prevalence of, level of infestation by A. pugettensis (62%). The parasitized shrimps were larger in size than normal shrimps but had lower weight per length ratio. Very few brooding shrimps were parasitized (0.2%), and a higher percentage of parasitized shrimps had empty stomachs and significantly lower stomach contents. We hypothesize that the parasite is affecting the shrimp by producing variation in its normal size and weight, sterilizing females, and reducing its ability to capture food. Finally, individuals of English sole and Pacific staghorn sculpin individuals preyed on the shrimps.
In this paper, adaptations and microanatomic changes in the branchial chamber, as well as influence of parasitosis on the reproductive function of shrimp, are analyzed. Probopyrus cf. oviformis was observed in the branchial chamber of shrimps of both sexes, with an infestation rate of 29%. The infestation frequency in relation to sex and size was not uniform, and two trends were observed: a higher frequency in bigger males in contrast to females, with less infestation frequency in older individuals. This aspect was related to changes in the sex ratio of shrimps, infested and noninfested, with the following conclusions: (1) Sexual inversions were not observed in females of P. argentinus; (2) male infestation with P. cf. oviformis showed tertiary sexual rate bias. It occurred because the metabolic parasite-host relationship led to an increase in size. These infested males were incorporated into a normal population characterized by females being bigger than males. The morphological and functional changes observed were (1) branchial chamber reduction, slendering of the cephalothorax lateral wall, together with local injury (oxygen consumption was below the normal values; and (2) the ovaries of infested females of P. argentinus remained stationary in incipient maturity (secondary vitellogenesis was not observed).
A population approach was employed to study the effects of a bopyrid isopod, Aporobopyrus muguensis, on the growth and reproduction of its anomuran host, Pachycheles rudis. Indirect evidence, provided by the size-specific prevalence pattern, and direct evidence, provided by laboratory moult frequencies and moult-stage data, indicated that the frequency of moulting was reduced among parasitized crabs. Moult increments of parasitized crabs were less than those of non-parasitized crabs. Although parasitized female P. rudis were able to reproduce, their fecundity was substantially reduced. Parasitized female hosts appeared to be delayed in their attainment of sexual maturity. Once mature, these crabs produced significantly smaller size-specific clutches than those produced by non-parasitized female crabs. Because fecundity increases with size in P. rudis, the slower growth rates of parasitized female hosts may further limit their fecundity. Potential mechanisms by which A. muguensis limits the growth and reproduction of P. rudis are discussed.(Accepted March 22 1982)
1. Disease severity may be altered by the differential responses of hosts and parasites to rising temperatures leading to an increase or reduction in disease. The net effect of climate change on emerging diseases will reflect the effects of temperature on all life history stages of both hosts and parasites.
2. To explore how climate change differentially influences hosts and parasites, we studied the effect of increasing temperatures on different life stages of the multi-host trematode parasite Ribeiroia ondatrae, which has been linked to the emerging phenomenon of amphibian limb malformations, and its snail intermediate host Planorbella trivolvis. We determined the effects of temperature on the development of R. ondatrae eggs and redia larvae and the effects of parasite exposure (exposed and sham-exposed), temperature (13, 20, and 26 °C) and their interaction on snail host vital rates, including growth, mortality and reproduction.
3. Ribeiroia eggs developed four times faster at 26 °C than at 17 °C and did not develop at 12 °C. Higher temperatures increased snail growth, egg production and mortality. Infection interacted with temperature to enhance the growth of infected snails while reducing their fecundity at 26 °C. These results suggest that pathology associated with infection is amplified at higher temperatures.
4. The timing of interactions between R. ondatrae and P. trivolvis may be influenced by their physiological responses to temperature. Temperature-driven increases in the growth of infected snails coupled with the cessation of parasite development at lower temperatures suggest that warming temperatures will change host–parasite dynamics. Taken together, these results indicate that future climate change could alter parasite abundance and pathology by creating a ‘phenological mismatch’ between snail hosts and parasites, potentially leading to infection of both snail and amphibian hosts in earlier and, in the case of amphibians, more vulnerable stages of development.
