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Probopyrus Pandalicola (Packard) (Isopoda, Epicaridea): Morphology and Development of Larvae in Culture
Abstract
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.
... The epicarideans use the phase of attachment to the copepod with a steady income of nutrients to drastically change the overall body morphology. While the epicaridium is rather stout in appearance compared to the subsequent larval stages, it possesses well-developed setae and specialized, fully developed appendages (Anderson and Dale, 1981). The microniscium is more slender. ...
... The absence of the last thoracic appendage is reminiscent to the condition in manca stages in other isopod species. During the 4 microniscium larval stage a significant growth and a morphological change (supposedly without moulting) towards the morphology of the cryptoniscium stage can be observed (Anderson and Dale, 1981). Cryptoniscium. ...
... They swim actively and at least some cryptoniscia are able to curl up (for protection?) (Fraisse, 1878). The overall morphology of cryptoniscium larvae is relatively uniform in all epicaridean species known from this stage (Anderson and Dale, 1981). The body is elongated with a convex dorsal and a concave ventral surface. ...
Epicaridea is an ingroup of Isopoda that comprises only parasitic crustaceans. Within parasitic isopods, epicarideans represent a special case: throughout their ontogeny they switch from a small intermediate host (copepod) to a final host (various larger crustaceans), and develop through distinct larval phases (epicaridium, microniscium and cryptoniscium). Young males of some species retain a larval morphology. Recent findings of fossil epicarideans in amber from the Miocene of Mexico consisted in the only epicaridean body fossils, until one specimen has been figured from Cretaceous amber from France. Here we provide a detailed analysis of this specimen and 20 more specimens from the same locality. The presented specimens represent the oldest occurrence of epicaridean body fossils, extending their fossil record by 67 million years. The fossils are exceptionally well preserved and, despite their small size of less than 0.5 mm, reveal even fine morphological details. The specimens correspond either to cryptoniscium larvae or males that have retained their larval morphology. There are no morphological features in the fossils that argue against conspecifity of all specimens. All character states found in the fossils are also present in extant species. Given the displayed combination of character states and the age difference, it is unlikely that the specimens are conspecific to any extant species nor to much younger fossils from the Miocene of Mexico. The species Vacuotheca dupeorum gen. et sp. nov. is described and interpreted as an epicaridean of uncertain affinities, but that is not part of the epicaridean ingroup Dajidae. Furthermore, multiple aspects of the evolutionary history of parasitic isopods and epicarideans in particular are discussed. This includes possible scenarios for host changes that could have led to the life cycle of modern epicarideans and the evolution of size within epicaridean larvae.
... Sars (1899) found microniscus stages on Metridia longa (Lubbock, 1854), which he provisionally attributed to a member of Podascon Giard & Bonnier, 1889 (Cryptoniscoidea: Podasconidae), but the authenticity of this record has yet to be confirmed. All other reports of associations between epicarideans and copepod hosts refer to the Bopyroidea, including the families Bopyridae (Veillet, 1945;Pike, 1960Pike, , 1961Danforth, 1963;Anderson, 1975Anderson, , 1990Beck, 1979;Anderson & Dale, 1981;Dale & Anderson, 1982;Dumbauld et al., 2011), Entoniscidae (Caullery, 1907(Caullery, , 1908Veillet, 1945) and Ionidae (Caroli, 1928(Caroli, , 1929Reverberi & Pitotti, 1942). Among the calanoids, members of the Acartiidae are by far the most commonly reported intermediate hosts for larval epicarideans. ...
... Among the calanoids, members of the Acartiidae are by far the most commonly reported intermediate hosts for larval epicarideans. However, many of these reports are not based on field samples but on studies involving experimental exposure of Acartia species in the laboratory (Caullery, 1907(Caullery, , 1908Caroli, 1928Caroli, , 1929Reverberi & Pitotti, 1942;Veillet, 1945;Pike, 1961;Danforth, 1963;Anderson, 1975Anderson, , 1990Anderson & Dale, 1981;Dale & Anderson, 1982). Various, mostly cursory, records exist for several other families, including the Arietellidae, Calanidae, Centropagidae, Clausocalanidae, E u c h a e t i d a e, M e t r i d i n i d a e, Pa r a c a l a n i d a e, Pontellidae, Scolecitrichidae and Subeucalanidae. ...
Adult isopods of the family Dajidae are exclusively ectoparasitic, typically infecting pelagic malacostracan crustaceans. It is assumed that their life cycle involves free-living and parasitic phases, with planktonic copepods acting as intermediate hosts. Most generic diagnoses proposed in the family have traditionally been incomplete, containing imperfect or misleading information, and characters whose states were wrongly assessed. In an attempt to analyse this state of affairs comprehensively, a taxonomic review and updated diagnosis of the species-rich genus Holophryxus are presented. Both traditional and novel morphological characters are critically assessed, forming the basis for updated differential diagnoses of all currently valid species. The presence of previously ignored sensory structures on the body and pereopods is highlighted and its significance discussed. Holophryxus citriformis sp. nov. is recorded on the common shrimp, Hymenodora glacialis, at 4300 m depth in the central Arctic Ocean. Its description, based on light microscopy and confocal laser scanning microscopy analysis of the female holotype, containing a dwarf male inside its marsupium, is proposed as a model of enhanced descriptive standards required in future morphological research on epicaridean isopods. Definitive host records and geographical distributions of all Holophryxus species are summarized as well as records of larval epicaridean stages associated with copepod hosts.
... Unlike other parasitic isopods, bopyrids have a complex life cycle that involves host changes from a small intermediate host (calanoid copepods) to a larger definitive host (decapod crustaceans) (Schädel et al., 2019). They develop through three distinct larval stages: epicaridium, microniscium, and cryptoniscium (Anderson and Dale, 1981;Williams and Boyko, 2012). ...
The morphology of female bopyrids is adapted to parasitism, but understanding the function of their thoracic and mouth appendages is hindered by their small size and cryptic lifestyle, limiting detailed examination. This study aimed to clarify the function of the first oostegites and maxillipeds in bopyrid isopods infesting the branchial chamber of caridean shrimp through behavioural observations and morphological examination. We tested whether the movement of these structures was exclusive to ovigerous female parasites during brood ventilation. The results revealed that the beating of the maxillipeds and flapping of the first oostegites were not restricted to ovigerous females. However, the frequency of these movements was significantly higher in ovigerous females than in non-ovigerous females. The frequency of maxilliped beating increased with embryonic development, whereas that of flapping the first oostegites exhibited the opposite trend. Microscopic observation using dye showed that the movements of the maxillipeds and the first oostegites expelled residual dye from the female brood chamber through the dorsal surface or beneath the first oostegites. The dye was then transported by the water current generated by the scaphognathite of the host shrimp. These findings suggest that these structures not only facilitate ventilation but also serve as a grooming mechanism for female parasites, which is critical for embryonic survival. The results of the present study represent the first observation of embryo grooming in bopyrid isopods. This study also provides new information on the functional morphology of bopyrid isopods, which is important for understanding their ecological dynamics and adaptation to parasitism.
