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The effects of the parasite Probopyrus pandalicola (Packard, 1879) (Isopoda, Bopyridae) on the behavior, transparent camouflage, and predators of Palaemonetes pugio Holthuis, 1949 (Decapoda, Palaemonidae)

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... 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). ...
... Alternatively, some literature indicates that bopyrid isopods may not drive non-predative host mortality of grass shrimp, as the survival of the isopod is dependent on the survivorship of the shrimp (Finn and Buck, 2024). Bopyrid isopods appear to decrease the risk of their hosts being predated, possibly through shifts in shrimp behavior (Bass and Weis 1999;Brinton and Curran, 2015a;Finn and Buck, 2024). Additionally, there are systems in which the prevalence of parasitic castrators is high, and yet host populations are not particularly affected because hosts have co-evolved with their parasites. ...
... Similarly, altered behavior exhibited by infected grass shrimp may influence predator-prey dynamics, and thus ecological communities within salt marshes. For instance, parasitized grass shrimp have been found to exhibit decreased backward thrusting in the presence of a predator, mummichogs (Fundulus heteroclitus) while also making hosts more conspicuous to predators (visually the parasites diminish shrimp camouflage; Brinton and Curran, 2015a). It is important to note that although we explored the relationship between Pr. pandalicola parasite prevalence and grass shrimp size, we did not examine the possible relationship between the sex of grass shrimp and the developmental stage of the bopyrid parasite. ...
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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.
... In summary, we report here a reduction in host responsiveness and activity for bopyrid-infected prawns. Our findings are consistent with previous work showing that bopyrid infection can lead to decreased activity in their host (Bass & Weis 1999, McGrew & Hultgren 2011, Brinton & Curran 2015, Pascal et al. 2020) but, as far as we are aware, this is the first behavioural study carried out on Palaemon serratus infected by Bopyrus squillarum. For infected prawns, decreased responsiveness and activity could lead to increased predation (Brinton & Curran 2015) and reduced prey capture (Bass & Weis 1999), which in turn can affect P. serratus populations. ...
... Our findings are consistent with previous work showing that bopyrid infection can lead to decreased activity in their host (Bass & Weis 1999, McGrew & Hultgren 2011, Brinton & Curran 2015, Pascal et al. 2020) but, as far as we are aware, this is the first behavioural study carried out on Palaemon serratus infected by Bopyrus squillarum. For infected prawns, decreased responsiveness and activity could lead to increased predation (Brinton & Curran 2015) and reduced prey capture (Bass & Weis 1999), which in turn can affect P. serratus populations. Fluctuations in their populations could have wider implications on coastal ecosystems, as has previously been shown for other crustacean species (Pascal et al. 2020), particularly due to the important link provided by P. serratus between high and low trophic levels (Kelly et al. 2012). ...
... It is not surprising to observe these changes in host behaviour in response to bopyrid infection, due to probable fatigue caused by the major nutritional drain constituted by the feeding activity of the parasite (Bass & Weis 1999, McGrew & Hultgren 2011, Brinton & Curran 2015, Pascal et al. 2020. Differences in behaviour between infected and uninfected crustaceans have also been reported in other systems. ...
Article
Most bopyrid isopod parasites, which are crustaceans themselves, settle in the branchial chamber of decapod crustaceans and feed on host haemolymph. Here we report the results of an experiment on the common prawn Palaemon serratus and the parasite Bopyrus squillarum . Infected and uninfected prawns were stimulated with pokes of a plastic rod until an escape response was triggered; the number of pokes was recorded as an indicator of prawn responsiveness, whereas the time spent moving following stimulation was used as an indicator of prawn activity. Our results show that bopyrid infection affects both prawn responsiveness and activity, with infected prawns requiring more pokes to move, and moving for less time compared to uninfected prawns. In nature, such behavioural changes may impact defence mechanisms and survival of infected prawns. This could contribute to decreases in P. serratus abundance, thereby affecting the coastal ecosystems home to this species and the fisheries reliant on it, such as the Irish shrimp fishery.
