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The effect of the parasitic isopod, Probopyrus pandalicola (Packard, 1879), on tidal activity patterns of the grass shrimp, Palaemonetes pugio Holthuis, 1949
Abstract
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.
... lakes and rivers) (Jiménez & Vargas, 1990;Jayasree et al., 2001;Chinabut, 2002). They are rarely found under aquaculture conditions but are common in the wild among freshwater organisms with genus Macrobrachium as their definitive hosts (Chaplin-Ebanks & Curran, 2005). ...
Introduction:
Macrobrachium amazonicum is widely distributed in South America, occurring in the Orinoco, Amazon and Paraguay river basins, being used as an important source of protein for feeding riverside populations. This prawn is host to the crustacean ectoparasites Probopyrus pandalicola, Probopyrus floridensis and Probopyrus bithynis (Bopyridae) that infest the gill cavity of the species.
Objective:
To report the prevalence and abundance of ectopasites (P. pandalicola, P. floridensis and P. bithynis) and the condition factor in M. amazonicum from the Amazon River, Eastern Amazon.
Methods:
The prawns were collected from May 2017 to April 2018, with the artisanal trap matapi in the municipalities of Mazagão (state of Amapá) and Santarém (state of Pará), Brazil.
Results:
216 prawns infected with ectoparasites were captured, 133 in the Mazagão region (53 P. pandalicola, 48 P. bithynis and 32 P. floridensis) and 83 in the Santarém region (45 P. pandalicola and 38 P. bithynis). In Mazagão, the highest prevalence values were recorded in May (1.98 %) for P. floridensis, July (2.18 %) for P. bithynis, and March (1.93 %) for P. pandalicola. In the Santarém region, the highest prevalence values were recorded in February, 3.47 for P. pandalicola and 2.89 for P. bithynis. Regarding the abundance of parasites, there was no difference between the species grouped between the regions (t = 0.32, p = 0.739). Parasitized prawns from Mazagão and Santarém presented condition factors below expectations, with an average of 0.85 ± 0.55 for Santarém and 0.88 ± 0.44 for Mazagão.
Conclusions:
During the study it was found that P. pandalicola, P. bithynis and P. floridensis were present in M. amazonicum throughout the year. Furthermore, there was an effect of parasitism on M. amazonicum in the study areas.
... The branchial chamber of parasitized M. stridulans developed a characteristic bulge. This bulge increases the pressure on the gills and reduces the respiratory efficiency of the host (Chaplin-Ebanks et al., 2005). Although such infestation does not immediately cause death, it is likely that the natural growth of the hosts is affected to some extent, leading to economic losses in commercial species. ...
We collected 3 596 Metapenaeopsis stridulans (Decapoda: Penaeidae) from the southeast coast of India between January and December 2007. Sixty three specimens (43 females and 18 males) were parasitized by the bopyrid isopod Epipenaeon ingens (Isopoda: Bopyridae). This is the first report of the occurrence of E. ingens in this host; therefore, it was considered as a new host record. The highest level of infestation (3.2%) occurred in October 2007, coincident with observations of gravid females (9). The total prevalence and presence of gravid females were 17.46% and 28%, respectively. Infestation caused a characteristic bulge of the branchial chamber, growth retardation, and degeneration of the sex organs, but had no effect on the host weight.
... Clearly E. ingens exhibits stenoxenic parasitic specificity. The level of-Ebanks et al., 2005). Although such infestation does not immediately cause death, it is likely that the natural growth of the hosts is affected to some extent, leading to economic losses in commercial species. ...
We collected 3 596 Metapenaeopsis stridulans (Decapoda: Penaeidae) from the southeast coast of India between January and December 2007. Sixty three specimens (43 females
and 18 males) were parasitized by the bopyrid isopod Epipenaeon ingens (Isopoda: Bopyridae). This is the first report of the occurrence of E. ingens in this host; therefore, it was considered as a new host record. The highest level of infestation (3.2%) occurred in October
2007, coincident with observations of gravid females (9). The total prevalence and presence of gravid females were 17.46%
and 28%, respectively. Infestation caused a characteristic bulge of the branchial chamber, growth retardation, and degeneration
of the sex organs, but had no effect on the host weight.