... The mouthpart morphology of epicaridium larvae have not been studied extensively across epicaridean families. Representative species of bopyrids and those from a few additional families are nevertheless known in enough detail to permit study of the development of the mouthparts (Walz, 1882;Giard & Bonnier, 1887, 1895Calman, 1898;Bonnier, 1900;Pérez, 1900;Caullery, 1908;Gilson, 1909;Hiraiwa, 1936;Holdich, 1975;Chaix & Veillet, 1981;Coyle and Muller, 1981;Anderson & Dale, 1981;Dale & Anderson, 1982;Sassaman, 1992;Cericola & Williams, 2015;Williams & An, 2009;Williams & Boyko, 2021). All epicaridium larvae start out with the following mouthparts: mandibles, maxillula (= maxilla 1), maxilla (= maxilla 2), and maxillipeds below a broad, raised labrum (see Wolff, 2009: fig. ...
External yolk sacs in free-living larvae of marine invertebrates are extremely rare, with all reported cases exhibiting yolk that is taken up through connection with the anterior alimentary canal. Herein, we confirm a novel yolk sac connected to the posterior end of the alimentary canal in the first larval stage of species in the bopyrid isopod genus PleurocryptellaBonnier, 1900, all known as ectoparasites in the branchial chambers of squat lobsters. Pleurocryptella poseidon Williams & Boyko sp. nov. infesting the munidopsid Galacantha bellis Henderson, 1885 in the Arabian Sea, is described on the basis of adults and larvae. In common with conspecifics, the new species exhibits a suite of putative “primitive” characters including the presence of oostegites on the sixth and seventh pereomeres of females and maxillipeds and articulated uropods in males. Pleurocryptella poseidon Williams & Boyko sp. nov. differs from other species of Pleurocryptella by characters of body shape, antennae, oostegite 1, pleon, and uropods of females and midventral tubercles, pleomeres, and pleopods of males. The epicaridium larvae have a large posterior, external yolk sac and segmented maxillipeds, a unique set of characters within Epicaridea. In addition to larval and adult characters, molecular data (COI) indicate that the genus is distinct from other members of Bopyridae, so we erect the new subfamily Pleurocryptellinae for it. Pleurocryptella poseidon Williams & Boyko sp. nov. bears a new genus and species of hyperparasitic isopod that is herein described based on its cryptoniscus stage. A review of epicaridium larval morphology and a key to the species of Pleurocryptella are provided.
... The embryos hatch as epicaridium, which attaches to an intermediate host and moults into a microniscus larva before further developing into a cryptoniscus larva (Lester, 2005;Williams and Boyko, 2012). After leaving the copepod, the cryptoniscus larva infects its final host (Anderson and Dale, 1981). The first larva to settle on the host becomes a female, whereas subsequent larvae develop into males (Reinhard, 1949). ...
The reproduction of bopyrid isopod parasites is thought to occur immediately following host ecdysis, but direct observations supporting this hypothesis are limited. The aim of this study was to describe the reproductive behaviour of the bopyrid isopod Bopyrus crangorum relative to host ecdysis based on video recordings. Several hours after host ecdysis, biphasic moulting of female parasites was observed. The cuticle of the posterior body was shed before that of the anterior body at an interval of 1 h. Two hours after female moulting, the male repeatedly moved from its initial position between the female pleopods and stopped at the anterior end of the fifth oostegite, immediately above the gonopore. To our knowledge, this repeated visiting behaviour by males has not been previously observed in bopyrid isopods. Oviposition through the female gonopore occurred 33 min later. The male-removal experiment showed that females with their males removed after visits to the gonopore oviposited eggs, whereas females with their males removed before visits did not. We propose that repeated visits by males to the gonopore are attempts to inseminate the female. We hypothesised that sperm are released onto the external surface of each gonopore and that the eggs are fertilised as they pass through the opening, which would explain the synchronous development of fertilised eggs inside the marsupium. The present study provides new information on the life history of bopyrid isopods, which allows for a better understanding of the host–parasite relationship.
... In particular, the intermediate hosts used by these parasites are very poorly known. Although copepods (particularly within the genus Acartia Dana, 1846) are intermediate hosts of other epicarideans (e.g., Pike 1960; Anderson & Dale 1981;Williams et al. 2022), to the best of our knowledge copepods have only been documented as intermediate hosts for two entoniscids in the genus Portunion Giard & Bonnier, 1886 and this was based on experimental research, not field observations. Caullery (1907) experimentally infested copepods and found epicaridium larvae of Portunion kossmanni (Giard & Bonnier, 1886) only infested Acartia clausii Giesbrecht, 1889 and A. discaudata (Giesbrecht, 1882); they would not settle on Centropages sp., Cyclopina sp. or euterpe sp. ...
Entoniscid isopods (Entoniscidae) are obligate endoparasites of other crustacean species. They have an indirect lifestyle, usually with two hosts and multiple larval stages; as adults they are found living within decapod hosts. Hermit crabs were previously known to be definitive hosts of only two species of entoniscid parasites: Paguritherium alatum, from the east coast of the United States in Pagurus spp. and Diogenion vermifactus from the Red Sea in Diogenes senex. Little beyond the original descriptions of these species has been reported in the literature. Recently, two species of entoniscids were found parasitizing hermit crabs (mostly Calcinus spp.) collected from shallow water coral reef areas in the Philippines. The goal of this study was to describe the morphology of both the adult and larval stages of these entoniscids through light and scanning electron microscopy and compare them to the previously described species that infest hermit crabs. One of these entoniscids is tentatively identified as D. vermifactus, which infested 0.95% (5 of 527) of the hermit crabs sampled. All specimens of D. cf. vermifactus were found in the abdomens of specimens of Calcinus gaimardii, C. minutus, C. pulcher and Pagurojacquesia polymorpha. Examination of D. vermifactus shows that this taxon belongs in its own subfamily: Diogenioninae n. subfam. The second entoniscid is a new species of the genus Paguritherium and infested 0.94% (7 of 744) of the hermit crabs (C. gaimardii and C. latens) sampled. Females of P. manggagaway n. sp. are characterized by a highly vaulted head, a slender body and long pleopods and males by a blunt head and stump-like pereopods covered in scales; the new species can be distinguished from P. alatum based on the specialized fan-like setae on the first five pereopods of the epicaridium larvae. A key to all entoniscid genera is provided.
... Epicaridea is a highly derived group of parasitic isopods (Anderson & Dale, 1981, Markham, 1986 in which most species use copepods as intermediate hosts and decapods, peracarids, or cirripedes as definitive hosts (Williams & Boyko, 2012). The affinities of epicarideans to other isopods have not been well resolved because of their modified morphology as a result of a parasitic life style, multiple ontogenetic stages, and paucity of specimens in collection (Markham, 1986;Williams & Boyko, 2012;Boyko et al., 2013;Yu et al., 2018). ...
Epicaridea is a group of isopods with high morphological diversity, reduction and loss of characters, and strong sexual dimorphism due to their parasitic lifestyles but their systematics is not well understood. Despite the use of nuclear and mitochondrial genes to test the phylogeny of many invertebrate groups, few molecular data from epicarideans are known, especially from the subfamily Orbioninae. Species in this group are obligate penaeoid shrimp parasites and the lack molecular data has hampered studies on the phylogeny of Orbioninae. To rectify this, mitochondrial and nuclear genes of 9 orbionine species are sequenced here. Compared to the isopod ground pattern, the sequences of orbionines seem to be more plastic near the control region and major translocations are located between rrns and cob. A phylogenetic analysis based on three data sets showed strong support for a monophyletic Orbioninae and that Epicaridea should be accepted at the rank of a suborder within Isopoda. The monophyly of Parapenaeon and Orbione is in doubt based on morphological and molecular data. The genus Parapenaeon is revised and a new genus Aparapenaeon is erected for Parapenaeon japonica and three closely related species.
