Global distribution patterns and geographic range of Cymothoa Fabricius, 1793 (Isopoda: Cymothoidae) associated with host fish.

Over recent years, fish parasites of the genus Cymothoa Fabricius, 1793, have received increased attention due to both their ecological and their economic importance to aquaculture and fishery. As the studies about Cymothoa have increased this improve our understanding on the host specificity and distribution of these parasites. The aim of this paper was to review the current global geographic distribution, distribution patterns and parasite-host interactions patterns of Cymothoa spp. associated with fish from marine and brackish water bodies around the world. A total of 144 samples were analyzed, from which 23 species of Cymothoa were found parasitizing 84 teleost fish species of 35 families and 20 orders. Most of these parasites were found in the mouth of the host fish, including in wild fish. The highest occurrence of parasites was found in host species belonging to the families Carangidae and Lutjanidae. Host specificity was an important factor in the geographic distribution of Cymothoa species as also environmental temperature. Cymothoa indica, Cymothoa exigua and Cymothoa excisa were the species with lowest specificity for host family and widest geographic distribution.

Blood meal identification reveals extremely broad host range and host-bias in a temporary ectoparasite of coral reef fishes.

Appreciation for the role of cryptofauna in ecological systems has increased dramatically over the past decade. The impacts blood-feeding arthropods, such as ticks and mosquitos, have on terrestrial communities are the subject of hundreds of papers annually. However, blood-feeding arthropods have been largely ignored in marine environments. Gnathiid isopods, often referred to as "ticks of the sea", are temporary external parasites of fishes. They are found in all marine environments and have many consequential impacts on host fitness. Because they are highly mobile and only associated with their hosts while obtaining a blood meal, their broader trophic connections are difficult to discern. Conventional methods rely heavily on detecting gnathiids on wild-caught fishes. However, this approach typically yields few gnathiids and does not account for hosts that avoid capture. To overcome this limitation, we sequenced blood meals of free-living gnathiids collected in light traps to assess the host range and community-dependent exploitation of Caribbean gnathiid isopods. Using fish-specific COI (cox1) primers, sequencing individual blood meals from 1060 gnathiids resulted in the identification of 70 host fish species from 27 families. Comparisons of fish assemblages to blood meal identification frequencies at four collection sites indicated that fishes within the families Haemulidae (grunts) and Lutjanidae (snappers) were exploited more frequently than expected based on their biomass, and Labrid parrotfishes were exploited less frequently than expected. The broad host range along with the biased exploitation of diel-migratory species has important implications for the role gnathiid isopods play in Caribbean coral reef communities.

First report of marine horsehair worms (Nematomorpha: Nectonema) parasitic in isopod crustaceans.

Nectonema, the only horsehair worm (Nematomorpha) genus found in marine environments, was previously known to be parasitic only in decapod crustaceans. We report Nectonema sp. as the first record of a marine nematomorph parasitic in isopod crustaceans. This is also the third record of marine nematomorphs from the North Pacific. Six infected isopods (Natatolana japonensis) collected from 1425 m of depth in the Sea of Japan each contained one to seven (mean 2.33) nematomorphs in the body cavity in the pereon. There was no correlation between the host body length and number of parasites. For Nectonema sp., we describe and illustrate morphological features of the parasitic juvenile stage and present nucleotide sequences for the cytochrome c oxidase subunit I gene (COI or cox1; 451 nt), 18S rRNA gene (1777 nt), and region spanning the internal transcribed spacer 1 (ITS1) and the 28S rRNA gene including the 5.8S rRNA gene and ITS2 (1218 nt in total). In an 18S maximum-likelihood tree that included 24 nematomorph species, Nectonema sp. grouped with N. agile from the northwestern Atlantic; the 18S gene from these two taxa was divergent by 11.8% K2P distance, suggesting that they are different species. Nectonema species may have a broader range of host groups than previously suspected, but may have been previously misidentified as nematode parasites.

Molecular detection of apicomplexan blood parasites of coral reef fishes from free-living stages of ectoparasitic gnathiid isopods.