KeywordBopyridae–Penaeidae–parasitism–shrimp–India
... The branchial chamber of parasitized P. stylifera developed a characteristic bulge. E. ingens bringing pressure on the host gills reduced the respiratory efficiency of the shrimp (Chaplin-Ebanks and Curran, 2005). It was collected a male shrimp measuring 8.9 cm with a female like rostrum.The infested shrimp showed degenerate primary and secondary sexual organs. ...
Epipenaeon ingens (Isopoda: Bopyridae) is reported for the first time from Parapenaeopsis stylifera (Decapoda: Penaeidae) in South India. According to the month the parasitic prevalence ranged from 0.0 to 2.9%. A characteristic bulge of the branchial chamber growth retardation and degenerated sex organs were observed in the infested shrimp.
... [10] It is estimated that approximately 3% of a population of P. pugio may become parasitized. [11] This parasite forms a large protrusion on the carapace of P. pugio that may possibly hinder the ability of the shrimp to feed and avoid predation by decreasing its energy level and reducing activity; [12] however, Chaplin-Ebanks and Curran [13] found no change in activity patterns as a result of the isopod. In addition, Probopyrus pandalicola causes both male and female P. pugio to become sexually sterile. ...
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).
... Probopyrus pandalicola prevents shrimp reproduction (Pike, 1960) and reduces shrimp respiration and metabolism (Anderson, 1972). Bass and Weiss (1999) duces the activity level of grass shrimp during the first 24 hr after feeding; however, we found no statistically significant effect of the bopyrid on activity levels of grass shrimp in a laboratory setting during which we controlled for the effects of both light and tidal stage, which did influence behavior (Chaplin-Ebanks and Curran, 2005). Shrimp parasitized by bopyrids are removed from the reproductive population because both males and females are sexually sterile, and males are feminized by reduced chelae length (Pike, 1960;Anderson, 1972). ...
The grass shrimp, Palaemonetes pugio, is an important food source for many invertebrate and fish species, including several of commercial importance. The bopyrid Probopyrus pandalicola prevents reproduction in P. pugio by sexual sterilization. The purpose of our research was to determine bopyrid prevalence in grass shrimp over the course of a year. Shrimp were collected from 2 estuarine systems in South Carolina and 2 estuarine systems in Georgia and examined for parasite presence, sex, and gravidity. Site-specific monthly prevalence ranged from 0 to 6.3%. Country Club Creek had the maximum mean +/- SE prevalence of 3.1 +/- 0.3%, and Harbour Town had the minimum of 1.3 +/- 0.3%. Maximum prevalence was concurrent with peak gravidity for Moon River; thus, at this site the negative effect of this parasite on reproductive output may be greater. Reduced egg production may affect grass shrimp abundance and ultimately the recruitment success of its predators.
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.
Although parasites represent a substantial part of marine communities’ biomass and diversity, their influence on ecosystem functioning, especially via the modification of host behaviour, remains largely unknown. Here, we explored the effects of the bopyrid ectoparasite Gyge branchialis on the engineering activities of the thalassinid crustacean Upogebia pusilla and the cascading effects on intertidal ecosystem processes (e.g. sediment bioturbation) and functions (e.g. nutrient regeneration).
Laboratory experiments revealed that the overall activity level of parasitized mud shrimp is reduced by a factor 3.3 due to a decrease in time allocated to burrowing and ventilating activities (by factors 1.9 and 2.9, respectively).
Decrease in activity level led to strong reductions of bioturbation rates and biogeochemical fluxes at the sediment–water interface.
Given the world‐wide distribution of mud shrimp and their key role in biogeochemical processes, parasite‐mediated alteration of their engineering behaviour has undoubtedly broad ecological impacts on marine coastal systems functioning.
Our results illustrate further the need to consider host–parasite interactions (including trait‐mediated indirect effects) when assessing the contribution of species to ecosystem properties, functions and services.