... The expanded cryptoniscus then seeks out the final host, typically a crab, on which it settles between the gill lamellae. The settled larvae molt to the juvenile, which is also termed bopyridium by some authors (Anderson and Dale 1981, Boxshall 2005, Williams and Boyko 2012. ...
This volume examines Developmental Biology and Larval Ecology, Chapters in this volume synthesize our current understanding of early crustacean development from the egg through the embryonic and larval phase. The first part of this volume focuses on the fundamental aspects of crustacean embryonic development. The second part of the book provides an account of the larval phase of crustaceans and describes processes that influence the development from hatching to an adult-like juvenile. The third and final part of the book explores ecological interactions during the planktonic phase and how crustacean larvae manage to find food, navigate the dynamic water column, and avoid predators in a medium that offers few refuges. Collectively, these fifteen chapters provide a thorough overview of our present knowledge across the major themes in crustacean developmental biology and larval ecology. We expect this volume will be valuable to scholars and students who are interested in gaining deeper insights into the processes that lead from a single cell to subsequent stages of life and how - growing organisms face the challenges posed by their environment.
... material Tables S1-S3). Few studies have targeted these stages or experimentally tested settlement of epicardium larvae on copepods (e.g., Caullery, 1907;Pike, 1960;Anderson & Dale, 1981), documented their impacts on copepods (e.g., Anderson, 1975;Uye & Murase, 1997) or examined microniscus larvae on field collected copepods (see Bass et al., 2021) (Supplementary material Tables S1-3). Because the cryptoniscus larvae are responsible for finding and settling on definitive hosts, more research has targeted this stage (e.g., Bourdon, 1968;Owens & Rothlisberg, 1991, 1995. ...
Zooplankton samples from the northeastern Pacific, USA were analyzed to identify and determine the abundance and distribution of parasitic isopod larvae and copepod hosts. Vertically stratified samples were collected at stations spanning the continental shelf off Oregon, USA. Two species of epicarideans were identified: Hemioniscus balaniBuchholz, 1866 (endoparasite of barnacles) and Argeia pugettensisDana, 1853 (ectoparasite of shrimps). Cryptoniscus larvae of these species can be distinguished based on the antennae (four basal and five flagellar articles in H. balani, four basal and four flagellar articles in A. pugettensis), tooth-like structures on the antennules and coxal teeth (present in H. balani, lacking in A. pugettensis), and pereopods (1, 2 gnathopodal and 5, 6 ambulatory in H. balani, all gnathopodal in A. pugettensis). Epicaridean larvae were rare in zooplankton samples with concentrations up to 10 m–3. Larvae were often found within 10 km of shore, with highest concentrations below the Ekman layer at 20–50 m depth near the bottom and between the 8 and 10°C isotherms. Likely as a result of dislodgment, only 26 copepods with epicaridium or microniscus larvae attached were confirmed. Larvae were mostly (78%) found attached to two species of Acartia, suggesting they were the preferred host, but five other genera of copepods were documented as hosts. The concentration of copepods and larvae exhibited a significant positive correlation when the analysis was limited to stations where both larvae and copepods were caught. The distribution of host copepods was significantly shallower than epicaridean larvae and generally closer to shore. The planktonic phase of the life cycle of epicarideans remains a black box for most of the +860 known species. Future work should include molecular data to link their larval and adult life cycle stages and connect the parasites with their intermediate hosts.
... The expanded cryptoniscus then seeks out the final host, typically a crab, on which it settles between the gill lamellae. The settled larvae molt to the juvenile, which is also termed bopyridium by some authors (Anderson and Dale 1981, Boxshall 2005, Williams and Boyko 2012. ...
In this chapter, we explore the different patterns of development following the hatching of the crustacean larvae. For many groups of crustaceans, the free-living, postembryonic, and prejuvenile phase is by far the most important part of their life cycle, providing the link between different life modes in successive phases (e.g., between a sessile adult life and the need for long-range plank-tonic dispersal). Among the aspects covered, we discuss the specific criteria for what a "larva" is, including the necessity for defining specific larval traits that are lacking in other phases of the life cycle. We examine the typical anamorphic and hemianamorphic developmental patterns based on larval examples from a wide selection of groups from Decapoda to Copepoda, Thecostraca to Branchiopoda. In these groups, we examine the most common larval development patterns (including intraspecific variability) of, for example, the zoea, furcilia, copepodite, nauplius, and cypris larvae. We also expand on the importance of the molting cycle as the main driver in larval ontogeny and evolution. Finally, we discuss some of the more general trends of crustacean larval development in light of the general patterns and latest knowledge on tetraconate and arthropod evolution.
... Diverse species of crustaceans are infested by bopyrid isopods, parasites that have a complex life cycle with two hosts: a calanoid copepod as an intermediate and a definitive host (Anderson & Dale 1981). Generally, a cryptoniscus larva infests the gill chamber of a juvenile definitive host, the first larva that reaches it develops into a female, and the later ones into males (Anderson 1975). ...
Growth is an important ecological factor of species on which information is scant for host–parasite associations. A sample of 680 Hippolyte zostericola parasitized by the isopod Bopyrina abbreviata were collected at Términos Lagoon, Mexico, to evaluate the growth of both members of this association by the von Bertalan y method, as well as longevity of parasitized and unparasitized hosts, and parasite females. Misidentification of bopyrid species could be attributed to morphological variations of stages of development, so the relative growth of some body parts of B. abbreviata females were estimated at different stages of development. Overall, H. zostericola parasitized by B. abbreviata had lower growth rate and longevity than did unparasitized shrimp. Unparasitized H. zostericola females lived longer (10.2 months) than males (8.9 months), but parasitized males lived longer (7.31 months) than females (5.62 months). B. abbreviata longevity (5.98 months) was similar to that estimated for its host (6.31 months). The relative growth of the morphological characters differed between immature and mature stages of B. abbreviata females; the appearance of coxal plates, tergal projections and the fusion of pleomeres was progressive throughout development, so a combination of characters is proposed to allow differentiation between immature and mature females of B. abbreviata.
... A female-male pair of isopods is usually present within the branchial chamber of each parasitized shrimp (Kensley & Schotte, 1989), which typically remains with the host until its death (Beck, 1980a). Research on this parasite has included its life history (Beck, 1980a; Anderson & Dale, 1981, 1989; Anderson, 1990), prevalence (Chaplin-Ebanks & Curran, 2007; Key et al., 2011), and relationship with its shrimp hosts (Beck, 1980b, c; Anderson, 1990; Cash & Bauer, 1993; Bass & Weis, 1999; Chaplin-Ebanks & Curran, 2005; Sherman & Curran, 2013). Consumption of hemolymph by P. pandalicola can reach 10% of the total energy intake (Anderson, 1977) and up to 25% of total hemolymph volume of the shrimp on a daily basis (Walker, 1977). ...
