Effects of three Caribbean cleaner shrimps on ectoparasitic monogeneans in a semi-natural environment

Most research on cleaning symbioses on coral reefs has focused on fish clients being cleaned by smaller fishes. While many shrimps and other crustaceans are reported as cleaners, whether they remove parasites from fish hosts and can effectively regulate populations of ectoparasites is unclear. The effects of Pederson shrimp (Periclimenes pedersoni), spotted shrimp (P. yucatanicus), and banded coral shrimp (Stenopus hispidus), on the parasitic monogenean Neobenedenia melleni on a host reef fish, blue tang (Acanthurus coeruleus), were investigated. The abundance and size of N. melleni from fish with and without access to shrimps in a semi-natural macrocosm was quantified. P. pedersoni had a strong effect on both the abundance and size of parasites. In contrast, P. yucatanicus and S. hispidus had no effect on the abundance of parasites but had a small yet statistically significant effect on average size. These data suggest that P. pedersoni can play a significant role in the biological regulation of at least some ectoparasites on Caribbean reef fishes, but further suggest that some other shrimps regarded as “cleaners” may have little or no effectiveness at removing parasites and underscore the need for further verification before this term is applied.     

Host preference and specialization in Gnathia sp., a common parasitic isopod of coral reef fishes

A gnathiid species (Crustacea: Isopoda; one of the most common ectoparasites of coral reef fishes) from the Great Barrier Reef, Australia, was allowed to choose among fishes from three different families to feed on (using two species of fishes per family). Gnathiids showed a strong preference for labrids, rarely feeding on pomacentrids or apogonids. In a separate experiment, gnathiid host preference did not vary among three labrid fish species. Gnathiids that fed on labrids had higher survival than those that fed on apogonids. Male gnathiids that fed on labrids also moulted to the adult stage more quickly. This suggests that host specialization and local adaptation might be occurring between these ectoparasites and their host fishes at the host fish family level.     

Evaluation of gill nets, fyke nets, and mark-recapture methods to estimate the number of Hirudinea and Crustacea on fish.

Twenty species of fishes (n = 20,759) were collected from Dauphin Lake, Manitoba, Canada, to determine the types and numbers of ectoparasites they harbored. Counts of ectoparasites on fishes collected with different gear were compared to evaluate different methods of collection and to estimate rates of recruitment of ectoparasites by fishes. Ectoparasites were found on 11 species of fishes and the majority of these were parasitic leeches (Myzobdella moorei, Cystobranchus verilli, and Placobdella montifera) and parasitic Crustacea (Argulus appendiculosus and Lernaea cyprinacea). Some fishes also were infested by neascus-type metacercariae (blackspot) or had tumors (lymphocystis). The prevalence of ectoparasites was correlated with the abundance, feeding habits, and spatial distribution of fish species. Argulus appendiculosus and blackspot were more prevalent on benthic fishes, whereas M. moorei and tumors were more prevalent on limnetic fishes. Mark-recapture records showed that fishes occupying shallow (less than or equal to 1.5 m) water had a higher prevalence of infestation and 28 of 29 infected fishes caught by gill nets were captured in shallow water. Placobdella montifera was the only ectoparasite found on fishes from deep (1.5-3.5 m) water and the only species that was acquired by fishes previously released with no ectoparasite (2 of 239 fishes). The littoral zone (less than or equal to 1.5 m) comprises only 14% of the surface area and 3% of the volume of Dauphin Lake, yet 72% of all gill-netted fishes harboring ectoparasites were collected there. Intensities of ectoparasites estimated from gill net and pound net samples were similar, but prevalence of ectoparasites estimated from samples obtained with gill nets was lower.     

Effect of Australian tea tree oil on Gyrodactylus spp. infection of the three-spined stickleback Gasterosteus aculeatus

Gyrodactylus spp. infections of commercially farmed fishes are responsible for significant economic losses. Existing treatments have proved uneconomic, stressful to the fishes, and ecologically damaging. Essential oils are naturally occurring compounds that exhibit a wide range of anti-microbial and anti-fungal activities. This study explored the possibility of using Australian tea tree (Melaleuca alternifolia) oil (TTO) to treat Gyrodactylus spp. infection on the three-spined stickleback Gasterosteus aculeatus. In the presence of 0.01 % Tween 80 as an emulsifier, TTO treatments at concentrations between 3 and 30 ppmv (parts per million by volume) lowered the prevalence and significantly reduced the parasite burden of sticklebacks naturally infected with Gyrodactylus spp. In addition, Tween 80 alone exhibited parasiticidal activity against Gyrodactylus spp. These findings show the potential of TTO in combination with Tween 80 as an effective treatment of Gyrodactylus spp. infection of fishes.     