... The bopyrid is a parasitic castrator that uses the shrimp as a final host in its complex (i.e., multi-host) life cycle. If the shrimp host is eaten by a predator, the bopyrid dies, so the parasite appears to decrease the likelihood of the host being consumed (Bass and Weis 1999;Brinton and Curran 2015b). In contrast, the trematode parasite uses the shrimp as a second intermediate host in its complex life cycle and has been shown to increase the likelihood of the host being consumed by a predator (Heard and Overstreet 1983;Gonzalez 2016). ...
... Grass shrimp primarily avoid predation by reducing activity and staying still when a predator is present. Thus, parasite-induced energy drain may reduce predation (Bass and Weis 1999;Kunz et al. 2006;Brinton and Curran 2015b). ...
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A conflict of interest occurs when parasites manipulate the behavior of their host in contradictory ways to achieve different goals. In grass shrimp (Palaemonetes pugio), trematode parasites that use shrimp as an intermediate host cause the shrimp to be more active than usual around predators, whereas bopyrid isopod parasites that use shrimp as a final host elicit the opposite response. Since these parasites are altering the host’s behavior in opposing directions, a conflict of interest would occur in co-infected shrimp. Natural selection should favor attempts to resolve this conflict through avoidance, killing, or sabotage. In a field survey of shrimp populations in four tidal creeks in the Cape Fear River, we found a significant negative association between the two parasites. Parasite abundance was negatively correlated in differently sized hosts, suggesting avoidance as a mechanism. Subsequent mortality experiments showed no evidence of early death of co-infected hosts. In behavior trials, co-infected shrimp did not show significantly different behavior from singly infected or uninfected shrimp, suggesting that neither parasite sabotages the manipulation of the other. Taken together, our results suggest that rather than sabotaging or killing one another, bopyrid and trematode parasites tend to infect differently sized hosts, thus avoiding a conflict and confirming the importance of testing assumptions in natural contexts.
... Parasite-host interactions can result in altered host behavior such as disorientation (Holmes and Bethel, 1972), increased conspicuousness (Holmes and Bethel, 1972;Bass and Weis, 1999;Brinton and Curran, 2015), and different activity levels (Holmes and Bethel, 1972;Bass and Weis, 1999;Kunz and Pung, 2004;Brinton and Curran, 2015). These alterations to host behavior can have cascading impacts on community structure (Mouritsen and Poulin, 2005). ...
... Parasite-host interactions can result in altered host behavior such as disorientation (Holmes and Bethel, 1972), increased conspicuousness (Holmes and Bethel, 1972;Bass and Weis, 1999;Brinton and Curran, 2015), and different activity levels (Holmes and Bethel, 1972;Bass and Weis, 1999;Kunz and Pung, 2004;Brinton and Curran, 2015). These alterations to host behavior can have cascading impacts on community structure (Mouritsen and Poulin, 2005). ...
Article
The daggerblade grass shrimp Palaemon pugio can be a host for many types of parasites including the microphallid trematode Microphallus turgidus and the haplosporidian hyperparasite Urosporidium crescens. Parasitic infection by trematodes can influence grass shrimp behaviors and may alter habitat selection. We conducted monthly sampling to determine the abundance, density, intensity, and prevalence of M. turgidus and U. crescens at two sites near Savannah, Georgia. The goals of this study were to determine which microhabitat type P. pugio frequented more often, either sandy substrates or rocks with the invasive and habitat altering red alga Agarophyton vermiculophyllum, which was present seasonally, and whether trematode infection corresponded to microhabitat usage. Additionally, we aimed to determine whether temporal changes in parasitic infection correlated to abiotic factors. The results indicated grass shrimp were more likely to be located over sand substrate, even when A. vermiculophyllum was present. Furthermore, the surveys did not detect a relationship between shrimp microhabitat usage and trematode abundance, density, or intensity. All analyzed measures of trematode and hyperparasite infection differed significantly among months with some instances of intraseasonal variation. A negative relationship was detected between salinity and trematode prevalence and mean abundance, but not with temperature. No relationship was observed between salinity or temperature and hyperparasite prevalence or mean abundance. Through consistent monthly sampling of a heterogeneous habitat containing a habitat-altering invasive species, this study supports previous findings that salinity plays a role in M. turgidus abundance within P. pugio and demonstrates that A. vermiculophyllum does not appear to influence host microhabitat preferences, regardless of trematode infection. However, salinity alone cannot account for all observed parasite patterns; thus, it is likely that a combination of fluctuating abiotic conditions, unaccounted for aspects of habitat structure, and the presence of other host species determines grass shrimp risk of parasite infection.