... Temperature, dissolved oxygen and pH levels found at KWA-01 and 02 were neither higher nor lower than the other sites. While water quality parameters may play a part in affecting P. pandalicola incidence, they may also impose limits on the calanoid copepod intermediate host (usually Acartia tonsa; Anderson and Dale 1981). All these studies show that further work is needed to fully assess the impacts of changes in water quality parameters on crustacean parasites. ...
... This study shows that larval characters can be informative in phylogenetic studies of epicarideans, as has been found in other parasitic crustacean groups like rhizocephalan barnacles (see Rybakov et al., 2002;Boyko & Williams, 2009;Glenner et al., 2010). Unfortunately few detailed descriptions of epicaridean larvae (epicaridium, microniscus, and cryptoniscus) exist (but see Anderson & Dale, 1981;Dale & Anderson, 1982;Cericola & Williams, 2015). Future researchers should examine these life history stages, with particular focus on their antennae and other taxonomically important features to further test hypotheses on the evolutionary relationships of epicaridean taxa. ...
A detailed reexamination of male and female Entophilus mirabiledictu Markham & Dworschak, 2005 (an endoparasite of callianassid shrimp), resulted in recognition of seven female and five male characters that separate the species from its sole congener, E. omnitectus Richardson, 1903 (an endoparasite of munidid squat lobsters). These characters show that the two species are so different as to warrant E. mirabiledictu being placed in its own genus within the Entophilidae. Additionally, a review of the morphological features of entophilid cryptoniscus larvae led to the finding that the number of flagellar segments on the second antenna offers morphological support for a recent molecular phylogeny of epicaridean taxa that rearranged the component families within the two recognised superfamilies. This work highlights the power of using larval characters in testing hypotheses on the evolutionary relationships of epicaridean taxa.
... More than 16 palaemonid shrimps are sexually sterilized by the hematophagous bopyrid isopod parasite Probopyrus pandalicola (Kensley and Schotte, 1989). The branchial chamber of an infected shrimp contains a female-male pair of isopods (Figure 1) (Anderson and Dale, 1981). Bopyrids have opaque black oostegites, which may affect the camouflage of their terminal shrimp hosts. ...
... • Grass shrimp play a crucial role in estuarine communities as detritivores (Welsh, 1975) • Consumed by commercially and recreationally important fish species (Clark et al., 2003) • Atlantic croaker Micropogonias undulatus • Striped bass Morone saxatilis • At least 16 freshwater and marine palaemonid shrimp parasitized by the isopod Probopyrus pandalicola (Kensley and Schotte, 1989) • Branchial chamber of an infected grass shrimp contains a female and male isopod (Anderson and Dale, 1981) • Causes parasitic castration (Beck, 1980) • Affects various aspects of shrimp physiology, including metabolic and consumption rates (Anderson, 1975) • Possibly affects shrimp behavior (Bass and Weis, 1999; Chaplin-Ebanks and Curran, 2005) ...
Mapping the global distribution of Probopyrus pandalicola (bopyrid parasite) and the distributions of its potential hosts.
... Parasitic copepods may eat portions of fish larvae such as tissues or mucus; this ingestion may be significant if we consider that parasitic copepods are relatively large in fish larvae. If so, fish larvae maintain the parasites through their own nutritional budget (Anderson and Dale 1981;Astete-Espinoza and Cáceres 2000). (2) The immune response of the hosts. ...
Eumetazoan parasites in fish larvae normally exhibit large body sizes relative to their hosts. This observation raises a question about the potential effects that parasites might have on small fish. We indirectly evaluated this question using energetic metabolic laws based on body volume and the parasite densities. We compared the biovolume as well as the numeric and volumetric densities of parasites over the host body volume of larval and juvenile-adult fish and the average of these parasitological descriptors for castrator parasites and the parasites found in the fish studied here. We collected 5266 fish larvae using nearshore zooplankton sampling and 1556 juveniles and adult fish from intertidal rocky pools in central Chile. We considered only the parasitized hosts: 482 fish larvae and 629 juvenile-adult fish. We obtained 31 fish species; 14 species were in both plankton and intertidal zones. Fish larvae exhibited a significantly smaller biovolume but larger numeric and volumetric densities of parasites than juvenile-adult fish. Therefore, fish larvae showed a large proportion of parasite biovolume per unit of body host (cm(3)). However, the general scaling of parasitological descriptors and host body volume were similar between larvae and juvenile-adult fish. The ratio between the biovolume of parasites and the host body volume in fish larvae was similar to the proportion observed in castrator parasites. Furthermore, the ratios were different from those of juvenile-adult fish, which suggests that the presence of parasites implies a high energetic cost for fish larvae that would diminish the fitness of these small hosts.
... Although A. takanoshimensis was originally welldescribed by Ishii (1914) and has subsequently been reported from multiple localities and hosts (see Natural history of a bopyrid parasitic isopod 249 review in An et al. 2011), this is the first report to provide a detailed redescription of the male and female of the species and to utilize SEM for description of its epicaridium larval stage. Few descriptions of epicaridium larvae of bopyrids exist (see Anderson & Dale 1981;Dale & Anderson 1982;Williams & An 2009) and larval stages may provide important data for future taxonomic and systematic studies on bopyrids. The cryptoniscus larval stage remains unknown in A. takanoshimensis and studies on their use of intermediate copepod hosts are needed to fully understand the life history of this bopyrid. ...
The bopyrid isopod Athelges takanoshimensis is a relatively common abdominal parasite of hermit crabs from Asia. This study investigated the prevalence, reproduction, and morphology of A. takanoshimensis from over 1560 hermit crab specimens collected in Hong Kong between 2000 and 2004. Among these collections, A. takanoshimensis was on ∼7% of the hermit crab Pagurus angustus and was also recorded from 5% of Pagurus hedleyi; no hermit crabs from the genus Clibanarius were infested. The male–female ratio of parasitized P. angustus was approximately 3:7, in contrast to a 3:2 ratio for uninfested hosts, suggesting that parasitism has an influence on host sex ratio. Athelges takanoshimensis produced up to 5031 embryos (average brood size = 2852). Estimates of body size (head length, pereon length, and total length) were analysed as predictors of fecundity but a significant correlation was only found between brood size and pereon length. The morphology of the life history stages of A. takanoshimensis is described using scanning electron microscopy (SEM), including the first investigation of epicaridium larvae for this species. Notes on the behaviour of ovigerous females and the release of their larvae are provided, thus providing a better understanding of the natural history and morphology of A. takanoshimensis.
... As in other epicarideans, the life cycle probably includes a microniscus larva prior to the cryptoniscus, and it may well utilise planktonic copepods as hosts (e.g. Shiino 1964, Anderson & Dale 1981. These larval stages appear to live for about 6 to 7 mo during winter to early summer. ...