The nested structure of marine cleaning symbiosis: is it like flowers and bees?

In a given area, plant-animal mutualistic interactions form complex networks that often display nestedness, a particular type of asymmetry in interactions. Simple ecological and evolutionary factors have been hypothesized to lead to nested networks. Therefore, nestedness is expected to occur in other types of mutualisms as well. We tested the above prediction with the network structure of interactions in cleaning symbiosis at three reef assemblages. In this type of interaction, shrimps and fishes forage on ectoparasites and injured tissues from the body surface of fish species. Cleaning networks show strong patterns of nestedness. In fact, after controlling for species richness, cleaning networks are even more nested than plant-animal mutualisms. Our results support the notion that mutualisms evolve to a predictable community-level structure, be it in terrestrial or marine communities.     

Infections of Gyrodactylus bullatarudis and Gyrodactylus turnbulli on guppies (Poecilia reticulata) in Trinidad.

Gyrodactylus bullatarudis Turnbull, 1956, and Gyrodactylus turnbulli Harris, 1986, are recorded from guppies (Poecilia reticulata) from the northern mountains of Trinidad. Mixed infections of the 2 species were found at 9 localities. Gyrodactylus turnbulli had a predominantly posterior distribution on the fishes, whereas G. bullatarudis was more anteriorly distributed. This is the first record of these species from guppies collected from within their original range.     

鱼类三代虫研究进展

三代虫是一类常见的鱼类体表寄生虫,广泛寄生于各种鱼类,其危害近年有加剧之势,对鱼类养殖业造成较大威胁。本文从三代虫的分类方法、种群动态和引起寄主免疫反应等方面综述了鱼类三代虫研究现状及发展趋势。     

Ecological niche differentiation between native and non-native shrimps in the northern Baltic Sea

Invasions of non-native species are modifying global biodiversity but the ecological mechanisms underlying invasion processes are still not well understood. A degree of niche separation of non-native and sympatric native species can possibly explain the success of novel species in their new environment. In this study, we quantified experimentally and in situ the environmental niche space of caridean shrimps (native Crangon crangon and Palaemon adspersus, non-native Palaemon elegans) inhabiting the northern Baltic Sea. Field studies showed that the non-native P. elegans had wider geographical range compared to native species although the level of habitat specialization was similar in both Palaemon species. There were clear differences in shrimp habitat occupancy with P. elegans inhabiting lower salinity areas and more eutrophicated habitats compared to the native species. Consequently, the non-native shrimp has occupied large areas of the northern Baltic Sea that were previously devoid of the native shrimps. Experiments demonstrated that the non-native shrimp had higher affinity to vegetated substrates compared to native species. The study suggests that the abilities of the non-native shrimp to thrive in more stressful habitats (lower salinity, higher eutrophication), that are sub-optimal for native shrimps, plausibly explain the invasion success of P. elegans.     

Adaptive patterns of osmotic and ionic regulation, and the invasion of fresh water by the palaemonid shrimps

To evaluate trends in the osmoregulatory behavior of neotropical, palaemonid shrimps, we investigated osmotic and ionic regulatory patterns in five species of Palaemon or Macrobrachium. The species' life histories depend on saline water to differing degrees, their habitats ranging from the marine/intertidal (P. northropi), through estuaries (P. pandaliformis) to coastal, freshwater streams (M. olfersii, M. potiuna) and inland, continental river systems (M. brasiliense). Hemolymph osmolality, chloride, sodium and magnesium concentrations were measured in shrimps exposed to experimental media ranging from fresh water (<0.5 per thousand ) to concentrated seawater (42 per thousand ) for up to 10 days. The marine and estuarine Palaemon species exhibit well-developed hyper/hypo-osmotic, sodium and chloride regulatory capabilities in mid-range salinities, tending to hyperconform in low salinities. The freshwater Macrobrachium species show variable hyperosmotic, sodium and chloride regulatory capacities, tending to hypoconform or unable to survive at higher salinities. All species hyper-regulate magnesium in fresh water, but hyporegulate strongly in saline media. Palaemonids from the saline habitats show the strongest osmoregulatory capabilities, and fresh water may have been gradually invaded by ancestral species with similar regulatory capacity. However, this regulatory plasticity has been lost to varying degrees in extant freshwater species.     