... Grass shrimp are easy to collect, handle, and maintain (Kunz et al., 2006) and have been used in many scientific studies (Welsh, 1975;Pung et al., 2002;Chaplin-Ebanks & Curran, 2007;Williamson et al., 2009;Partridge, 2010;Sherman & Curran, 2013, 2015Garcia et al., 2014;Brinton & Curran, 2015a). For example, Kunz et al. (2006) shrimp were observed to determine whether the behavior of the animal was altered by a parasite (Chaplin-Ebanks & Curran, 2005;Brinton, 2014;Brinton & Curran, 2015b), potentially increasing its susceptibility to predators (Brinton, 2014;Brinton & Curran, 2015b). Grass shrimp have also been used in K-12 activities to teach students about marine organisms and scientific research, because they are ideal organisms for young students to observe (Aultman & Curran, 2008;Aultman et al., 2010;Siler & Curran, 2011;Gunzburger & Curran, 2013;Gerido & Curran, 2014). ...
... Grass shrimp are easy to collect, handle, and maintain (Kunz et al., 2006) and have been used in many scientific studies (Welsh, 1975;Pung et al., 2002;Chaplin-Ebanks & Curran, 2007;Williamson et al., 2009;Partridge, 2010;Sherman & Curran, 2013, 2015Garcia et al., 2014;Brinton & Curran, 2015a). For example, Kunz et al. (2006) shrimp were observed to determine whether the behavior of the animal was altered by a parasite (Chaplin-Ebanks & Curran, 2005;Brinton, 2014;Brinton & Curran, 2015b), potentially increasing its susceptibility to predators (Brinton, 2014;Brinton & Curran, 2015b). Grass shrimp have also been used in K-12 activities to teach students about marine organisms and scientific research, because they are ideal organisms for young students to observe (Aultman & Curran, 2008;Aultman et al., 2010;Siler & Curran, 2011;Gunzburger & Curran, 2013;Gerido & Curran, 2014). ...
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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.
... Effects on the host are manifold and can be dramatic (Table 5.1). Van Wyk (1982), Calado et al. (2006), Hernáez et al. (2010) Castration McDermott (1991, González and Acuña (2004), Markham and Dworschak (2005), Sherman and Curran (2013) Feminization of males O'Brien and Van Wyk (1985), Markham and Dworschak (2005), Petrić et al. (2010), Romero-Rodríguez and Román-Contreras (2011), Yasuoka and Yusa (2017) Altered sexual characters of females Lee et al. (2016), Yasuoka and Yusa (2017) Gill damage and scar tissue development Bursey (1978), McDermott (1991), Corrêa et al. (2018) Reduced molt frequency Van Wyk (1982), O'Brien and Van Wyk (1985) (Unintended) mortality Anderson (1990) Increased predation risk Brinton and Curran (2015) Lower activity levels Bass and Weis (1999), McGrew and Hultgren (2011) Lower oxygen consumption Anderson (1975), Neves et al. (2000) Different host sex ratios Somers and Kirkwood (1991), McDermott (2002), Cericola and Williams (2015) Sources are not comprehensive A. A. Klompmaker et al. The body fossil record of epicarideans is nearly nonexistent. ...
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The fossil record of crustaceans as hosts of parasites has yielded three confirmed associations: swellings on Jurassic–Pleistocene decapods attributed to epicaridean isopods, feminization of Cretaceous and Miocene crabs possibly caused by rhizocephalan barnacles, and presumed pentastomids on/in Silurian ostracods. Cestode platyhelminth hooks and swellings by entoniscid isopods have yet to be recognized. Relative to 2014, we report a 45% increase to 128 fossil decapod species with swellings (ichnotaxon Kanthyloma crusta) in the branchial chamber attributed to epicarideans. Furthermore, using a Late Jurassic decapod assemblage from Austria, we find (1) no correlation between genus abundance and prevalence of K. crusta, (2) host preference for some galatheoids (as for a mid-Cretaceous assemblage from Spain), and (3) a larger median size of parasitized versus non-parasitized specimens for two abundant species. The latter result may be caused by infestation throughout ontogeny rather than exclusively in juveniles and/or possible selection for larger individuals.