Double infection by 2 crustacean parasites was found on the mysid Siriella okadai collected from the Seto Inland Sea, Japan. An epicaridean isopod, Prodajus curviabdominalis, and a siphonostomatoid copepod, Neomysidion rahotsu, both occupied the lumen of the host marsupium, and fed voraciously upon host eggs. Interestingly, adult females of these 2 parasites occurred alternately on the host, with almost no overlap: the copepod occurred from mid-winter to summer when water temperatures were < 20 degrees C (with mean prevalence of 7.2 %), whereas the isopod occurred exclusively from midsummer to late autumn when water temperatures exceeded 20 degrees C (with mean prevalence of 9.1 %). Possible factors responsible for generating and maintaining this alternation of microhabitat occupancy on the host are discussed on the basis of the life cycles and host-specificities of the 2 parasites. In addition, we explored the possible means by which these obligate parasites survive during the periods when they Eire not on the mysid host. In the case of the isopod, we hypothesise that survival away from the mysid host involves the utilisation of an intermediate host by an as yet undiscovered microniscus larva, as in other epicarideans. For the copepod, we considered the available evidence in support of a number of hypotheses. A new pattern of behaviour, unique within the copepod family Nicothoidae, was discovered in N. rahotsu. After the infective female copepodid stage attached to the host, it moulted into an immature female and penetrated the host tissue, It then migrated internally, typically through the dorsal trunk musculature of the host, finally emerging into the host marsupium. This behaviour was observed exclusively during the season when copepods occurred within the marsupium. We inferred that this internal migration behaviour in some ways facilitates the synchronisation of the parasite life cycle with the oviposition by the host into the marsupium., It remains uncertain how and where N. rahotsu passes the exclusive occurence of P. curviabdominalis.
... The lecithotrophic larvae are positively phototactic and swim near the surface until they encounter a calanoid copepod to which they attach. The epicaridium metamorphoses via a moult into a microniscus which then develops into a cryptoniscus (Anderson & Dale 1981). The cryptoniscus then detaches and searches for a postlarval prawn as a definitive host (Beck 1980). ...
Three Gulf-wide cruises were examined for cryptonisci and the data analysed for the effect of environmental variables on cryptoniscid abundance. Location, season and location-season interaction accounted for 80% of the variability, with each accounting for 65, 25 and 10% of the explained variability respectively. More cryptonisci were found offshore in the northern and north-western areas of the Gulf and autumn had the highest abundance. In decreasing order, depth, temperature, salinity, light and their interactions were components within season and location and they accounted for 13, 6, 6, 4 and 43% of the variability respectively. The depth effect was related to the main prawn host Penaeus semisulcatus which also had a preference for deeper water. Fourteen different copepod intermediate hosts were identified by direct observation of attached cryptonisci; Cantho-calanus pauper and Paraeuchaeta concinna were the most important. Environment, however, was more important than intermediate hosts in explaining Variation in cryptoniscid numbers.
... These detach from the copepod and begin to seek the de nitive host (a decapod). The rst cryptoniscus that settles on the de nitive host grows up and turns into a female, while the second one turns into a male, which is always dwarfed and lives among the female pleopods (Anderson & Dale, 1981;Dale & Anderson, 1982). In the laboratory, the epicaridium of P. oridensis readily infested the copepod Acartia tonsa Dana, 1849; its development from epicaridium to cryptoniscus lasted 6 to 8 days (Dale & Anderson, 1982). ...
The population structure of the bupyrid isopod Probopyrus floridensis infesting the freshwater shrimp Macrobrachium potiuna from the Pereque River was monthly analysed from January 1996 to October 1996. The parasites, taken from preserved shrimps, were measured and sexed. A total of 635 isopod parasites was obtained from 197 shrimps. The following developmental stages and sexes were recognized within the parasite population: cryptoniscus, bopyridium, immature males, immature females, mature males, mature females, and ovigerous females. The parasitic density fluctuated between 1 (January and May) and 33 (June) parasites per host. The parasitic incidence varied from 1.1% (April) to 97.6% (September). Ovigerous females were observed only in October. The cryptoniscus infestation occurred mainly in June (early winter) and continued for three months. By July (winter), the majority of the parasite population was still composed of juvenile or immature parasites, but from August to October (spring), the adult stages predominated. Probopyrus floridensis reproduces only once a year. Its life cycle is discussed in more detail.
... If the female dies, males of some species have the ability to change sex and become females, and are thus considered protandric hermaphrodites (Reverberi 1947;Reinhard 1949). The present description of the epicaridium represents one of the few studies to examine the morphology of this larval stage with SEM (see Anderson and Dale 1981;Dale and Anderson 1982) and could aid in future taxonomic studies of the genus Orthione. The morphology of the microniscus and cryptoniscus larvae has not been studied and unfortunately the identity of the copepod intermediate host remains unknown. ...
The parasitic isopod Orthione griffenis Markham, 2004 was originally described from thalassinid mud shrimp hosts collected in Oregon. Subsequently, O. griffenis has been cited as a non-indigenous species in estuaries of the Pacific Northwest of North America; however, no taxonomic work has provided evidence that specimens from the western coast of the United States and other localities are conspecific. We report the first record of O. griffenis from Chinese waters based on collections made in the 1950s, which pre-date any records of the species from the United States by at least 20 years. Females of the Chinese specimens match the original description except in the number of articles on antennae 2 (six and five articles in the Chinese material and holotype, respectively). However, newly examined material from the United States showed females are variable in this character, exhibiting 5-6 articles on antennae 2. Although males of O. griffenis from Oregon were originally described as having second antennae with five articles, reexamination of the allotype showed that antennae 2 were damaged and missing terminal articles. Thus, the number of articles in the second antennae of males is six, as found in both the Chinese and new samples from the United States. Scanning electron microscopy (SEM) of males from USA and China revealed curled setae on the distolateral margins of the uropods, which were not reported in the original description. In China the species is found on Austinogebia wuhsienweni (Yu) from Shandong province, whereas along the western coast of North America the species extends from British Columbia to California on Upogebia pugettensis (Dana) and U. macginitieorum Williams (the latter species replacing U. pugettensis south of Pt. Conception, California). Orthione griffenis has also been reported from Japan on Upogebia issaeffi (Balss) and Austinogebia narutensis (Sakai). In Coos Bay, Oregon, the prevalence of the species was ∼65% in the mature U. pugettensis. The species was presumably introduced as larvae released in ballast water from ships originating in Asia. The epicaridium larvae of O. griffenis were examined with SEM, and aspects of the life history of the species are reviewed.
All species of Brazilian parasitic isopods belonging to Epicaridea (Bopyroidea and Cryptoniscoidea) known to date, including references and distribution information, are listed. The list comprises 37 valid species, 18 of which are endemic to the country, 17 are also recorded from other countries in the Americas, and only two species are distributed outside of the American continent as well. Synonym list, known hosts and distribution are given for each of the species, along with taxonomic and ecological remarks when relevant.
Six species of bopyrids were detected by inspection of crustaceans of diverse taxa collected in the Gulf of Mexico and the Mexican Caribbean that were deposited in two scientific collections housed in the Universidad Nacional Autónoma de México. Probynia ramiroromani, new species is described, becoming the first species of the genus from the American continent. The occurrence of Pseudione cf. crenulata is recorded for the first time in the west Atlantic coast, the distribution ranges of Orthione furcata, Parabopyrella thomasi, and Robinione overstreeti are extended, and O. furcata and Urobopyrus processae are reported for the first time in Mexican waters. Munida valida, Periclimenaeus perlatus, Processa bermudensis, and Upogebia vasquezi are now recognized as hosts of P. cf. crenulata, P. ramiroromani, U. processae, and O. furcata, respectively.