The behaviour of the Atlantic stingray (Dasyatis sabina) is affected by environmental cues, including time of day and tide. The purpose of the present study was to determine whether these cycles and differences in creek geomorphology affected presence and movement patterns of Atlantic stingrays near Savannah, GA, USA. Forty-five stingrays were tagged with Vemco coded-acoustic transmitters and passively tracked in two creek systems between December 2012 and December 2014. The geomorphology of the creeks was classified using the Horton stream-order concept, with the smallest tributaries assigned to the first order. Stingrays moved most at dusk (0.26 ± 0.09 movements day–1), followed by night (0.23 ± 0.09 movements day–1). Stingrays were found in deeper water during the cold season than during the warm season. Patterns in creek usage across tidal stages were nearly consistent across seasons. However, the diel pattern varied; stingrays utilised all creek orders throughout the diel cycle in the warm seasons, but entered only shallow creeks during the day in the cold season. Because presence and movements of stingrays were affected by tidal and diel cycles, these environmental factors could also affect their foraging patterns and their influence as an ecosystem engineer.
Mapping the global distribution of Probopyrus pandalicola (bopyrid parasite) and the distributions of its potential hosts.
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.
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.
Epipenaeon ingens occurs most commonly in
Southeast Coast of India parasitized the penaeid shrimp.
The present study provides the prevalence, morphological
and molecular characterisation of E. ingens collected from
the host Metapenaeopsis stridulans. In the present study
highlights the significance of high prevalence and genetic
diversity of E. ingens in M. stridulans. Intra specific analysis
also revealed that E. ingens species detected in the
present study can be easily distinguished from the other
genospecies of bopyrids. Further application of this molecular
tool to investigate the genetic variability among
bopyrids detected in different hosts may facilitate our understanding
of the significance of genetic diversity in relation
to the infestation of bopyrid species in south coast of
India.
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.
In developing a useful tool to detect parasitic dynamics in an estuarine ecosystem, a denaturing high-performance liquid chromatography (DHPLC) assay was optimized by cloning plasmid DNA from the grass shrimp Palaemonetes pugio, and its two parasites, the trematode Microphallus turgidus and bopyrid isopod Probopyrus pandalicola. The optimal separation condition was an oven temperature of and 62-68% of buffer B gradient at a flow rate of 0.45 mL/min. A peptide nucleic acid blocking probe was designed to clamp the amplification of the host gene, which increased the amplification efficiency of genes with low copy numbers. Using the DHPLC assay with wild-type genomic, the assay could detect GC Gram positive bacteria and the bopyrid isopod (P. pandalicola). Therefore, the DHPLC assay is an effective tool for surveying parasitic dynamics in an estuarine ecosystem.
A bopyrid isopod was found attached in the gill chamber of a wild giant freshwater prawn, Macrobrachium rosenbergii (De Man, 1879) from the Timun River, Negeri Sembilan (Malaysia) (2°28′N 102°02′E), with a prevalence of 0.27% (2/743). The specimens measured 18.25 ± 0.35 mm in length and 15.25±0.35 mm in width. The body of the isopod was subcordate and slightly distorted. It has five oostegites, with black pigment. The first oostegites are large, the 2 nd and 3 rd are suboval and smaller, while the 4 th and 5 th are long and ending in sharp points. Both specimens were identified as adult female Probopyrus buitendijki (Horst, 1910). The isopod was found only in January of 2009 and 2010, which months recorded a relatively low rainfall. A histopathological study of the infected gill showed impairment of the gill filaments, necrosis, and hyperplasia. Such effects may reduce the respiration efficiency of the gills. Un isopode Bopyridae a été trouvé fixé dans la chambre branchiale de la crevette géante d'eau douce, Macrobrachium rosenbergii (De Man, 1879) de la rivière Timun, Negeri Sembilan (Malaisie) (2°28′N 102°02′E), avec une prévalence de 0.27% (2/743). L'isopode mesurait 18,25 ± 0,35 mm de long et 15,25 ± 0,35 mm de large. Le corps de l'isopode était subcordiforme et légèrement déformé. Il possède cinq oostégites, avec un pigment noir. Les premières oostégites sont de grande taille, les 2èmes et 3èmes sont de forme subovale et plus petites, tandis que les 4èmes et 5èmes sont longues et terminées en pointes aigües. Les spécimens ont été identifiés comme des femelles adultes de Probopyrus buitendijki (Horst, 1910). L'isopode a été trouvé seulement en janvier 2009 et 2010, mois présentant des précipitations relativement basses. Une étude histopathologique de la branchie infectée s'a révélé une détérioration des filaments branchiaux, une nécrose et une hyperplasie. De tels effets pourraient réduire l'efficacité de la respiration des branchies.