Macrobrachium ohione is a migratory (amphidromous) river shrimp (Decapoda, Caridea) that may be parasitized by the branchial parasite Probopyrus pandalicola (Isopoda, Bopyridae). The parasite disrupts gonadal maturation and spawning in female shrimps, resulting in the total loss of reproduction. Shrimps are usually infected by bopyrid parasites during the late zoeal or early postlarval stages; in this study, we investigated the apparent parasite infection of adult shrimps. We analyzed the relationships between parasite body size (total length) and host shrimp body size (carapace length) to test the hypothesis that parasite infection of adult shrimps occurs during the shrimps' reproductive migrations. The results presented here indicate that infection of adult shrimps is common in M. ohione in the Atchafalaya and Mississippi Rivers, Louisiana, USA. In the two upriver sites sampled, Butte La Rose (BLR) and River Bend (RB), parasite size was not associated with host body size. In these locations, many parasitized adult M. ohione were infected with immature P. pandalicola (40.3% in BLR and 51.2% in RB), indicating that the shrimps were adults at the time of infection. A possible explanation is that when female shrimps enter the estuary to hatch larvae, they molt and spawn another brood. The smaller male shrimps that accompany the females downstream are also assumed to molt and continue growth. The intermediate host of the parasite is an estuarine copepod, and thus the parasite cryptoniscus larva that infects the host shrimp is primarily estuarine as well. Newly molted shrimps have soft cuticles, which may facilitate their infection by parasite cryptonisci. Our conclusion is that most infections of adult shrimps occur during their migration into estuarine waters, the primary habitat of infective parasite larvae, and that host vulnerability is probably increased following host ecdysis.
A population of Palaemonetes pugio Holthuis 1949, inhabiting a fairly constant high salinity estuarine environment (North Inlet), exhibited more rapid growth, earlier first reproduction, a smaller clutch size, more fluctuating sex ratio, and shorter life span. A population in a less saline environment (Minim Creek) showed relatively slower growth, delayed first reproduction, larger clutch size, female-dominated sex ratio, and longer life span. Growth in both areas was rapid in summer and slower in winter, with the females growing much larger than the males. Summer generation females first reproduced at the age of 3.5 months in North Inlet and at 4.8 months in Minim Creek. Minim Creek females larger than 30-mm TL carried more eggs than North Inlet females of similar sizes. Life span in North Inlet was calculated to be 6–7 months for the summer generation and 9–10 months for the winter generation; in Minim Creek, the corresponding longevity estimates were 9–10 months and 12–13 months, respectively. Variations in life history patterns are hypothesized to be the results of numerous environmental factors acting differentially on the various life-stages of the organism. The results suggest that the reproductive flexibility of P. pugio enhances its ability to persist in a variety of environments.
Estuarine assemblages of fishes and natant decapod crustaceans (i.e. nekton) comprise both permanent resident species and juveniles of coastal marine species that use estuaries primarily as nurseries. In an attempt to understand how the young of marine species successfully invade communities of permanent estuarine residents we studied potential interactions between two of the most abundant decapod crustaceans in nekton assemblages of the southeastern United States. Three years of quantitative samples from an intertidal marsh on Sapelo Island, Georgia showed that densities of the resident daggerblade grass shrimp Palaemonetes pugio were reduced during the time that juvenile white shrimp Penaeus setiferus used the estuary as a nursery. Results of a field enclosure experiment showed that white shrimp had no significant lethal or sublethal effects on adult grass shrimp. However, they did reduce survival of both juvenile and larval grass shrimp in laboratory experiments, suggesting the potential importance of a stage-dependent predatorprey interaction between the two shrimp species. The mortality rate of young grass shrimp in the presence of white shrimp was unaffected by grass shrimp density, but larvae (2.6–3.0 mm) suffered higher mortalities than did juveniles (5.0–15.0 mm). We suggest that the vulnerability of grass shrimp to predation by white shrimp is related to their molting cycle. The window of vulnerability opens more often for younger grass shrimp because they molt more frequently. When combined with losses due to other predators and competitors, the impact of early white shrimp cohorts on grass shrimp larvae and juveniles may prevent the resident species from maintaining its population at high densities, thereby freeing resources in the nursery for subsequent cohorts of juvenile white shrimp.
The distribution, hatching dates, growth, and food habits of larval and juvenile red drum (Sciaenops ocellatus) in Tampa Bay, Florida, are described. From September 1981 through November 1983, 800 larvae and 7,536 juveniles (98%<100
mm SL) were collected, primarily with plankton nets and bag seines. Analysis of otoliths and length-frequency distributions
indicate that spawning took place from mid-August through late November with a major peak during October in 1981 and 1982.
Larvae became less abundant, but increased in size, from the mouth to the upper bay, indicating that spawning took place in
the bay mouth or nearshore waters. At about 8 mm SL (17 days old) larvae settled out along the bay shore before migrating
toward low salinity backwater areas. Juveniles grew to about 55 mm SL by the end of December and 303 mm SL by the end of their
first year. Young red drum gradually moved back into the bay with increased size and age. Eighty-five percent of larval stomachs,
examined were empty; those with food contained copepods almost exclusively. Fewer than 7% of juvenile stomachs were empty.
Small juveniles fed primarily on mysids, amphipods, and shrimp, whereas larger juveniles fed more on crabs and fish. Changes
in diet were noted with growth, but few differences were seen among areas or habitat types.