This study was conducted at depth 5-20 meters from the coastal area of Bushehr during July to September, 2013. The aim of this study was identification of Bopyrid: Isopod in two shrimp species Penaeus semisulcatus and Metapenaes affinis and the effects of biological and environmental factors on its disturbance. In this study 814 kg of samples included of 735 kg of Green tiger shrimp (P. semisulcatus), 68 kg of jinga shrimp (M. affinis) and 20 kg other species were collected. The identified Bopyridae parasite was belonged to Epipenaeon ingens. The result showed that the abundance of bopyridae parasite in the Green tiger shrimp (P. semisulcatus) was 26 %, which observed in the depth of 10 – 20 meters. No Bopyridae parasite was detected from jinga shrimp (M. affinis). The average weight and length of infected green tiger prwan specimens were 39.87±0.27 gr and 19.61±0.07 cm, respectively. The physiological state of infected shrimps indicated that, reduction of ovarian development and petasma in female and male, respectively. There was a significant relationship between water temperature and salinity increased with increasing of E. ingens abundance in P. semisulcatus in the studied area.
Within Isopoda (woodlice and relatives), there are lineages characterised by a parasitic lifestyle that all belong to Cymothoida and likely form a monophyletic group. Representatives of Epicaridea (ingroup of Cymothoida) are parasitic on crustaceans and usually go through three distinct larval stages. The fossil record of Epicaridea is sparse and thus little is known about the palaeoecology and the origin of the complex life cycle of modern epicarideans. We present an assemblage of over 100 epicarideans preserved in a single piece of Late Cretaceous Myanmar amber. All individuals are morphologically similar to cryptoniscium stage larvae. The cryptoniscium stage usually constitutes the third and last larval stage. In modern representatives of Epicaridea, the cryptoniscium larvae are planktic and search for suitable host animals or adult females. These fossil specimens, though similar to some extant species, differ from other fossil epicaridean larvae in many aspects. Thus, a new species (and a new genus), Cryptolacruma nidis , is erected. Several factors can favour the preservation of multiple conspecific animals in a single piece of amber. However, the enormous density of epicarideans in the herein presented amber piece can only be explained by circumstances that result in high local densities of individuals, close to the resin-producing tree.
Two fossils from Burmese amber are the subject of this study. The specimens differ in size; yet, they appear to be conspecific because of the profound morphological similarity. The fossils are interpreted as representatives of Isopoda, more precisely of the group Cymothoida, due to the presence of a triangular basipod of the uropod. Cymothoida comprises parasitic forms of Isopoda as well as many other types of feeding-habits. The morphology in the studied fossils suggests that they are not representatives of any of the parasitic ingroups of Cymothoida. Since there are no other findings of Isopoda from the Cretaceous with the same morphological features, the fossils at hand are described as a new species - Electrolana madelineae sp. nov. The smaller specimen lacks well-developed walking appendages on trunk segment seven; it can thus be interpreted as a manca stage (immature) individual. The systematic affinity and the functional morphology of the herein described fossils, as well as three seed shrimps (Ostracoda) in close proximity to one of the specimens, and the presence of pyrite in the amber piece points towards an aquatic lifestyle and a preservation in moist conditions. In addition, we review the fossil record of immature forms of Isopoda.
The effects of infestation by the bopyrid isopod Megacepon goetici on the varunid crab Gaetice depressus were investigated. This crab is one of the most common crabs in Japanese intertidal shores where it plays a key role in structuring the benthic community. Samples were collected in Wakayama Prefecture, Japan. From a total of 1694 crabs, 61 (3.6%) were parasitized by bopyrid isopods. No ovigerous females were parasitized, which may be evidence of parasitic castration of female host crabs, as has been described in other parasitized brachyuran crabs. Total weight was reduced in both males and females, and infested crabs also exhibited subtle lateral and dorsal carapace swelling due to the presence of parasites under the carapace. We therefore conclude that the morphology and the reproductive capacity of G. depressus were significantly affected by the bopyrid isopod.
Ghost and mud shrimps in Axiidea and Gebiidea are hosts to parasitic epicaridean isopods, including species in Bopyridae and Ionidae. These isopods can reach high prevalence levels on their mud shrimp hosts and may strongly influence host ecology and biology. Currently, 54 species of bopyrids and eight species of ionids are known to parasitize ghost and mud shrimps. We present new taxonomic data on three species of ionids and ten species of bopyrids (nine previously described and one new to science), as well as on an undescribed species of nematode from an axiidean host. New locality and host records are given for all species. Our analysis of new material and review of museum specimens includes the description of the new species Acrobelione halimedae n. sp. from Austinogebia spinfrons (Haswell, 1881). We also provide an improved definition for the genus Pseudione Kossmann, 1881, based on morphological characters found in both sexes, and resolution of the type species, P. callianassae Kossmann, 1881. In our revision of Pseudione we erect a new genus, Robinione, and placed two species therein: R. overstreeti (Adkison & Heard, 1995) and R. brattstroemi (Stuardo, Vega & Cespedes, 1986). In addition, two other species are removed from Pseudione: P. compressa (Shiino, 1964) is moved to Ionella Bonnier, 1900, and P. panopei Pearse, 1947 is considered a synonym of Progebiophilus upogebiae (Hay, 1917). Bopyrid isopods represent a large, diverse taxon and our findings help clarify the taxonomy of those species found on ghost and mud shrimps.
Thalassinidean shrimps are common macrofaunal components of the intertidal and shallow subtidal zones of beaches and estuaries. These organisms present burrowing behavior and are exposed to low oxygen concentrations in their natural environment. In addition, the parasitic isopod Ionella agassizi is frequently found in the branchial chamber of the ghost shrimp Neotrypaea uncinata. Previous studies have shown that the presence of this parasite affects the physiological condition of N. uncinata, provoking a negative effect on reproduction. In this study we evaluated the effects of exposure to hypoxia and parasitism on host metabolic capacity. For this, we evaluated the effect of the parasite on area of gas exchange in the host and the ability to resist hypoxic conditions by evaluating haemolymphatic concentrations of proteins, haemocyanin, lactate, glucose and the activity of enzyme lactate-dehydrogenase (LDH). Our results indicate that the presence of the parasite reduces the gill area in N. uncinata. During exposition of the ghost shrimp to hypoxic conditions, this increases its hemolymphatic concentrations of glucose, lactate, and the activivity of LDH. These results are interpreted as the utilization of metabolic alternatives to aerobic metabolism during periods of oxygen deficiency.
In the symbiosis between ghost shrimps and bopyrid isopods we studied some reciprocal effects on the reproduction of the symbionts. Samples were taken between february and july 1995 at Lenga, Chile (36 degrees 45' S; 73 degrees 10' W). Hosts were sampled from two habitats: estuary and beach, and consisted on 214 Callichirus garthi (Retamal 1975) and 497 Neotrypaea uncinata (Edwards, 1837). The distribution, abundance and fecundity of isopods in shrimps were compared among habitats and species. Also, we studied the correlation between the isopod body size and the host body size, as well as the relationship between isopod body size and its fecundity. We evaluated the effect of isopods on the host reproduction by comparing the gonadic maturity and the morphometry of sexual secondary characters in parasitized and isopod-free shrimps. The ghost shrimp N. uncinata was the only parasitized species: Ionella agassizi Bonnier 1900 accounted for 98.8% of the 324 isopods collected. The other isopod species was Ione ovata Shiino 1964. prevalence increased with host body length and large shrimps harboured bigger isopods, which instead had higher fecundity. We found that the beach shrimps were less parasitized than the estuary shrimps. However, the host's habitat was not as important in the isopod fecundity as the host body size. I. agassizi affected glaringly the host reproduction, because prevented ovarian maturation and the secondary sexual characters of the parasitized shrimps were smaller than in unparasitized ones. This is interpreted as resulting from the high nutritional interference by the parasitic isopod on its host.
