Habitat and host specificity of trematode metacercariae in fiddler crabs from mangrove habitats in Florida

Fiddler crabs (Uca spp.) are common inhabitants of temperate and tropical coastal communities throughout the world, often occupying specific microenvironments within mangrove and salt marsh habitats. As second intermediate hosts for trematodes, we investigated patterns of host distribution and parasitism for 3 species of sympatric fiddler crabs in mangrove habitats adjacent to the Indian River Lagoon, Florida. Fiddler crab distribution varied among species, with Uca speciosa dominating the low and mid intertidal regions of mangrove banks. This species also exhibited higher prevalence and abundance of Probolocoryphe lanceolata metacercariae compared with Uca rapax, which is relatively more abundant in the high intertidal zone. We conducted a field experiment to test whether U. speciosa was more heavily parasitized by P. lanceolata as a result of its habitat distribution by raising U. speciosa and U. rapax under identical environmental conditions. After exposure to shedding cercariae under the same field conditions, all individuals of U. speciosa became parasitized by P. lanceolata, whereas no U. rapax were parasitized, suggesting that differences in parasitism were driven by host selection.     

High serotonin levels due to the presence of the acanthocephalan Hexaglandula corynosoma could promote changes in behavior of the fiddler crab Uca spinicarpa

Between February and June 2010, 113 fiddler crabs Uca spinicarpa were collected from the Chuburna lagoon system on the northern coast of the Yucatan Peninsula, México. Of the 68 crabs gathered outside their burrows, 13 were infected with 25 cystacanths of Hexaglandula corynosoma (intensity of infection from 1 to 5) and the remaining 55 crabs were uninfected. The other 45 crabs were found inside their burrows and only one was found infected with 1 cystacanth of H. corynosoma. Serotonin (5-HT) levels were higher in the group of crabs infected with H. corynosoma in contrast to the group of uninfected crabs and the group of those infected with other parasites. A redundancy analysis corroborated a positive relationship between 5-HT and the intensity of infection with H. corynosoma. In contrast, dopamine levels remained similar among different groups of crabs.     

Helminth parasites of the southern sea otter Enhydra lutris nereis in central California: abundance,distribution and pathology

From October 1997 to May 2001, the gastrointestinal tracts from 162 beach-cast southern sea otters Enhydra lutris nereis were examined for helminth parasites and associated lesions. Carcasses were collected opportunistically in central California between Pt. San Pedro and Pt. Arguello. The primary goals of this study were to examine spatial and temporal variability in mortality due to parasite infection, identify factors associated with increased risk of infection, and illustrate the process of intestinal perforation by Profilicollis spp. Two genera and 4 species of acanthocephalans (Profilicollis altmani, P. kenti, P. major, Corynosoma enhydri) were found in 46.3% (Profilicollis spp.) and 94.4% (C. enhydri) of the carcasses examined. Three species of Digenea (Microphallus pirum, M. nicolli, Plenosoma minimum) were found in 47% of carcasses, at times in massive numbers (> 3000 per cm2). This is the first report of the latter 2 species from the sea otter. Mortality resulting from infection by Profilicollis spp. occurred in 13.0% (n = 21) of sampled carcasses, either directly, due to perforation of the intestinal wall and peritonitis (9.9%, n = 16), or indirectly, due to inhibition of host nutrient uptake or depletion of host energy reserves to fight chronic infections (3.1%, n = 5). The most massive infections (< 8760 parasites), and all cases of intestinal perforation occurred in carcasses infected by P. altmani and/or P. kenti. Mortality due to infection by Profilicollis spp. occurred more frequently among juvenile and old-adult females (chi2 = 17.479, df = 9, p = 0.045) from sand and mixed habitats in Monterey and Santa Cruz in the north of the sea otter range (chi2 = 9.84, df = 4, p = 0.045). Spatial differences in sea otter mortality coincided with the relative distributions of Profilicollis altmani, P. kenti, and P. major, and may reflect differences in sea otter diet, or differences in intensity of infection in intermediate hosts. Mortality rate due to infection by Profilicollis spp. decreased between 1998 and 2001, though differences were not significant (chi2 = 3.983, df = 3, p = 0.40), and may vary on multi-year cycles due to environmental factors such as density of definitive hosts (e.g. the surf scoter Melanitta perspicillata), or El Ni?o. Corynosoma enhydri did not cause significant damage to the intestine of the host, even when present in great numbers.     

Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict?

Larval helminths of different species that share the same intermediate host and are transmitted by predation to the same definitive host may cooperate in their attempts to manipulate the behaviour of the intermediate host, while at the same time having conflicts of interests over the use of host resources. A few studies have indicated that intermediate hosts harbouring larval helminths have altered concentrations of neurotransmitters in their nervous system, and thus measuring levels of neurotransmitters in host brains could serve to assess the respective and combined effect of different helminth species on host behaviour. Here, we investigate potential cooperation and conflict among three helminths in two species of crab intermediate hosts. The acanthocephalan Profilicollis spp., the trematode Maritrema sp. and an acuariid nematode, all use Macrophthalmus hirtipes (Ocypodidae) as intermediate host, whereas Profilicollis and Maritrema also use Hemigrapsus crenulatus (Grapsidae). All three helminths mature inside gulls or other shore birds. There was a significant decrease in the mean volume of Profilicollis cystacanths as the intensity of infection by this parasite increased in H. crenulatus, the only host in which this was investigated; however, there was no measurable effect of other helminth species on the size of acanthocephalans, suggesting no interspecific conflict over resource use within crabs. There was, in contrast, evidence of a positive interspecific association between the two most common helminth species: numbers of Profilicollis and Maritrema were positively correlated among crabs, independently of crab size, in M. hirtipes but not H. crenulatus. More importantly, we found that the total number of larval helminths per crab correlated significantly, and negatively, with concentrations of serotonin in crab brains, again only in M. hirtipes; numbers of each parasite species separately did not covary in either crab species with serotonin or dopamine, the other neurotransmitter investigated in this study. The relationship with serotonin appears due mainly to numbers of Profilicollis and Maritrema and not to nematodes. This is the first demonstration of a potentially synergistic manipulation of host behaviour by different helminth species, one that appears host-specific; our results also point toward the neurobiological mechanism underlying this phenomenon.     

Discapseudes holthuisi (Crustacea: Tanaidacea) as an intermediate host of Caballerorhynchus lamothei (Acanthocephala: Cavisomidae)

The intermediate host of the acanthocephalan Caballerorhynchus lamothei Salgado-Maldonado, 1977, is reported for the first time. Cystacanths of C. lamothei were found in the hemocoel of the tanaid shrimp Discapseudes holthuisi Bacescu and Gutu, 1975, in Alvarado and Sontecomapan lagoons, Veracruz, Mexico. This is the first report of a palaeacanthocephalan using a tanaid shrimp as an intermediate host. Prevalence by locality, shrimp length, sex and developmental stage, and an analysis of the distribution of number of cystacanths per host are presented. A higher prevalence, and percentage of multiple infections and larger host size were found in Alvarado Lagoon.     

Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites?