Laboratory experiments were conducted to separate the effect of predation from that of disturbance by grass shrimp, Palaemonetes pugio Holthuis, on the densities of benthic invertebrates from a salt marsh on Sapelo Island, Georgia, U.S.A. Blocks of marsh substratum (20 × 20 × 10 cm) and their associated natural invertebrate assemblages were exposed for 10 days to the following treatments: (1) intact adult grass shrimp (predation + disturbance), (2) adult shrimp which were inhibited from grasping prey by the excision of a dactyl from each chelate pereiopod (disturbance only), (3) no shrimp (control). Shrimp predation reduced the densities of nematodes, a burrowing anemone, Nematostella vectensis Stephenson, an ostracod, Cyprideis floridana (Howe & Hough), and a sabellid polychaete, Manayunkia aestuarina Bourne. There was some evidence (F-tests, P ≤ 0.07) to suspect that predation by Palaemonetes pugio also reduced densities of the tanaidacean, Hargeria rapax (Harger) and the polychaete, Capitella capitata (Fabricius). Hydrobiid snails were the only taxon to exhibit reduced densities as a result of disturbance by shrimp. Oligochaetes and the polychaetes, Nereis succinea (Frey and Leuckart) and Streblospio benedicti Webster were unaffected by the shrimp treatments in this experiment.
Grass shrimp, Palaemonetes pugío, were injected with 14C-labelled amino acids to determine hemolymph losses caused by an ectoparasite, the isopod Probopyrus pandalícola (Packard) (Epicaridea; Bopyridae). The female parasites were removed from labelled shrimp at intervals over 36 hr to monitor hemolymph ingestion. The parasites were found to feed discontinuously throughout the host's molt cycle, ingesting an average of 7–9 μl of hemolymph over a 24-hr period. Feeding was curtailed in darkness; probopyrids consumed only 2–3 μl of hemolymph after 12 hr in the dark. In all experiments, a number of parasites did not feed. The results of this study indicate that significant losses of the host's hemolymph result from the feeding activity of P. pandalicola. The determination of these losses is essential to begin testing the hypotheses that losses of hemolymph inhibit gonadogenesis in the host by either (i) creating a nutrient imbalance or (ii) depleting titers of reproductive hormones.
The present work studied the degree of inhibition caused by the bopyrid isopod Eophryxus lysmatae (Caroli, 1930 [Caroli, E., 1930. Notizia di tre specie nuove ed una poco nota di Bopiridi addominali, parassiti di Caridei del golfo di Napoli. (Contributo alla conoscenza del genere Phrixus Rathke). Boll. Soc. Nat. Napoli 41, 258–269]), an abdominal parasite, on the reproductive performance of its host, the protandric simultaneous hermaphrodite shrimp Lysmata seticaudata (Risso, 1816). Parasitized shrimp (PS) was not able to produce embryos, although they could successfully fertilise the eggs of unparasitized shrimp (US). All US paired with PS were able to fertilise eggs when paired with other US. The average number of larvae (±S.D.) produced by US shrimp paired with US and PS (344±27 and 346±23, respectively) was not significantly different (p=0.73). The average intermolt period duration (±S.D.) for US and PS (10±1.2 and 11±0.8 days, respectively) was not significantly different (p=0.82), with bopyrid parasites molting synchronously with their host. No PS lost its parasite during ecdysis. Although only three parasitized shrimp were used in the present work, parasitic castration induced by E. lysmatae seems to only affect the female sexual system of the simultaneous hermaphrodite L. seticaudata, and therefore parasite-induced “reproductive death” does not occur in this species as in other gonochoric and sequencial hermaphroditic caridean shrimp. Nutritional drain and disruption of endocrine mechanisms possibly caused by the bopyrid parasite are discussed.
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.
The smooth bay shrimp, Lissocrangon stylirostris, was sampled using a beach seine and a hyperbenthic sledge in the summer of 2006 at
a dissipative sandy beach in southern Oregon. We investigated possible variations in the population structure due to environmental
variables, preferred prey, sexual system employed, impacts due to parasitism by the bopyrid isopod Argeia pugettensis, and possible
predators. The population was 63% female, and females were generally larger than males. The density of L. stylirostris varied significantly
with the time of day. A cohort of small shrimp was observed from July to September while large adult shrimps were rare during the same
months. The net effect was that shrimp densities were stable over the summer. The shrimps fed mostly at night on the mysid Archaeomysis
grebnitzkii. The differences in female to male ratio, the larger size of females relative to males, and the relatively little overlap in size
frequency distribution between males and females could be because this species exhibits a type of protandry. Both male and female
shrimps supported an equal, high prevalence of, level of infestation by A. pugettensis (62%). The parasitized shrimps were larger in size
than normal shrimps but had lower weight per length ratio. Very few brooding shrimps were parasitized (0.2%), and a higher percentage of
parasitized shrimps had empty stomachs and significantly lower stomach contents. We hypothesize that the parasite is affecting the shrimp
by producing variation in its normal size and weight, sterilizing females, and reducing its ability to capture food. Finally, individuals of
English sole and Pacific staghorn sculpin individuals preyed on the shrimps.