Gnathiid isopods are marine ectoparasites that feed on the blood of fishes that have been implicated as vectors of blood parasites, with transmission possibly occurring through biting during their parasitic life-stages, or through ingestion by fishes. However, evidence for their role as vectors is limited, reflecting the small number of research groups working on them. Here, we used a molecular barcode approach to identify fish hosts and apicomplexan parasites in free-living gnathiids from the eastern Caribbean Sea, with the goal of further evaluating their potential role as reservoirs and/or vectors for these parasites. Apicomplexa were only identified in 8% of the Gnathia analyzed, and in four cases we could identify both Apicomplexa and fish host DNA. The results further suggest that Gnathia spp. in this region may serve as reservoirs for Apicomplexa, but whether they are vectors for this parasite remains uncertain.

Apparent kleptoparasitism in fish-parasitic gnathiid isopods.

Gnathiid isopods are common external parasites/micropredators that feed on the blood of marine fishes. During the course of processing samples of gnathiid isopods collected from light traps in the central Philippines, we observed a gnathiid attached to and apparently feeding from the abdomen of another gnathiid. Because the abdomens of both gnathiids were enlarged, it was unclear whether one actually fed on the blood meal of the other. Introduction of unfed gnathiids with fed gnathiids revealed that one gnathiid could and did feed on the blood meal of another. This is the first observation of apparent conspecific kleptoparasitism reported for gnathiid isopods.

Do behavioural defence mechanisms explain different levels of trematode infections in congeneric hosts?

Susceptibility and tolerance to parasite infection vary greatly between host species. The congeneric isopod species Austridotea annectens and Austridotea lacustris often occur in sympatry and can both serve as intermediate hosts for the trematode Maritrema poulini. However, the intensity and prevalence of infections vary greatly in natural populations, with A. annectens often being heavily infected and A. lacustris rarely being infected. To shed light on the factors that may be involved in infection avoidance in A. lacustris, 100 isopods were collected and experimentally exposed to M. poulini cercariae. To examine for potential behavioural mechanisms, we used carbonated water as a paralysing agent to temporarily stop any movement by the isopods, and exposed paralysed isopods to cercariae. In the experiments, none of the individuals that were exposed to the parasite were found to be infected, although some cercariae seemed to have penetrated isopod hosts. Behavioural defence mechanisms do not seem to explain the different infection levels between A. lacustris and A. annectens, suggesting a physiological, possibly immunological, factor may be present. At the ecosystem level, this suggests a potential dilution effect caused by this low-competency host, and its effects on parasite transmission dynamics should be investigated.

Parasite-mediated microhabitat segregation between congeneric hosts.

Parasite-mediated competition can shape community structure and host distribution. If two species compete for resources, parasites may indirectly change the outcome of competition. We tested the role of a trematode parasite in mediating microhabitat use by congeneric isopods Austridotea annectens and Austridotea lacustris Although both isopods share resources, they rarely co-occur in the same discrete microhabitats. We set up mesocosms with and without competition and/or parasites to examine the role of parasites in host distribution and habitat segregation. Austridotea annectens showed a clear preference for one microhabitat type regardless of competition or parasitic infection. By contrast, A. lacustris showed little habitat selection in the absence of competition, but favoured sandy habitats in the presence of uninfected A. annectens and rocky habitats when competing with infected A. annectens Our results suggest that parasites in one species affect the distribution of another species, and mediate competition between these species. We demonstrated the impacts of a parasite on the microhabitat use of its host's competitor. This also represents an example of a super-extended phenotype, where a parasite affects the phenotype of a non-host.

Saduria entomon infected with Hysterothylacium aduncum found in situ in the stomach of cod (Gadus morhua) from the Baltic Sea.

The parasite fauna of cod (Gadus morhus) is well described, but the life cycles of Baltic cod parasites are known only in general terms. Invertebrates commonly found in the stomach of cod are recognized as intermediate hosts in the life cycles of nematodes or acanthocephalans. The aim of this study was to determine the source of infection of Baltic cod with parasites found in situ in invertebrates present in the cod stomach. Our results indicate that Saduria entomon is both a source of infection of Baltic cod with parasites and an intermediate host in the life cycle of Hysterothylacium aduncum in the Baltic Sea.

Multiple paternity in a wild population of Armadillidium vulgare: influence of infection with Wolbachia?