Density-dependent effects on parasite fitness have been documented from adult helminths in their definitive hosts. There have, however, been no studies on the cost of sharing an intermediate host with other parasites in terms of reduced adult parasite fecundity. Even if larval parasites suffer a reduction in size, caused by crowding, virtually nothing is known about longer-lasting effects after transmission to the definitive host. This study is the first to use in vitro cultivation with feeding of adult trematodes to investigate how numbers of parasites in the intermediate host affect the size and fecundity of adult parasites. For this purpose, we examined two different infracommunities of parasites in crustacean hosts. Firstly, we used experimental infections of Maritrema novaezealandensis in the amphipod, Paracalliope novizealandiae, to investigate potential density-dependent effects in single-species infections. Secondly, we used the crab, Macrophthalmus hirtipes (Ocypodidae), naturally infected by the trematodes, M. novaezealandensis and Levinseniella sp., the acanthocephalan, Profilicollis spp., and an acuariid nematode. These four helminths all develop and grow in their crustacean host before transmission to their bird definitive host by predation. In experimental infections, we found an intensity-dependent establishment success, with a decrease in the success rate of cercariae developing into infective metacercariae with an increasing dose of cercariae applied to each amphipod. In natural infections, we found that M. novaezealandensis-metacercariae achieved a smaller volume, on average, when infrapopulations of this parasite were large. Small metacercariae produced small in vitro-adult worms, which in turn produced fewer eggs. Crowding effects in the intermediate host thus were expressed at the adult stage in spite of the worms being cultured in a nutrient-rich medium. Furthermore, excystment success and egg-production in M. novaezealandensis in naturally infected crabs were influenced by the number of co-occurring Profilicollis cystacanths, indicating interspecific interactions between the two species. Our results thus indicate that the infracommunity of larval helminths in their intermediate host is interactive and that any density-dependent effect in the intermediate host may have lasting effects on individual parasite fitness.     

Evaporative water loss, corporal temperature and the distribution of sympatric fiddler crabs (Uca) from south Texas

Desiccation and thermal stress are among the primary factors limiting terrestriality in crustaceans. Water loss was estimated as weight change in five sympatric species of Uca from south Texas for periods up to 7 hr in dry air. Simultaneously, corporal temperature was measured with a thermocouple placed under the carapace. To estimate integumental permeability to water, 115 mm2 portions of dorsal carapace were glued to U-shaped tubes containing a crab Ringer's solution. These were exposed to dry air and water permeability was estimated from weight change. In whole-animal studies, most rapid weight loss occurred in the first 5 min of exposure to dry air as the body temperature fell below ambient (25 degrees C) in all species. The three most terrestrial species exhibited significant survival over more aquatic congeners after prolonged desiccation. The greatest rate of water loss was observed in Uca subcylindrica which lost 22.9+/-3.0% body weight. Uca panacea and Uca spinicarpa lost 14.1+/-1.6% and 18.5+/-1.8%, respectively. Based on blood osmolarity changes, Uca longisignalis and Uca rapax were more resistant to water loss than Uca subcylindrica under these conditions. Water loss from sections of the dorsal carapace were highest in Uca spinicarpa (10.4 mg/hr/cm2) and Uca longisignalis (8.9 mg/ hr/cm2). Uca subcylindrica and Uca panacea were intermediate (4.5 and 4.2 mg/hr/cm2) while Uca rapax expressed the lowest value (2.9 mg/hr/cm2). These observations support the notion that water loss can effectively lower body temperature in fiddler crabs. However, an inverse relationship between terrestriality and integumental permeability was not evident in these sympatric congeners. Ultimately a balance between physiological and behavioral mechanisms must be achieved for adaptation to the semi-arid habitats in south Texas.     

Profilicollis novaezelandensis n. sp. (Polymorphidae) and two other acanthocephalan parasites from shore birds (Haematopodidae and Scolopacidae) in New Zealand,with records of two species in intertidal crabs (Decapoda: Grapsidae and Ocypodidae)

Profilicollis novaezelandensis n. sp. (Acanthocephala: Polymorphidae) is described from the South Island pied oystercatcher Haematopus ostralegus finschi Martens (Haematopodidae) and the intertidal crab Hemigrapsus crenulatus (Milne Edwards) (Brachyura: Grapsidae) from the South Island of New Zealand. The new species can be distinguished from all the other species of the genus by a combination of the following characters: long neck (13% of total body length for adults) and a subspherical proboscis with 14–16 longitudinal rows of 7–8 hooks. The mud crabs Helice crassa Dana (Grapsidae) and Macrophthalmus hirtipes (Heller) (Ocypodidae) were also harbouring cystacanths and the bar-tailed godwit Limosa lapponica (Linnaeus) (Scolopacidae) juveniles of P. novaezelandensis. This is the first record of brachyuran decapods as intermediate hosts of Acanthocephala from New Zealand. P. antarcticus is recorded from three crab species (Helice crassa, Hemigraspus crenulatus and Macrophthalmus hirtipes) and two bird species (Haematopus o. finschi and Limosa lapponica) in New Zealand. An unidentified species of Plagiorhynchus was also found in two bird species (H. o. finschi and H. unicolor Forster). P. antarcticus and P. novaezelandensis are the first records of Profilicollis from New Zealand.     