Female blue crabs (Callinectes sapidus Rathbun) with mature embryos have a spawning migration in which they: (1) undergo ebb-tide transport for movement seaward from estuaries, (2) release their larvae, and (3) reverse direction by undergoing flood-tide transport for up-estuary movement. The study determined whether ebb-tide transport during the spawning migration is based upon an endogenous rhythm in vertical migration. Under constant conditions in a rectangular container, which limited horizontal and vertical movements, females with young and mature embryos had circatidal rhythms (periods=12.11-12.95 h) in migratory restlessness (swimming activity) and egg maintenance behavior (abdominal pumping). However, the rhythms were out of phase, as migratory restlessness occurred during the expected time of ebb tide in the field, and egg maintenance behavior, during the time of flood tide. Under constant conditions in vertical columns (1.32 m high), crabs with mature embryos had a circatidal rhythm (periods=12.2-13.7 h) in which they had frequent bouts of swimming to the surface of the column during the expected time of ebb tide in the field and remained on the bottom during the time of flood tide. This rhythm was not present in crabs with young embryos and disappeared after larval release. Thus, an endogenous rhythm in vertical migration does underlie the ebb-tide transport behavior of ovigerous blue crabs with mature embryos during their spawning migration.
Small (5–10.9 mm carapace length), medium (11–15.9 mm), and large (16–20.9 mm) juveniles of Metapenaeus anchistus, Metapenaeus sp., Penaeus monodon and P. merguiensis were stocked individually in glass tanks provided with sand substrate, sea water, artificial bamboo shelter, aeration and food. The seven activity types (recorded for each shrimp hourly for 24 h) were classified as below (burrowing) or above substrate (swimming, walking, stationary, in shelter, feeding and cleaning). Shrimp juveniles exhibited a strong diel periodicity — emergence and activity at night and burrowing in the day. The chi-square test showed that type of activity (above/below substrate) was associated with period (light/dark). Diurnal burrowing was greater among Metapenaeus than Penaeus; inversely, above substrate activities were more frequent for Penaeus species compared to Metapenaeus. Feeding was the major above substrate and nocturnal activity for M. anchistus, Metapenaeus sp. and P. monodon. Only P. Monodon used the shelter consistently. Frequency of the 7 activity types was dependent on juvenile size for Penaeus, e.g., the preference for shelters shifted to burrowing with increase in size in P. monodon. Results are discussed in relation to the importance of mangrove habitats in providing shelter to penaeids, in particular the mangrove-associated P. monodon and P. merguiensis.
1. Spontaneous locomotory activity was recorded continuously for several days in Carcinus maenas (L.).
2. A complex rhythm was observed which could be analysed into two components, one of diurnal frequency (24 hr.), with peaks of activity during the hours of darkness, and one of tidal frequency (ca. 12.4hr.), with peaks at the time of high tide.
3. The rhythms persist in constant dim light at constant temperatures, whether the crabs are kept moist in air or continuously immersed in sea water.
4. The resultant effect of the two rhythms is to produce particularly high activity peaks during periods which recur with a semi-lunar frequency.