... These authors concluded that the alterations were consistent with the ingestion of the branchial tissue by P. bithynis, which would have a negative impact on the respiratory capacity of the host. Infestation by Probopyrus females may also induce the castration of the host, the feminization of the males (Beck, 1980), reduction of the development of the nutritional conditions of the host (de Barros et al., 2021), and even predator−prey interactions, through the reduction in the capacity of the host to camouflage itself, leaving it more susceptible to predation (Brinton and Curran, 2015b). ...
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Bopyrid isopods of the genus Probopyrus are well-known parasites of freshwater prawns of the genus Macrobrachium. The parasitism of coastal populations of Macrobrachium amazonicum by Probopyrus bithynis, for example, has been documented since the late 1980s. Despite this, molecular data on different populations are not available for any Probopyrus species. The present study is the first to describe Probopyrus populations from distinct regions of the Amazon basin based on sequences of two genes, the mitochondrial cytochrome oxidase C subunit I (COI) and the nuclear 18S ribosomal DNA (18S rDNA) gene. The analyses indicated the presence of two Probopyrus species, each parasitizing either the coastal or the inland populations of M. amazonicum. The results indicated the potential use of the COI barcode for the identification of Probopyrus species. We discuss the potential implications of the findings for the taxonomy of Probopyrus bithynis and other species of the genus Probopyrus.
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Parasites can kill hosts directly, but also indirectly, by enhancing susceptibility to environmental factors and biotic interactions. In the United States South Atlantic Bight region of the northwest Atlantic Ocean, white shrimp (Penaeus setiferus) support a substantial commercial fishery and are also valuable prey for many marine and estuarine species. Since the late 1990s, a condition known as black gill has been observed in penaeid shrimp in the South Atlantic Bight. In this region, black gill has been linked to an apostome ciliate that elicits an innate immune response in shrimp, manifested through the melanization of gill tissues, which impedes respiratory functions and hemolymph ion regulation. The objective of this study was to determine if black gill subjects shrimp to higher rates of predation by red drum (Sciaenops ocellatus), spotted seatrout (Cynoscion nebulosus), and blue crab (Callinectes sapidus). A series of simultaneous prey choice mesocosm experiments was conducted, during which single-species predators were able to consume shrimp that were both symptomatic and asymptomatic of black gill over a four-hour period. Predator species were 1.4 to 3.0 times more likely to consume symptomatic shrimp than asymptomatic shrimp. The hinderance of shrimp physiology and escape responses due to gill melanization likely increases the vulnerability of shrimp to predation. This study emphasizes that mortality from parasitic infections is not always direct and that black gill may have a significant impact on penaeid shrimp through secondary, or indirect, mortality.
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Two species of bopyrid isopods of the Bopyrinae subfamily are recorded from new localities and hosts in northeastern Brazil. Parabopyrella lata (Nierstrasz and Brender à Brandis, 1929) was recorded from the state of Ceará, found for the first time parasitising the caridean shrimp Alpheus packardii Kingsley, 1880. In addition, Probopyrus cf. pandalicola (Packard, 1879) is recorded from the state of Bahia, parasitising the palaemonid shrimp Palaemon northropi (Rankin, 1898). Taxonomic comments are provided for each species.
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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.
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Parasites that are transmitted from prey to predator are often associated with altered prey behavior. Although many concur that behavior modification is a parasite strategy that facilitates transmission by making parasitized prey easier for predators to capture, there is little evidence from field experiments. We observed that conspicuous behaviors exhibited by killifish (Fundulus parvipinnis) were associated with parasitism by larval trematodes. A field experiment indicated that parasitized fish were substantially more susceptible to predation by final host birds. These results support the behavior-modification hypothesis and emphasize the importance of parasites for predator-prey interactions.