A preliminary study of Cu-, Cd- and Zn-binding components in the hepatopancreas of Palaemon elegans (Crustacea: Decapoda)

Three low molecular weight, metal-binding components have been isolated from the hepatopancreas of the shrimp Palaemon elegans. The two larger components P-I (11-15,000) and P-II (4-6000) were associated with large amounts of copper in field-collected and copper-exposed shrimps and with cadmium in shrimps exposed to elevated Cd concentrations. A smaller component, P-III was associated with zinc. The recovery of these components was dependent upon the use of a protease inhibitor and the reducing agent mercaptoethanol (2-M) during the separation procedure. Copper, zinc and cadmium are not evenly distributed between individual tissues of P. elegans, the highest concentrations occurring in the hepatopancreas, gills and eyes.     

Geographic Variation in the Behaviour of the Cleaner Fish Labroides dimidiatus (Labridae)

Geographical variation in the outcome of interspecific interactions has a range of proximate ecological causes. For instance, cleaning interactions between coral reef fishes can result in benefits for both the cleaner and its clients. However, because both parties can cheat and because the rewards of cheating may depend on the local abundance of ectoparasites on clients, the interaction might range from exploitative to mutualistic. In a comparative analysis of behavioural measures of the association between the cleaner fish Labroides dimidiatus and all its client species, we compared cleaning interactions between two sites on the Great Barrier Reef that differ with respect to mean ectoparasite abundance. At Heron Island, where client fish consistently harbour fewer ectoparasites, client species that tended to pose for cleaners were more likely to receive feeding bites by cleaners than client species that did not pose for cleaners. This was not the case at Lizard Island, where ectoparasites are significantly more abundant. Client fish generally spent more time posing for cleaners at Lizard Island than their conspecifics at Heron Island. However, fish at Heron Island were inspected longer on average by cleaners than conspecifics at Lizard Island, and they incurred more bites and swipes at their sides per unit time from cleaners. These and other differences between the two sites suggest that the local availability of ectoparasites as a food source for cleaners may determine whether clients will seek cleaning, and whether cleaners will feed on parasites or attempt to feed on client mucus. The results suggest that cleaning symbiosis is a mosaic of different outcomes driven by geographical differences in the benefits for both participants.     

The mitochondrial genome of Gyrodactylus derjavinoides (Platyhelminthes: Monogenea)--a mitogenomic approach for Gyrodactylus species and strain identification

Systematists and evolutionary biologists are constantly on the lookout for new sources of characters to discriminate amongst taxa and estimate interrelationships within and between taxa. Entire mitochondrial genomes provide a wealth of data, both at the nucleotide and amino acid level. Molecular markers are of particular utility when applied to small, morphologically conserved taxa, as is the case for many monogenean ectoparasites of fish. Gyrodactylus species display a considerable degree of anatomical conservatism, complicating diagnostics based solely on morphology, and some are significant pests of wild and cultured fish. Here we sequenced the complete mitochondrial genome of Gyrodactylus derjavinoides Malmberg, Collins, Cunningham & Behiar 2007, one of the most frequently found gyrodactylid species on salmonids in Scandinavia, and compared it with the recently published genomes of Gyrodactylus salaris Malmberg, 1957 and Gyrodactylus thymalli Zitnan 1960. Through comparative sliding window analysis we identified regions of high sequence variability and designed new primer sequences. In total, 6 new primer pairs have been developed, amplifying fragments of cox1, cox3, nad1, nad2, nad4, nad5 and atp6. Together, they amplify regions capturing almost half the nucleotide variability present in the complete mitochondrial genome. These degenerate primers should also work for other Gyrodactylus species parasitizing salmonids. In addition, we developed a multiplex assay that simultaneously amplifies four fragments in a single PCR reaction. Besides the diagnostic value, these fragments can be used for studying the transmission dynamics of Gyrodactylus, providing crucial information for an improved understanding of the spread and epidemiology of these important fish pathogens.     