A new species of Microphallus (Trematoda: Microphallidae) from Venezuela

During 1997-1999, a total of 94 crabs, Uca rapax were collected from La Sabana, La Ceiba and El Paujil, Sucre State, Venezuela. Of these 36 were infected with metacercariae. Two parasites were located in the abdominal muscles and one under the tissue of carapace and gonad. These metacercariae grew to adults in the following genera: Levinseniella, Microphallus and Maritrema, in the period of 2-5 days after feeding experimentally to the rat Rattus norvegicus, mice Mus musculus and duck Cairinia moschata. Specimens of the genus Microphallus were described herein as a new species M. sabanensis. The life cycle of M. sabanensis sp.nov. were studied experimentally using rat, mice and duck. All developmental stages and the adult are described. In addition, M. sabanensis was collected from wild birds Anas discors, Pluvialis squatarola, Butorides striatus, Egretta caerulea and Nycticorax violaceus from the same localities.     

A gastropod scavenger serving as paratenic host for larval helminth communities in shore crabs

The whelk Cominella glandiformis is an important predator-scavenger of New Zealand intertidal ecosystems; a few whelks can quickly eat all the soft tissues of recently dead crabs. In this study, we demonstrate that whelks can also ingest and act as paratenic hosts for at least 4 helminth species that use crabs as intermediate hosts: metacercariae of the trematode Maritrema sp. and of another unidentified trematode, larval acuariid nematodes, and cystacanths of the acanthocephalans Profilicollis spp. Large whelks ingest disproportionately more helminth larvae than small whelks, but the survival of parasites during their short stay in the whelks is not affected by whelk size. The majority of metacercariae and nematodes are passed out in whelk feces within 3 days of ingestion, whereas the few cystacanths found did not leave whelks until after that time; no parasite was left in whelks 5 days postingestion. Survival of all 4 helminth species was generally very high, though it decreased day by day in 2 species. Given that the avian definitive hosts of all 4 helminths also eat whelks, our results indicate that alternative transmission pathways exist and that parasites can take routes through food webs that are too often ignored.     

Altered dopamine levels induced by the parasite Profilicollis antarcticus on its intermediate host, the crab Hemigrapsus crenulatus

A serotonergic pathway is apparently involved in parasite-host interactions. Previous studies conducted in our laboratory showed increased rates in oxygen consumption and alterations in body posture in the crab Hemigrapsus crenulatus parasitized by the acanthocephalan, Profilicollis antarcticus. Such changes may be related to the functions described for biogenic amines in crustaceans. During the infective stage the acanthocephalans live freely in the hemocelomic cavity, suggesting that the possible alteration induced by biogenic amines may be related to their neurohormonal function in crustaceans. To test whether the presence of P. antarcticus produced neurohormonal changes in its intermediate host, H. crenulatus, we analyzed serotonin and dopamine levels in the host using HPLC with electrochemical detection. Two groups of 11 female crabs were studied; one group was artificially inoculated with two cystacanths while the other was used as the control. Our results show a dramatic increase in hemolymph dopamine, but not serotonin in H. crenulatus parasitized by the acanthocephalan P. antarcticus. Our results, along with those reported by Maynard (1996), suggest a parasite-specific strategy involved in the behavior alteration caused by the acanthocephalans on their intermediate host. The use of a biogenic amine as a mechanism of interaction by the parasites gives them an endless number of alternative potential actions on their intermediate hosts.     

Reintroduction of Profilicollis Meyer, 1931, as a genus in acenthocephala: significance of the intermediate host.