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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.
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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.
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Densities of the small, surface-dwelling invertebrates which make up most of the benthic community (Manayunkia aestuarina, Streblospio benedicti, Leptochelia rapax, ostracods, hydrobiid snails, and Gemma gemma) were highest in enclosures containing large fish, and lowest in closed controls and in enclosures containing small fish. Intermediate invertebrate densities occurred in enclosures containing medium-size mummichogs. The effects of fish size were enhanced at high fish densities (2-4 fish/m2), although fish density alone had little effect on invertebrate abundance. Small epibenthic predators-disturbers like the grass shrimp, Palaemonetes pugio, were commonly observed in the experimental enclosures. The gut contents of fish taken from the enclosures indicated that the shrimp were ingested only by medium and large size-classes of mummichog. Infaunal densities probably increased in response to the control of small epibenthic predator-disturbers (ie. P. pugio) by the larger F. heteroclitus. -from Authors
Article
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.
Article
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.
Article
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.
Article
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.
Article
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.
Article
Swimming responses of Probopyrus pandalicola (Packard) cryptoniscus larvae to water solutions either conditioned or unconditioned by hosts were determined using a simple Y-tube choice apparatus. Results document that larvae swim at random or downstream with respect to water current in unconditioned control solutions. In the presence of either “crude extract” or “host-metabolite” solution, prepared using definitive hosts Palaemonetes pugio (Holthuis), cryptonisci are strongly rheopositive. However, upstream swimming cryptonisci swam toward the source of the host-conditioned water (i.e., made the correct ‘choice’) only when it was rather concentrated; when ‘host-metabolite’ solution was employed, rheopositive parasite larvae swam toward control solution as frequently as toward the experimental solution. We conclude that distance chemoreception may play a role in host finding by P. pandalicola.
Article
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.
Article
Larven von Probopyrus pandalicola, einer die ästuarine Garnele Palaemonetes pugio parasitierenden Art der Isopodenfamilie Bopyridae, wurden im Labor gezüchtet. Obwohl verschiedene Arten ästuariner Copepoden frei schwimmenden Larven des Parasiten ausgesetzt wurden, hat sich Acartia tonsa als die einzige, regional häufig vorkommende Copepoden-Art erwiesen, die von P. pandalicola als Zwischenwirt angenommen wurde. Licht- und Rasterelektronenmikroskopie wurden eingesetzt, um die beobachteten Larvenstadien eingehend zu beschreiben: Epicaridium, Microniscus sofort und später nach der Häutung sowie Cryptoniscus. Es wurde beobachtet, daß zwar die Transformation vom Epicaridium- zum Microniscus-Stadium durch eine Häutung geschieht, daß aber die Weiterentwicklung zum Cryptoniscus-Stadium ohne Unterbrechung durch eine erneute Häutung erfolgt. Die Entwicklung zum Cryptoniscus-Stadium dauert 6-8 Tage vom Moment des Befalls des Copepoden.
Article
La localisation des larves et des adultes de Probopyrus pandalicola sur Palaemonetes puludosus est décrite. L'Isopode femelle se trouvait en position oblique dans la chambre branchiale de la crevette, avec la tête en position postéro-dorsale par rapport à l'hôte, sans préférence pour l'un des côtés de celui-ci. Le minuscule mâle était généralement attaché entre les pléopodes de la femelle parasite. Cependant, certains mâles étaient attachés aux branchies de la crevette, et dans quelques cas il y avait des mâles surnuméraires. Les Isopodes larvaires étaient localisés sur l'abdomen et dans la chambre incubatrice de la femelle parasite et, sur la crevette, en arrière des antennes jusqu'au telson.