5. Experimental results relate to observed behaviour on the shore.
A rhythm of tidal (12.4 h) frequency with activity maxima during the early ebb was observed in the swimming activity of Corophium volutator (Pallas), collected intertidally and kept under constant conditions in the laboratory. This rhythm persists for about 3 days. It is independent of temperature changes within the range of those encountered on the shore during different stages of the tide. Corophium collected from generally non-tidal brackish pools at Oxwich were arhythmic, indicating that diurnal variations in light intensity are not responsible for the entrainment of the rhythm. Corophium collected from M.H.W.S. and M.L.W.S. tide levels showed synchronous activity peaks, which that the rhythm is not phased to the times at which the animals are covered or exposed by the tide. Rhythmic swimming activity, phased to the tides in the usual way, was induced in arhythmic laboratory Corophium by returning them to the shore or shallow sublittoral in containers covered with boulting cloth. Others kept in containers floating from a buoy did not develop this typical response. This indicates that tidal changes in hydrostatic pressure, rather than variations in intensity of wave action of water currents, may be responsible for entrainment of the rhythm. Corophium collected intertidally generally responded in the laboratory to cyclical pressure changes of 20 min frequency, by swimming more actively following a pressure decrease. This response cannot be depth-regulatory, being opposite in sense. On the other hand, Corophium collected from generally tideless pools at Oxwich showed a depth-regulatory response to pressure changes. Corophium collected intertidally and subjected to cyclical pressure changes of tidal amplitude and frequency, but opposite in phase to the naturally occurring tides, rapidly came into phase with this artificial cycle. It therefore seems that the rhythm of activity is probably entrained by the decrease in pressure as the tide ebbs. Field observations indicate that, although Corophium may be induced to leave the mud by the incoming tide, they do not swim for long before seeking the bottom again, and that still greater numbers swim during the ebb tide.
The nursery function of mangroves as shelter has been postulated to explain the positive correlation between shrimp catches and mangrove area. This study was undertaken to document shelter use and other activities in mangrove‐associated penaeids and to determine diel and size differences relating to these activities. Juvenile Metapenaeus ensis, Penaeus latisulcatus and P. merguiensis collected from mangrove areas in Guimaras, central Philippines and stocked individually in glass tanks (= replicates) provided with artificial shelters and sand substrate were observed every hour for 25 h. Size classes tested were very small (1–5.9 mm carapace length); small (6–10.9mm CL); medium (11–15.9mm CL); large (16–20.9mm CL); and very large (21–25.9 mm CL). Due to limited juvenile supply, only 3 sizes were tested for each species: P. merguiensis (very small to medium), M. ensis (small to large) and P. latisulcatus (medium to very large) with 5 replicate animals (one per tank) per size. Juvenile M. ensis and P. latisulcatus showed a strong diel periodicity of daytime burial and nocturnal activity. In contrast, P. merguiensis showed active swimming and feeding throughout the day and night. Very small to small P. merguiensis were observed on the shelters, but burying was exhibited only by a few medium‐sized juveniles. This shelter use is consistent with observations of small P. merguiensis entering the mangrove forest (where roots, twigs, etc. contribute to structural complexity) on the flood tide and concentrating in the shallow, turbid waters of adjoining creeks during ebb tide and slack water.