The ghost shrimp Neotrypaea uncinata is parasitized in the branchial chamber for the isopod Ionella agassizi. Previous works had indicated that the parasite causes a negative effect in the reproductive biology of the ghost shrimp, influencing seriously the development of reproductive organs and the expression of secondary sexual characteristics. This effect can be produced by a general reduction of the reserve substances of N. uncinata caused by the presence of the parasite. In order to evaluate the effect of the parasite on the nutritional status of the ghost shrimp we measured the concentration of some metabolites related to the nutritional physiology of N. uncinata. The results showed a greater frequency of infection in adult males, which suggests differential mortality by effect of the parasite through the host ontogeny. The parasitized individuals showed a reduction of the body mass and a diminution of both protein and haemocyanin levels. However, the measured lactate levels are smaller in parasitized individuals, but the levels of glucose were higher in this individuals, this relationships suggest the use of lactate as substrate for glucose synthesis. Finally the lipid reduction in parasitized ghost shrimps demonstrates the scarcity of the reserve substances in this species.
On coastal habitats near Concepcion city, Chile, there are two isopod species Ione ovata Shiino, 1964, and Ionella agassizi Bonnier, 1900 both occupying the gill chambers of the ghost shrimp Neotrypaea uncinata (H. Milne Edwards, 1837). However, in I. ovata, the prevalence is smaller, there is a low frequency of coupled isopods in the same gill chamber, and is less host specific than I. agassizi. These observations suggest that both isopod species have different life histories. To improve the understanding of the causes of these differences some life history traits of isopods species (fecundity, egg size and reproductive investment and the capability of individual males isopods to survive in uninfested ghost shrimps) are examined and compared. lore agassizi has lower fecundity but larger eggs than I. ovata. However, there were neither differences in reproductive investment nor in relation to their body size between the two species. Experimental infestation of ghost shrimps by males of both species of isopods showed that only males of I. ovata could remain on the hosts for a few weeks and metamorphose into females. It would be necessary to estimate survival of isopods during the total life cycle, in order to improve the interpretation of these results.
In the present study, we determine the presence of parasites in fish larvae collected from nearshore waters along the northern and central coast of Chile. The parasites were identified to the lowest possible taxonomic level based on morphological and molecular analyses. The fish sample was composed of 5 574 fish larvae. Of these, 3% harboured only larval ectoparasitic copepods whereas no endoparasites were found in the 1 141 fish evaluated for this group of parasites. The parasitic copepods collected were initially classified as 'morphotypes' according to differences in morphological characteristics. They were then analysed using molecular techniques based on the 28S and COI genes. Seven morphotypes of parasitic copepods (mostly at chalimus stages) were recognised: two of the morphotypes belonged to Pennellidae Burmeister, 1835, three to Caligidae Burmeister, 1835 and two were not identified. Only five morphotypes of copepods were analysed using molecular sequences, which confirmed the existence of six species: two pennellids of the genus Trifur Wilson, 1917 and two caligids of the genus Caligus Müller, 1785, plus two additional species that were morphologically different from these taxa. The pennellids were present in several fish species, being generally more prevalent than the caligids, in both the central and northern localities of Chile. Multispecies infections in larval fish were infrequent (< 1%). We conclude that fish larvae were rich in parasites, considering that these hosts exhibited small body sizes and were very young. We suggest that fish larvae could play a role, as intermediate hosts, in the life cycle of the parasitic copepods found.
To understand the distribution of bopyrid isopods and assess their impact on host penaeid prawn populations, studies on factors
affecting their larval behaviour and dispersal were undertaken Three series of stratified plankton samples were taken in the
Gulf of Carpentaria at three seasons of the year. The bopynd cryptoniscid larvae migrated nocturnally to the surface and migrated
diurnally to the bottom waters A multiple correlation coefficient of 0 70 showed that the number of cryptonisci varied negatively
with light intensity and positively with the plankton biomass and the sampled depth. Partial correlation decomposition of
the correlation coefficient showed light, depth and biomass to have partial coefficient values of -0 45, 0 43 and 0.28 respectively
In the Mornington Island area, a multiple regression analysis combining depth sampled and the copepod species Acrocalanus gibber and Corycaeus dahli gave a correlation coefficient of 0 91 with cryptoniscid abundance However, the largest single correlation coefficient was
with Calanopia ethpnca (r = 0.77) which was highly correlated with depth sampled. Estimated advection distances were between 80 and 120 km As cryptonisci
and prawn larvae both migrate vertically and also move over similar distances, postlarval prawns can be infected on the nursery
grounds by the bopyrid cryptonisci
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.
Thalassinidean shrimps are common macrofaunal components of the intertidal and shallow subtidal zones of beaches and estuaries. These organisms present burrowing behavior and are exposed to low oxygen concentrations in their natural environment. In addition, the parasitic isopod Ionella agassizi is frequently found in the branchial chamber of the ghost shrimp Neotrypaea uncinata. Previous studies have shown that the presence of this parasite affects the physiological condition of N. uncinata, provoking a negative effect on reproduction. In this study we evaluated the effects of exposure to hypoxia and parasitism on host metabolic capacity. For this, we evaluated the effect of the parasite on area of gas exchange in the host and the ability to resist hypoxic conditions by evaluating haemolymphatic concentrations of proteins, haemocyanin, lactate, glucose and the activity of enzyme lactate-dehydrogenase (LDH). Our results indicate that the presence of the parasite reduces the gill area in N. uncinata. During exposition of the ghost shrimp to hypoxic conditions, this increases its hemolymphatic concentrations of glucose, lactate, and the activivity of LDH. These results are interpreted as the utilization of metabolic alternatives to aerobic metabolism during periods of oxygen deficiency.
Several Probopyrus ssp. produce ecto- and endoparasitic (tissue) larvae. The purpose of this paper is to evaluate the colonization and distribution of cryptoniscus larvae in shrimp of both sexes and to perform a microanatomical analysis of the larvae-bearing tissue in order to typify the tissues involved and their eventual reaction. The following conclusions are drawn: (1) ecto- and endoparasitic cryptoniscus colonize the various body areas of Palaemonetes argentinus at random, affecting young shrimp, maturing shrimp, and sexually mature shrimp; (2) only the ectoparasitic larvae that reach the branchial chamber become actually integrated to the consortium; (3) the tissue larvae are erratic guests of the shrimp's connective-hemolymphatic tissue and no tissue reaction leading to the isolation of the larvae occurs and this is not the result of a systemic immunological depression in the host; (4) the tissue cryptonisci located next to the gonad of shrimp of either sex do not have any effect on the normal development of germinal cells.