Female multiple mating has been extensively studied to understand how nonobvious benefits, generally thought to be of genetic nature, could overcome heavy costs such as an increased risk of infection during mating. However, the impact of infection itself on multiple mating has rarely been addressed. The interaction between the bacterium Wolbachia and its terrestrial crustacean host, Armadillidium vulgare, is a relevant model to investigate this question. In this association, Wolbachia is able to turn genetic males into functional females (i.e. feminization), thereby distorting the sex ratio and decreasing the number of available males at the population scale. Moreover, in A. vulgare, females have been shown to mate multiply under laboratory conditions and males prefer uninfected females over infected ones. Additionally, different Wolbachia strains are known to infect A. vulgare and these strains differ in their transmission rate and virulence. All these elements suggest a potential impact of different Wolbachia strains on multiple mating. To investigate this assumption, we collected gravid females in a wild A. vulgare population harbouring both uninfected females and females infected with one of two different Wolbachia strains (wVulM and wVulC) and performed paternity analyses on the obtained broods using microsatellite markers. We demonstrate that (i) multiple paternity is common in this wild population of A. vulgare, with a mean number of fathers of 4.48 ± 1.24 per brood and (ii) females infected with wVulC produced broods with a lower multiple paternity level compared with females infected with wVulM and uninfected ones. This work improves our knowledge of the impact of infections on reproductive strategies.

Competitive growth, energy allocation, and host modification in the acanthocephalan Acanthocephalus dirus: field data.

The acanthocephalan Acanthocephalus dirus is a trophically transmitted parasite that modifies both the physiology and behavior of its intermediate host (isopod) prior to transmission to its definitive host (fish). Infected isopods often contain multiple A. dirus individuals and we examined the relationships between host sharing, body size, energy content, and host modification to determine if host sharing was costly and if these costs could influence the modification of host behavior (mating behavior). Using field-based measures of parasite energy content (glycogen, lipid) and parasite body size (volume), we showed that host sharing was costly in terms of energy content but not in terms of body size. Analysis of the predictors of host behavior revealed that energy content, and body size, were not predictors of host behavior. Of the variables examined, parasite intensity was the only predictor of host behavior. Hosts that contained more parasites were less likely to be modified (i.e., less likely to undergo mating suppression). We suggest that intraspecific competition influenced parasite energy content and that the costs associated with competition are likely to shape the strategy of growth and energy allocation adopted by the parasites. These costs did not appear to have a direct effect on the modification of host mating behavior.

Acanthocephalan-related variation in the pattern of energy storage of a behaviorally and physiologically modified host: field data.

The acanthocephalan parasite Acanthocephalus dirus infects the freshwater isopod Caecidotea intermedius as an intermediate host before completing its life cycle in a fish. Transmission to the definitive host occurs after the parasite has reached the cystacanth stage, and development into this stage is associated with changes in several behavioral and physiological traits of the host. Given the potential importance of host energy availability to trait modification, we examined the relationship between cystacanth-stage infection and energy storage of adult isopods. Six samples of infected and uninfected male C. intermedius were collected from a population in March, April, and May during which time cystacanth-stage A. dirus dominate infections and modification of behavior and physiology occurs in nature. Biochemical assays revealed that infected male C. intermedius contained more glycogen and more lipid than uninfected males and that this difference was present throughout the sampling period, which represents the entire adult phase of the host's life. Additional analysis revealed that infected and uninfected males differed in their pattern of allocation to each energy source and that host lipid levels were negatively correlated with parasite intensity. We propose that the typical pattern of allocation and storage of host energy appears to be disrupted by A. dirus infection and that the changes are more likely to favor the parasite than the host.

Intra-population variation in behavior modification by the acanthocephalan Acanthocephalus dirus: are differences mediated by host condition?

The acanthocephalan parasite Acanthocephalus dirus infects the freshwater isopod Caecidotea intermedius as an intermediate host before completing its life cycle in a fish. Male C. intermedius infected by A. dirus parasites are less likely to engage in mating behavior than uninfected males but there is a significant intra-population variation in the occurrence of this behavioral change. Previous studies on uninfected isopods have shown that glycogen content is a predictor of male mating behavior and we examined whether the intra-population variation in the mating behavior of infected male C. intermedius could be explained by this relationship. A field-based behavioral experiment was used to quantify intra-population variation in male mating behavior, which showed that 50% of infected males were responsive to females and 50% were not responsive. Biochemical analysis of responsive and non-responsive males revealed that glycogen content was a predictor of the mating behavior for uninfected males but was not a predictor of mating behavior for infected males. For infected males, parasite intensity was a predictor of mating behavior. Males that contained more A. dirus parasites were less likely to undergo modification of mating behavior. We propose that the intra-population variation in the mating behavior of infected C. intermedius identified in nature was not mediated by host condition.