Article
The grass shrimp Palaemonetes pugio, a common inhabitant of brackish water marshes, is often used in experimental studies. To support studies concerned with the behavior of P. pugio in controlled laboratory conditions, a behavior catalog (or ethogram) was developed. Twelve grass shrimp activities, six moving and six stationary, were observed and described. The most frequently observed activities included hovering in the water column, walking and three types of swimming. Activities observed less often included backward thrusting, jabbing with the rostrum tip and taking cover. The value of the ethogram was assessed using a predator-prey experiment in which the frequency of grass shrimp behaviors in response the predatory fish Fundulus heteroclitus was examined. In the presence of a fish, grass shrimp decreased the frequency of swimming and increased the frequency of covered and motionless behaviors. We also noted a significant increase in the occurrence of two active antipredator defenses: backward thrust and jabbing with the rostrum tip. Backward thrust quickly propelled shrimp away from a fish. Jabbing with the rostrum tip was directed toward an advancing fish and usually caused the fish to swim off in the opposite direction. These observations provide clues as to the levels and types of interactions that occur between the grass shrimp and their fish predators in the wild. The catalog of recorded activities may be of value in future studies designed to examine the effect of different experimental conditions on grass shrimp behavior.
Article
Predation by visual predators is often affected by light conditions and may therefore exhibit strong diel variation. The dominant predators on grass shrimp, Palaemonetes pugio, are finfish predators that are thought to locate their prey by visual cues. We examined the response of grass shrimp to diel variation in predation risk in the nearshore shallow waters of the Chesapeake Bay. We used diel shoreline seines to assess the relative abundance of predators. We assessed the relative risk of predation with shrimp tethered at refuge (30 cm) and nonrefuge (60 cm) depths. To measure grass shrimp response to predation risk, we used dipnets to monitor habitat use. Four predominantly visual predators dominated the shoreline seine catches, Fundulus heteroclitus, Micropogonias undulatus, Morone americana and Morone saxatilis. Total predator abundance had a diel component, with dramatic nighttime decreases in total abundance, whereas guild composition and relative abundance remained unchanged. Relative predation risk for tethered shrimp exhibited significant time by habitat interaction. During the day, depth negatively affected survivorship of tethered shrimp while at night overall survivorship increased and there was no effect of depth. Shrimp habitats use reflected diel predation risks. Abundances in the near shore were highest during the day with decreased abundances at night. Together, the seine and tethering data highlight the importance for a refuge (e.g., shallow water) from predation during the daytime and a relaxation of predation pressure at night.
Article
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.
Article
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.
Article
Analysis of prey capture ability of mummichogs, Fundulus heteroclitus (L.) from a mercury-polluted tidal creek compared with conspecifics from an uncontaminated environment showed that the latter captured the prey organism Palaemonetes pugio Holthuis at a significantly faster rate and had significantly lower levels of mercury in their brain tissues. Exposure of uncontaminated fish to conditions similar to those of the polluted creek caused both a reduction in their prey capture rate and an increase in brain mercury to levels similar to those of fish native to the creek. Polluted fish maintained in the laboratory for extended periods failed to show either an increase in prey capture rate or a decrease in their levels of brain mercury. Size-selective predation on grass shrimp was observed among mummichogs from both sites, but did not appear to vary between sites. Videotape analysis of predatory behavior showed that fish from the polluted creek made significantly fewer attempts to capture prey. Fish from the polluted environment suffered significantly greater mortality in the presence of a predator, the blue crab Callinectes sapidus Rathbun, than fish from the unpolluted environment.
Article
In this laboratory study, the frequency of locomotor behaviors for two grass shrimp species, Palaemonetes pugio and Palaemonetes vulgaris, and the killifish Fundulus heteroclitus were determined. Additional behaviors, such as grouping of grass shrimp, and pursuit by killifish, the grass shrimp's common predator, were also analyzed. The results show that mean behavioral frequencies for the two shrimp species were rarely significantly different statistically. Each shrimp species altered its behavior differently in the presence of the other shrimp species, but responded similarly to the presence of the predator. The results indicate that the response of each shrimp species to the predator was dependent upon the predator's size and health. In situations involving the large health predator, both grass shrimp species significantly reduced swimming, but did not show a significant difference in walking. Behavioral frequencies of large and small healthy killifish were not significantly different from each other when alone, but were significantly different in the presence of prey, while the large unhealthy killifish's behavior was significantly decreased in all situations compared to both the large and small health killifish.
Article
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.