Parasites and related symbionts of marine and estuarine hosts of the northern Gulf of Mexico are described in this guidebook. It is meant primarily to serve as a teaching aid for the novice student, but it also contains more technical aspects for the experienced parasitologist. Forms and examples of symbiosis are explained in an introductory statement. Information, diagrams, and illustrations on the various hosts of parasites are then presented in separate sections. These include: (l) invertebrates as hosts (highlighting symbionts of the American oyster; blue crab, penaeid and grass shrimp); (2) vertebrates as hosts (concentrating on parasites of fishes, the alligator, birds, and marine mammals); (3) miscellaneous symbionts (explaining the infestations by selected nematodes, flatworms, barnacles, and gnats); (4) fish-kills and miscellaneous diseases (identifying causal factors contributing to the kills); and (5) technical aspects (citing research findings related to the specific organisms covered in preceding sections). A listing is provided of all the referenced literature and a glossary is also included of the common terms related to symbionts. (ML)
Up-estuary migration of crab larvae to adult habitats is thought to be accomplished by selective tidal transport in which late-stage larvae enter the water column on flood tides and remain on or near the bottom on ebb tides. This study measured endogenous rhythms in swimming by the last larval stage (megalopa) of blue crabs Callinectes sapidus and fiddler crabs Uca spp. Previous field studies found that megalopae of both species were only abundant in the estuarine water column on nocturnal rising tides. Megalopae were collected from the Newport River Estuary, North Carolina (3441N; 7640W) during August–September 1992 and swimming activity was recorded for 4.5 to 7 d under constant conditions with a video system. Rhythms exhibited by both genera in the laboratory were not identical to those recorded in the field. Uca spp. displayed a circatidal rhythm, with maximum swimming occurring near the time of high tide in the field. Rhythm amplitude increased when crushed oyster shells were present, which suggested that megalopae bury or cling to the substrate during quiescent periods. In contrast, C. sapidus had a circadian rhythm in which maximum swimming coincided with the day phase in the field. In most trials, the activity of blue crab megalopae was unrelated to the expected tidal cycle. It was concluded that a tidal rhythm in swimming was the behavioral basis of flood-tide transport for fiddler crab larvae. The endogenous rhythm in blue crabs does not participate in transport, which probably results from behavioral responses to environmental cues associated with flood tide.
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.
Postlarval and juvenile grass shrimp (Palaemonetes pugio Holthuis) ≦15 mm total length (TL) were abundant at low tide in shallow aquatic microhabitats (i.e. puddles and films of
residual tidal water) in the intertidal zone of a salt marsh on Sapelo Island, Georgia, USA from 1982 to 1984. The highest
concentrations of young P. pugio occurred at 190 to 200 cm above mean low water, ∼10 to 20 cm below mean high water. The intertidal distributions of young
grass shrimp expanded and contracted with changes in tidal amplitude. Postlarval grass shrimp (6 to 8 mm TL) continuously
recruited into the intertidal marsh population from May until October, but densities varied in a regular pattern with peaks
in abundance occurring at ∼2-week intervals, corresponding to spring tide periods in the lunartidal cycle. Although present
nearly year-round in the intertidal marsh, juveniles (9 to 15 mm TL) were most abundant from August to October. Apparent growth
rates of individuals up to 15 mm TL averaged 0.268±0.026 (mean±95% C.I.) mm d-1 from May to October and 0.070±0.032 mm d-1 in November and December. Unlike larger aquatic organisms, which can forage in the emergent marsh only when it is flooded
by the tide, juvenile grass shrimp have constant access to intertidal resources. Although potentially important predators
in this system, the role of young P. pugio in the trophic organization of salt marsh benthic invertebrate assemblages has yet to be examined.
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.
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.
Typescript. Thesis (M.S.)--University of South Carolina. Includes bibliographical references.
Microphallus piriformes (Trematoda) is unusual in having only two hosts and no motile free-living stages. The intermediate host, the rough periwinkle, Littorina saxatilis, is present year-round on rocky shores and has a high parasite prevalence near breeding colonies of the definitive host, the herring gull, Larus argentatus, which is present in numbers at these sites for only 4 months per year. Given the seasonal availability of gulls for infection and a low incidence of periwinkles in the normal diet of herring gulls, specialized transmission between stages appears necessary for maintenance of the parasite's life cycle. We investigated the hypothesis that M. piriformes alters its intermediate host's behaviour during the gull's breeding season in a manner that may facilitate predation of the infected periwinkle by breeding gulls. We studied the movements of periwinkles during simulated tidal cycles in the laboratory; parasite status was established subsequently. Periwinkles with mature infections moved further upwards but showed less downwards and horizontal movement than uninfected periwinkles. The movement of periwinkles with immature (nontransmissible) infections was less affected by the parasite. During the tidal cycle, infected and uninfected periwinkles differed in both timing and extent of movement. A field experiment confirmed the greater upwards movement of infected periwinkles. The parasite-induced changes in periwinkle behaviour may increase the chances of predation by the final host and could represent an important survival strategy for M. piriformes. Copyright 2000 The Association for the Study of Animal Behaviour.
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.