New insights into the life cycle of Platynosomum (Trematoda: Dicrocoeliidae).

The platynosomiasis, a worldwide parasitic disease with importance for domestic cat, has an etiological agent species of trematodes of the genus Platynosomum, whose complete life cycles are not yet known. The real role of lizards in the transmission of this dicrocoeliid parasite (as obligatory intermediate or paratenic host) still needs to be defined. In the present study, oval-shaped encysted metacercariae obtained from terrestrial isopods (Oniscidea sp. and Nagurus nanus) and elongated excysted metacercariae found in biliary ducts and gallbladder of lizards (Hemidactylus mabouia) in Brazil were used for morphological characterization and experimental infection of mice. Adult parasites recovered from bile ducts and liver of mice inoculated orally with metacercariae from both hosts (isopods and lizards) were identified as Platynosomum illiciens (=Platynosomum fastosum), showing that lizards are paratenic (not obligatory) hosts involved in the life cycle of this parasite. Moreover, Subulina octona is reported as the first intermediate host of P. illiciens in South America, and terrestrial isopods are presented here as new natural second intermediate hosts of the parasite. Finally, it is pointed out that high prevalence and intensity of infection of intermediate and paratenic hosts were observed. These findings on the life cycle of P. illiciens are relevant considering that they may indicate possible control measures of platynosomiasis.

Two new species of Maritrema Nicoll, 1907 (Digenea: Microphallidae) from New Zealand: morphological and molecular characterisation.

Two new species of the microphallid genus Maritrema (Maritrema) Nicoll, 1907 are described from freshwaters in the South Island of New Zealand. Maritrema deblocki n. sp. occurs as an adult in the mallard Anas platyrhynchos (L.); Maritrema poulini n. sp. is found as sporocysts/cercariae in Potamopyrgus antipodarum (Gray) and as metacercariae in two species of amphipod and two species of isopod. We use morphological and molecular characterisation to distinguish between the two species, and compare them to their four morphologically closest congeners. M. deblocki n. sp. and M. poulini n. sp. are distinguished from each other by the relative sucker size, the positions of the genital pore and ovary, the convergence of the vitelline ribbons, and overall size. With the aid of molecular data, we matched life cycle stages of M. poulini n. sp. and assessed its use of multiple second intermediate hosts. Phylogenetic analyses included sequences for the two new species and the available microphallid sequences for the large ribosomal subunit and the internal transcribed spacer 1 of the ribosomal RNA gene. Closer to each other than to any other species, the sister species together with Maritrema novaezealandense Martorelli, Fredensborg, Mouritsen & Poulin, 2004, Maritrema heardi (Kinsella & Deblock, 1994), Maritrema eroliae Yamaguti, 1939 and Maritrema oocysta (Lebour, 1907) formed a well-supported clade. In addition, we clarify the taxonomic identity of several unidentified Microphallus spp. in the recent ecological literature from New Zealand and propose corrected spellings for a number of Maritrema species epithets.

Exploring the preservation of a parasitic trace in decapod crustaceans using finite elements analysis.

The fossil record of parasitism is poorly understood, due largely to the scarcity of strong fossil evidence of parasites. Understanding the preservation potential for fossil parasitic evidence is critical to contextualizing the fossil record of parasitism. Here, we present the first use of X-ray computed tomography (CT) scanning and finite elements analysis (FEA) to analyze the impact of a parasite-induced fossil trace on host preservation. Four fossil and three modern decapod crustacean specimens with branchial swellings attributed to an epicaridean isopod parasite were CT scanned and examined with FEA to assess differences in the magnitude and distribution of stress between normal and swollen branchial chambers. The results of the FEA show highly localized stress peaks in reaction to point forces, with higher peak stress on the swollen branchial chamber for nearly all specimens and different forces applied, suggesting a possible shape-related decrease in the preservation potential of these parasitic swellings. Broader application of these methods as well as advances in the application of 3D data analysis in paleontology are critical to understanding the fossil record of parasitism and other poorly represented fossil groups.

Collecting Marine Gnathiid Isopod Fish Parasites with Light Traps.