鱼类三代虫分子生物学的研究进展

三代虫是一类常见的鱼类体外寄生虫,绝大多数种类寄生于鱼类的体表和鳃,大量寄生可导致苗种甚至成鱼大批死亡,或引起其他病原感染而致继发性鱼病,造成严重的经济损失.本文从三代虫目前的分类学概况、DNA分类学和条形码技术、核糖体基因及线粒体基因的研究等方面概述了鱼类三代虫分子生物学的研究现状,为三代虫及扁形动物的分子生物学研究及其应用提供有用的资料.     

Predatory fishes affect trophic cascades and apparent competition in temperate reefs

We provide evidence for a trophic cascade involving apex predators and mesopredators of marine temperate reefs, lingcod and rockfish, respectively. We measured spatio-temporal variation in the relative abundance of lingcod, subadult rockfish and two shrimp groups eaten by rockfish (Pandalus sp. and three smaller-bodied genera aggregated). Lingcod had an indirect positive effect on shrimps, as mediated by the direct negative effects of lingcod on rockfish and of rockfish on shrimps. These top-down effects on shrimps, however, were stronger for Pandalus than for small-bodied shrimps. Further, abundances of Pandalus and small-bodied shrimps were negatively correlated and the latter had a stronger positive effect on rockfish, suggesting that rockfish mediated asymmetrical apparent competition between shrimps. Our results indicate mechanisms by which predatory fishes may influence the structure of marine communities.     

Can Mixed-Species Groups Reduce Individual Parasite Load? A Field Test with Two Closely Related Poeciliid Fishes (Poecilia reticulata and Poecilia picta)

Predation and parasitism are two of the most important sources of mortality in nature. By forming groups, individuals can gain protection against predators but may increase their risk of being infected with contagious parasites. Animals might resolve this conflict by forming mixed-species groups thereby reducing the costs associated with parasites through a relative decrease in available hosts. We tested this hypothesis in a system with two closely related poeciliid fishes (Poecilia reticulata and Poecilia picta) and their host-specific monogenean ectoparasites (Gyrodactylus spp.) in Trinidad. Fish from three different rivers were sampled from single and mixed-species groups, measured and scanned for Gyrodactylus. The presence and abundance of Gyrodactylus were lower when fish of both species were part of mixed-species groups relative to single-species groups. This is consistent with the hypothesis that mixed-species groups provide a level of protection against contagious parasites. We discuss the importance of potentially confounding factors such as salinity and individual fish size.     

Utilizing stomach content and faecal DNA analysis techniques to assess the feeding behaviour of largemouth bass Micropterus salmoides and bluegill Lepomis macrochirus

In this study, the feeding behaviour of the non‐native invasive predatory fishes largemouth bass Micropterus salmoides and bluegill Lepomis macrochirus was studied in the Ezura River, a northern tributary of Lake Biwa, Japan. Prey composition was estimated based on visual examination of stomach contents and faecal DNA analysis to determine feeding habits of these predatory fishes. Stomach content analysis showed that native fishes (e.g. ayu Plecoglossus altivelis and gobies Rhinogobius spp.) and shrimps (e.g. Palaemon paucidens) were the major prey items for M. salmoides, while snails, larval Chironomidae and submerged macrophytes were the dominant prey items of L. macrochirus. Micropterus salmoides tended to select larger fish in the case of crucian carp Carassius spp., but smaller fishes in the case of P. altivelis and Rhinogobius spp. Faecal DNA analyses revealed prey compositions similar to those identified in predator stomach contents, and identified additional prey species not detected in stomach content inspection. This study demonstrated that both stomach content inspection and DNA‐based analysis bear several inherent shortcomings and advantages. The former method is straightforward, although identification of species can be inaccurate or impossible, whereas the latter method allows for accurate species identification, but cannot distinguish prey size or stage. Hence, integration of morphology‐based and DNA‐based methods can provide more reliable estimates of foraging habits of predatory fishes.     

“Cleaner” shrimps?

In the western North Atlantic, some shrimps of the genusPericlimenes interact with fishes. Accoring to prevailing wisdom, these shrimps “clean” the fishes (i.e. they remove parasites, diseased tissue, or detritus from their exposed surfaces). With one exception, the numerous literature entries recite anecdotal evidence. The only report based on empirical studies has dismissed the notion that “cleaner” shrimps perform the services attributed to them, leaving the nature of the relationship unresolved.     