Polymorphid acanthocephalans with long necks, spheroid proboscides, and eggs without polar swellings of the fertilization membrane constitute a morphologically distinct group of species. In the past, this taxon was considered a separate genus, Profilicollis. More recently, workers have been unwilling to accept these features as generic-level characters, and presently the group is considered a subgenus of Polymorphus. An analysis prompted by our studies of various polymorphid cystacanths in crabs along the coasts of Scotland and the U.S.A. reveals that all records of Polymorphus in decapods refer to species with 6 cement glands frequently assigned to Hexaglandula, to incidental occurrences of species purported to be Polymorphus minutus, or to species of the subgenus Profilicollis. Occurrence in decapod crustaceans implies substantial life history differences from the other species of the genus occurring in amphipod crustaceans. We conclude this, together with morphological distinctiveness, justifies return of Profilicollis to full generic status within Polymorphidae.     

Changes in prevalence and intensity of infection of <Emphasis Type="Italic">Profilicollis altmani</Emphasis> (Perry, 1942) cystacanth (Acanthocephala) parasitizing the mole crab <Emphasis Type="Italic">Emerita analoga</Emphasis> (Stimpson, 1857): an El Niño cascade effect?

Prevalence and intensity changes in cystacanths of the acanthocephalan Profilicollis altmani parasitizing the mole crab Emerita analoga under El Niño (EN) and non-El Niño (non-EN) conditions are analyzed. Both, mean intensity and prevalence of infection by P. altmani differ significantly for the whole size range and for each size class of 10 mm intervals (except prevalence for size classes exceeding 18 mm carapace length) between EN (1998) and non-EN (2002) years, without observed size distribution differences in the intermediate host E. analoga under either condition. Significant difference in infestation rates of the intermediate host E. analoga is discussed as being an EN cascade effect on predators such as sea birds (i.e., Larus spp. and Calidris sp.), acting as definitive hosts of P. altmani, and which are known to decrease significantly in abundance during EN.     

Parasite volume as an indicator of competition: the case of Acanthocephalus tumescens and Pseudocorynosoma sp. (Acanthocephala) in their intermediate host

In Lake Mascardi (Patagonia), 2 acanthocephalan species, Acanthocephalus tumescens and Pseudocorynosoma sp., share an amphipod intermediate host but have different definitive hosts. Because both acanthocephalan species are potentially capable of manipulating amphipod behavior, one of the parasites may, therefore, have no opportunity to complete its life cycle; accordingly, negative interactions between them can be expected. The purpose of the present work was to examine the possibility of competition in the intermediate host through a comparison of A. tumescens and Pseudocorynosoma sp. cystacanth volume. Specimens of the amphipod Hyalella patagonica were collected monthly over almost 2 yr. Amphipods were measured (total length), necropsied, and cystacanths collected. Cystacanths were also measured, and their volume was calculated. Size of both acanthocepalan species was positively associated with amphipod total length. Competition, during 3 different infection periods, was assessed: high level of Pseudocorynosoma sp. infection (HP), high level of A. tumescens infection (HA), and high level of mixed infection (HM). In Pseudocorynosoma sp., intra-specific competition in HM was the only interaction found. In contrast, in A. tumescens, inter-specific competition in HP, intra-specific competion in HA, and intra- and inter-specific competition in HM were found. We suggest that Pseudocorynosoma sp. is a non-plastic species mostly found in single infections, while A. tumescens is a more variable species occurring more frequently in co-infections.     

Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala)

Studies on parasite species with a wide geographic and ecological range may be confounded by still equivocal taxonomic identification. Here, we investigated genetic polymorphism and behavioural changes induced in a common intermediate host, in two different forms of Pomphorhynchus laevis based on the morphology of the larval infective stage (cystacanth). A 'smooth type' (S) and a 'wrinkled type' (W) of cystacanth were distinguished based on their surface and shape. We analysed sequence divergence at both nuclear (ribosomal gene 18S rDNA, and ribosomal internal transcribed spacers, ITS1/ITS2) and mitochondrial (cytochrome c oxidase subunit 1) genes of P. laevis cystacanths and adults at various geographical scales. A high level of sequence divergence at ITS1, ITS2 and cytochrome c oxidase subunit 1 (11, 8 and 20%, respectively) was found between these two forms. The divergence pattern consistently discriminated two groups independently of geographic origin or host, and was congruent with larval morphology. The two forms also strongly differed in the intensity of behavioural change induced in their common intermediate host, Gammarus pulex, with the S-type parasite inducing a positive phototactism, whereas W-type infected gammarids were as photophylic as uninfected ones. Overall, our data strongly support the specific status of these two forms. We suggest that smooth cystacanths correspond to P. laevis, whereas wrinkled cystacanths might correspond to the previously described and poorly documented, Pomphorhynchus tereticollis, considered a synonym of P. laevis. This study also confirms the value of a joint analysis of internal transcribed spacers and cytochrome c oxidase subunit 1 genes to biogeographic studies on these species. Finally, we emphasize the importance of linking morphological and biological characteristics of acanthocephalan cystacanths to molecular data, in the study of the evolutionary ecology and systematics of this group.     

Profilicollis botulus (Van Cleave, 1916) from diving ducks and shore crabs of British Columbia

Adults of Profilicollis botulus were found in 6 species of diving ducks in British Columbia including 3 new hosts: common goldeneye, Bucephala clangula (L.); Barrow's goldeneye, B. islandica (Gmelin); and greater scaup, Aythya marila (L.). The identification of the species was verified by the examination of co-types and specimens from eider ducks, Somateria mollissima (L.), from Scotland and oldsquaw, Clangula hyemalis (L.), from New Brunswick. Cystacanths from the hairy shore crab, Hemigrapsus oregonensis (Dana), were similar in morphology to those from Carcinus maenas (L.) from Scotland.     

Effect of acanthocephalan parasites on hiding behaviour in two species of shore crabs

The effect of acanthocephalan parasites (Profilicollis spp.) on the hiding behaviour during low tide of two species of shore crabs (intermediate hosts), Macrophthalmus hirtipes (Brachyura: Ocypodidae) and Hemigrapsus crenulatus (Brachyura: Grapsidae), was examined at Blueskin Bay, South Island, New Zealand. Exposed M. hirtipes were found to have significantly higher infection levels than did hidden conspecifics. This pattern was not observed for H. crenulatus. Mean cystacanth numbers were found to be considerably higher in M. hirtipes than H. crenulatus. Crabs exposed at low tide are at a greater risk of predation by definitive shorebird hosts than are hidden conspecifics. Preferential manipulation of one intermediate host species over another could influence diversity within ecosystems.     

Parasite infection and sand coarseness increase sand crab (Emerita analoga) burrowing time

Parasites with indirect life cycles require trophic transmission from intermediate hosts to definitive (vertebrate) hosts. Transmission may be facilitated if parasite infection alters the behavior of intermediate hosts such that they are more vulnerable to predation. Vulnerability to predation may also be influenced by abiotic factors; however, rarely are the effects of parasites and abiotic factors examined simultaneously. The swash zone of sandy beaches is a particularly harsh environment. Sand crabs (Emerita analoga) burrow rapidly in the swash zone to avoid predators and dislodgment. We examined prevalence and abundance of the acanthocephalan parasite Profilicollis altmani in sand crabs, and investigated the synergistic effects of sand grain size (an important abiotic factor), parasite infection, body size and reproductive condition on burrowing speed in females, from three California sites. More heavily parasitized crabs burrowed more slowly, making them potentially more vulnerable to predation by marine bird definitive hosts. Ovigerous females harbored more parasites than non-ovigerous females, but burrowed more quickly. All crabs burrowed slowest in the coarsest sand, and burrowing times increased with repeated testing, suggesting that it is energetically costly. Abiotic and biotic factors influence burrowing, and behavioral variation across sites may reflect the response to natural variation in these factors.