A method to collect marine gnathiid isopod fish parasites with the use of light traps is presented. Gnathiid isopods are a major group of marine fish parasites that feed on blood and fluid from host fishes, mostly at night. Like ticks and mosquitos on land, they associate only temporarily with their host and spend most of their life free-living in the benthos. Given their high mobility and transient and predominantly nocturnal association with hosts, they cannot easily be collected by capturing free-living hosts. However, they are readily attracted to underwater light sources, creating the opportunity to collect them in light traps. Here the design and individual steps involved in the deployment and processing of specially adapted light traps for collecting free-living stages of gnathiid isopods are outlined. Sample results and possible modifications of the basic protocol for a variety of different sampling needs are presented and discussed.

First report on Mermithidae (Mermithida) infection in Ligidium sp. (Isopoda, Ligiidae).

Specimens of Ligidium sp. (Crustacea, Isopoda, Oniscidea) collected from Kanagawa Prefecture in Japan were found to be infected with parasitic nematodes. We have obtained two Mermithidae (Nematoda) by dissecting the fresh specimen and from the dead specimen of Ligidium, which marks the second known discovery of a mermithid infection in the order Isopoda. Herein, a report on the nuclear 28S rDNA and 18S rDNA sequence of the isolated Mermithidae nematodes and on the morphology of the juveniles is provided.

The nematode Caenorhabditis elegans and the terrestrial isopod Porcellio scaber likely interact opportunistically.

Phoresy is a behavior in which an organism, the phoront, travels from one location to another by 'hitching a ride' on the body of a host as it disperses. Some phoronts are generalists, taking advantage of any available host. Others are specialists and travel only when specific hosts are located using chemical cues to identify and move (chemotax) toward the preferred host. Free-living nematodes, like Caenorhabditis elegans, are often found in natural environments that contain terrestrial isopods and other invertebrates. Additionally, the C. elegans wild strain PB306 was isolated associated with the isopod Porcellio scaber. However, it is currently unclear if C. elegans is a phoront of terrestrial isopods, and if so, whether it is a specialist, generalist, or developmental stage-specific combination of both strategies. Because the relevant chemical stimuli might be secreted compounds or volatile odorants, we used different types of chemotaxis assays across diverse extractions of compounds or odorants to test whether C. elegans is attracted to P. scaber. We show that two different strains-the wild isolate PB306 and the laboratory-adapted strain N2 -are not attracted to P. scaber during either the dauer or adult life stages. Our results indicate that C. elegans was not attracted to chemical compounds or volatile odorants from P. scaber, providing valuable empirical evidence to suggest that any associations between these two species are likely opportunistic rather than specific phoresy.

Differences in parasite susceptibility and costs of resistance between naturally exposed and unexposed host populations.

It is generally assumed that resistance to parasitism entails costs. Consequently, hosts evolving in the absence of parasites are predicted to invest less in costly resistance mechanisms than hosts consistently exposed to parasites. This prediction has, however, rarely been tested in natural populations. We studied the susceptibility of three naïve, three parasitized and one recently isolated Asellus aquaticus isopod populations to an acanthocephalan parasite. We found that parasitized populations, with the exception of the isopod population sympatric with the parasite strain used, were less susceptible to the parasite than the naïve populations. Exposed but uninfected (resistant) isopods from naïve populations, but not from parasitized populations, exhibited greater mortality than controls, implying that resistance entails survival costs primarily for naïve isopods. These results suggest that parasites can drive the evolution of host resistance in the wild, and that co-existence with parasites may increase the cost-effectiveness of defence mechanisms.

Acanthocephalan size and sex affect the modification of intermediate host colouration.

For trophically transmitted parasites, transitional larval size is often related to fitness. Larger parasites may have higher establishment success and/or adult fecundity, but prolonged growth in the intermediate host increases the risk of failed transmission via natural host mortality. We investigated the relationship between the larval size of an acanthocephalan (Acanthocephalus lucii) and a trait presumably related to transmission, i.e. altered colouration in the isopod intermediate host. In natural collections, big isopods harboured larger worms and had more modified (darker) abdominal colouration than small hosts. Small isopods infected with a male parasite tended to have darker abdominal pigmentation than those infected with a female, but this difference was absent in larger hosts. Female size increases rapidly with host size, so females may have more to gain than males by remaining in and growing mutually with small hosts. In experimental infections, a large total parasite volume was associated with darker host respiratory operculae, especially when it was distributed among fewer worms. Our results suggest that host pigment alteration increases with parasite size, albeit differently for male and female worms. This may be an adaptive strategy if, as parasites grow, the potential for additional growth decreases and the likelihood of host mortality increases.