On coastal habitats near Concepción city, Chile, there are two isopod species Ione ovata Shiino, 1964, and Ionella agassizi Bonnier, 1900 both occupying the gill chambers of the ghost shrimp Neotrypaea uncinata (H. Milne Edwards, 1837). However, in I. ovata, the prevalence is smaller, there is a low frequency of coupled isopods in the same gill chamber, and is less host specific than I. agassizi. These observations suggest that both isopod species have different life histories. To improve the understanding of the causes of these differences some life history traits of isopods species (fecundity, egg size and reproductive investment and the capability of individual males isopods to survive in uninfested ghost shrimps) are examined and compared. Ione agassizi has lower fecundity but larger eggs than I. ovata. However, there were neither differences in reproductive investment nor in relation to their body size between the two species. Experimental infestation of ghost shrimps by males of both species of isopods showed that only males of I. ovata could remain on the hosts for a few weeks and metamorphose into females. It would be necessary to estimate survival of isopods during the total life cycle, in order to improve the interpretation of these results
The ghost shrimp Neotrypaea uncinata is parasitized in the branchial chamber for the isopod Ionella agassizi. Previous works had indicated that the parasite causes a negative effect in the reproductive biology of the ghost shrimp, influencing seriously the development of reproductive organs and the expression of secondary sexual characteristics. This effect can be produced by a general reduction of the reserve substances of N. uncinata caused by the presence of the parasite. In order to evaluate the effect of the parasite on the nutritional status of the ghost shrimp we measured the concentration of some metabolites related to the nutritional physiology of N. uncinata. The results showed a greater frequency of infection in adult males, which suggests differential mortality by effect of the parasite through the host ontogeny. The parasitized individuals showed a reduction of the body mass and a diminution of both protein and haemocyanin levels. However, the measured lactate levels are smaller in parasitized individuals, but the levels of glucose were higher in this individuals, this relationships suggest the use of lactate as substrate for glucose synthesis. Finally the lipid reduction in parasitized ghost shrimps demonstrates the scarcity of the reserve substances in this species
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.
Thirteen species of parasitic bopyrid isopods occur on New Zealand decapod crustaceans. Six species: Pseudione pontocari; P. murawaiensis; Gyge angularis; Gigantione pikei; Rhopalione atrinicolae; and Pseudostegias otagoensis are new to science. Five species: Pseudione affinis (Sars); P. hyndmanni (Bate & Westwood); Pleurocryptella infecta Nierstrasz & Brender à Brandis; Hemiarthrus nematocarcini Stebbing; and Eophrixus shojii Shiino are recorded for the first time in New Zealand. The 2 remaining species, Pseudione hayi Nierstrasz & Brender à Brandis and Athelges lacertosi Pike are previously described endemics. These 13 species belong to 4 of the 10 currently recognised subfamilies of the Bopyridae. The new species are described, and all species are figured.
In this paper, adaptations and microanatomic changes in the branchial chamber, as well as influence of parasitosis on the reproductive function of shrimp, are analyzed. Probopyrus cf. oviformis was observed in the branchial chamber of shrimps of both sexes, with an infestation rate of 29%. The infestation frequency in relation to sex and size was not uniform, and two trends were observed: a higher frequency in bigger males in contrast to females, with less infestation frequency in older individuals. This aspect was related to changes in the sex ratio of shrimps, infested and noninfested, with the following conclusions: (1) Sexual inversions were not observed in females of P. argentinus; (2) male infestation with P. cf. oviformis showed tertiary sexual rate bias. It occurred because the metabolic parasite-host relationship led to an increase in size. These infested males were incorporated into a normal population characterized by females being bigger than males. The morphological and functional changes observed were (1) branchial chamber reduction, slendering of the cephalothorax lateral wall, together with local injury (oxygen consumption was below the normal values; and (2) the ovaries of infested females of P. argentinus remained stationary in incipient maturity (secondary vitellogenesis was not observed).
The behaviour of two ectosymbiotic animals, Peregrinamor
ohshimai (a bivalve attached to the ventral cephalothorax of the host), and Phyllodurus sp. (a bopyrid isopod attached to the second pleopod of the host), during ecdyses of the host thalassinidean Upogebia shrimps was studied by time-lapse video of infested shrimps. In the intermoult stages of the hosts, both ectosymbionts did not move. However they moved on to the newly emerged body of the host at the time when the host moulted. Peregrinamor
ohshimai began to move just after the host started moulting, whereas Phyllodurus sp. moved prior to ecdysis of the host and waited near the fissure from which the newly moulted body emerges first. There are highly correlated morphological relationships between the symbionts and the hosts. It is suggested that both ectosymbionts grow with the same host individuals after infection, keeping morphological affinity with their hosts without being discarded during ecdyses of the hosts.
The ghost shrimp Neotrypaea californiensis is imported into southern California from Oregon and Washington for use as live bait in recreational marine fisheries. We
studied the population genetic structure of N. californiensis across much its range to assess the possibility that the transport of ghost shrimp across phylogeographic boundaries poses
a risk of homogenizing existing genetic variation in the species. Analyses of two mitochondrial DNA markers showed little
phylogeographic structure across the sampled range, suggesting that this risk is low. Unexpectedly, mitochondrial DNA analyses
revealed that a second putative species of ghost shrimp frequently coexisted with N. californiensis in southern California intertidal habitats; almost all previous studies of soft-sediment communities in the region report
the presence of N. californiensis only. We also assessed the possibility that the import of ghost shrimp might pose a risk of introduction of a parasitic castrator,
the bopyrid isopod Ione cornuta, into southern California waters, where it does not appear to be native. Prevalence of living I. cornuta in samples purchased from bait shops was high (5.8%), suggesting that this is a real risk that merits further study.
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.
Moulting in Isopod Crustacea usually occurs in two phases and invariably the ecdysis of posterior half precedes the anterior. The hormonal control for regulating such a unique biphasic mode of moulting can only be explained by an effectively functional physiological mechanism probably involving circulatory inhibitions or restricted neurosecretive activities. This paper describes the observations made at McMurdo, Antarctica on an unusual single phase moulting in the endemic antarctic giant isopod Glyptonotus.
1. In Panulirus argus, premolt animals may be detected by the appearance of a resorptive or ecdysial line along the branchiostegites.2. One of the most obvious external changes in Panulirus a few hours before ecdysis is the swollen condition of the intersegmental membranes.3. Five to fifteen minutes preceding ecdysis, animals of 80-89 mm. carapace length increase their body weight by approximately 10%. This weight increase begins four to six hours preceding ecdysis and is entirely due to water absorption. There is a loss of weight following ecdysis due to loss of the exuviae. Within a few hours following molt, the weight of the individual begins to rise and continues to do so until a maximum is reached at 28-35 days. The water content begins to rise the day preceding molt, reaches its highest peak (11% above the intermolt value of 71%) one day following molt, slowly declines but does not return to its intermolt value before 28-35 days. At this period the animal has fully calcified its new skeleton, and ap...
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.
1.1. Larval isopods of the parasitic species Probopyrus pandalicola do not consume oxygen at a rate which is a direct function of their body size. Their metabolic rate is dependent mainly on “mode of existence” as well as category of metabolism taking place for a given larval stage.2.2. A comparison of the mean metabolic rates between infected and uninfected copepod intermediate hosts Acartia tonsa indicates that oxygen consumption in the host decreases as a result of infection.