Structure of the parasite communities of a coral reef fish assemblage (Labridae): testing ecological and phylogenetic host factors

The role of ecological and phylogenetic processes is fundamental to understanding how parasite communities are structured. However, for coral reef fishes, such information is almost nonexistent. In this study, we analyzed the structure of the parasite communities based on composition, richness, abundance, and biovolume of ecto- and endoparasites of 14 wrasse species (Labridae) from Lizard Island, Great Barrier Reef, Australia. We determine whether the structure of the parasite communities from these fishes was related to ecological characteristics (body size, abundance, swimming ability, and diet) and/or the phylogenetic relatedness of the hosts. We examined 264 fishes from which almost 37,000 individual parasites and 98 parasite categories (types and species) were recorded. Gnathiid and cestode larvae were the most prevalent and abundant parasites in most fishes. Mean richness, abundance, and biovolume of ectoparasites per fish species were positively correlated with host body size only after controlling for the host phylogeny, whereas no such correlation was found for endoparasites with any host variable. Because most ectoparasites have direct transmission, one possible explanation for this pattern is that increased space (host body size) may increase the colonization and recruitment of ectoparasites. However, endoparasites generally have indirect transmission that can be affected by many other variables, such as number of prey infected and rate of parasite transmission.     

A new gyrodactylid species from Cobitis granoei (Rendahl) (Cobitidae) in central China

Gyrodactylus granoei n. sp. (Monogenea: Gyrodactylidae) is described from the fins and body surface of the spine loach, Cobitis granoei (Rendahl) (Cobitidae), in central China. It resembles a suite of species from cyprinid and cobitid fishes that have short, compact hamuli, a ventral bar with no obvious anterolateral projections, a linguiform posterior membrane, a male copulatory organ with small hooks in multiple rows, a simple cylindrical dorsal bar, and short marginal hooks, with an expanded sickle heel. Of these, the new species resembles most closely Gyrodactylus micracanthus Hukuda, 1940 from Misgurnus anguillicaudatus (Cantor) (Cobitidae), but it is identified by the length of the hamuli and the morphology of dorsal and ventral bars. When searched using BLAST, sequence data (829 bp) spanning the ITS1, 5.8s, and ITS2 region did not return an identical match; close similarity (82-88%) was found with sequenced members of the subgenus Gyrodactylus. It is suggested that the new species is part of a freshwater lineage that has radiated successfully among cyprinid fishes in North America, Europe, and Asia, and some of their predator and amphibian neighbors.     

Diversity in the Monogenea and Digenea: does lifestyle matter?

If the cestodes are excluded, then the parasitic platyhelminths of fishes divide neatly into the external and monoxenous Monogenea and the internal and heteroxenous Digenea. Both groups have apparently had long associations of coevolution, host switching and adaptation with fishes and have become highly successful in their respective habitats. Current estimates of species richness for the two groups suggest that they may be remarkably similar. Here we consider the nature of the diversity of the Monogenea and Digenea of fishes in terms of richness of species and higher taxa to determine what processes may be responsible for observed differences. The Monogenea includes at least two super-genera (Dactylogyrus and Gyrodactylus) each of which has hundreds of species; no comparable genera are found in the Digenea. Possible reasons for this difference include the higher host specificity of monogeneans and their shorter generation time. If allowance is made for the vagaries of taxonomic 'lumping' and 'splitting', then there are probably comparable numbers of families of monogeneans and digeneans in fishes. However, the nature of the families differ profoundly. Richness in higher taxa (families) in the Digenea is explicable in terms of processes that appear to have been unimportant in the Monogenea. Readily identifiable sources of diversity in the Digenea are: recolonisation of fishes by taxa that arose in association with tetrapods; adoption of new sites within hosts; adoption of new diets and feeding mechanisms; adaptations relating to the exploitation of ecologically similar groups of fishes and second intermediate hosts; and adaptations relating to the exploitation of phylogenetic lineages of molluscs. In contrast, most higher- level monogenean diversity (other than that associated with the subclasses) relates principally to morphological specialisation for attachment by the haptor.