Article
Abstract1.Standard metabolic rates for Palaemonetes pugio and P. pugio parasitized by the epicaridean isopod Probopyrus pandalicola were measured using manometric techniques.2.Results in most instances show lower rates of oxygen consumption for infected shrimp than for control shrimp of equal size. This effect is generally most pronounced in the smallest sized hosts.3.It is suggested that the observed results may reflect changes in lipid metabolism as a host response to parasitism.4.The marked degree of metabolic temperature independence of P. pugio is not significantly altered as a result of parasitism.
Article
Any animal whose form or behavior facilitates the avoidance of predators or escape when attacked by predators will have a greater probability of surviving to breed and therefore greater probability of producing offspring (i.e., fitness). Although in theory the fitness consequences of any antipredation behavior can simply be measured by the resultant probability of survival or death, determining the functional significance of antipredation behavior presents a surprising problem. In this review we draw attention to the problem that fitness consequences of antipredation behaviors cannot be determined without considering the potential for reduction of predation risk, or increased reproductive output, through other compensatory behaviors than the behaviors under study. We believe we have reached the limits of what we can ever understand about the ecological effects of antipredation behavior from empirical studies that simply correlate a single behavior with an apparent fitness consequence. Future empirical studies must involve many behaviors to consider the range of potential compensation to predation risk. This is because antipredation behaviors are a composite of many behaviors that an animal can adjust to accomplish its ends. We show that observed variation in antipredation behavior does not have to reflect fitness and we demonstrate that few studies can draw unambiguous conclusions about the fitness consequences of antipredation behavior. Lastly, we provide suggestions of how future research should best be targeted so that, even in the absence of death rates or changes in reproductive output, reasonable inferences of the fitness consequences of antipredation behaviors can be made. Copyright 2005.
Article
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Article
Changes in host behaviour following infection with parasites are frequently reported in the literature, and are often hypothesized to be adaptive for either host or parasite. However, investigators of such phenomena often use the "adaptation" label for host behavioural changes based on their intuition and not on rigorous criteria. Alterations in host behaviour following infection can only be considered adaptive if they satisfy certain conditions: (1) they must be complex; (2) they must show signs of a purposive design; (3) they are more likely to be adaptations if they have arisen independently in several lineages of hosts or parasites; and (4) they must be shown to increase the fitness of either the host or the parasite. A survey of published examples of host behavioural changes indicates that while some are spectacularly complex and are extremely well-fitted to their presumed function, most are simple increases or decreases in an activity performed prior to infection. There are some suggestions of convergent evolution in behavioural change in distantly related host or parasite groups but more evidence is needed. Finally, most known behavioural changes have not been demonstrated to lead to fitness gains in either hosts or parasites. Few known examples satisfy more than two of the above criteria, and, in general, the adaptive function of changes in host behaviour following infection is in need of more solid proof.
Article
The effect of the trematode Microphallus turgidus on its second intermediate host, the grass shrimp, Palaemonetes pugio, was tested. To do so, we measured the susceptibility of infected and uninfected shrimp to predation by the mummichog, Fundulus heteroclitus. Shrimp behavior was compared in the presence and absence of a fish predator, and the swimming stamina and backthrust escape responses of infected and uninfected shrimp were measured. Infected shrimp were more likely to be eaten by a predator than uninfected shrimp, had lower swimming stamina, and spent more time swimming and less time motionless in the presence of a predator. There was no difference between backthrust distances traveled in response to a stimulus by either infected or uninfected shrimp. Thus, M. turgidus may increase the predation of P. pugio in the wild, possibly by affecting the swimming stamina and predator avoidance responses of the shrimp.
Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Gulf of Mexico) -grass shrimp
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The effect of the isopod parasite Probopyrus pandalicola (Packard, 1879) on the predation and gravidity of the daggerblade grass shrimp Palaemonetes pugio Holthuis
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The effects of coded wire tags and the isopod parasite Probopyrus pandalicola on the growth and predation of daggerblade grass shrimp Palaemonetes pugio Holthuis
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Behavioral effects of the parasite Probopyrus pandalicola on the swimming endurance and toxicity of fipronil to the daggerblade grass shrimp Palaemonetes pugio, and integrating shrimp density data into a K-12 activity
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