The role of relatedness in structuring the social network of a wild guppy population

Parasite avoidance is increasingly considered to be a potential driving factor in animal migrations. In many marine and freshwater benthic fish, migration into a pelagic environment by developing larvae is a common life history trait that could reduce exposure to parasites during a critical window of developmental susceptibility. We tested this hypothesis on congeneric fish (family Galaxiidae, genus Galaxias) belonging to a closely related species complex sampled from coastal streams in southeastern New Zealand. Migratory Galaxias have larvae that migrate to pelagic marine environments, whereas the larvae of non-migratory species rear close to adult habitats with no pelagic larval phase. Both migratory and non-migratory fish are hosts to two species of skin-penetrating trematodes that cause spinal malformations and high mortality in young fish. Using generalized linear models within an Akaike information criterion and model averaging framework, we compared infection levels between migratory and non-migratory fish while taking into account body size and several other local factors likely to influence infection levels. For one trematode species, we found a significant effect of migration: for any given body length, migratory fish harboured fewer parasites than non-migratory fish. Also, no parasites of any kind were found in juvenile migratory fish sampled in spring shortly after their return to stream habitats. Our results demonstrate that migration spares juvenile fish from the debilitating parasites to which they would be exposed in adult stream habitats. Therefore, either the historical adoption of a migratory strategy in some Galaxias was an adaptation against parasitism, or it evolved for other reasons and now provides protection from infection as a coincidental side-effect.     

Weir removal in salmonid streams: implications, challenges and practicalities

Low-head dams and weirs can greatly limit the distribution and abundance of Atlantic salmon and other migratory salmonids in streams. Weirs can significantly increase the vulnerability of migratory fish to anglers, alter natural migration patterns, and exacerbate the effects of opportunistic predators. Overcrowding of fish at downstream pools can also facilitate the spread of parasites and infectious diseases, magnify the impact of pollution incidents, and increase the risk of mass mortalities, particularly at low flows. Not surprisingly, augmenting the accessible stream area constitutes one of the best ways to restore depleted salmonid populations. In this context, the removal of unused or illegal weirs can be an efficient, cheap solution to increase stream accessibility. Here, I examine some impacts of weirs on Atlantic salmon populations, and document with case studies the removal and breaching of weirs in several Iberian streams. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. Guest editors: R. L. Welcomme & G. Marmulla Hydropower, Flood Control and Water Abstraction: Implications for Fish and Fisheries     

Migratory birds have higher prevalence and richness of avian haemosporidian parasites than residents

Individuals of migratory species may be more likely to become infected by parasites because they cross different regions along their route, thereby being exposed to a wider range of parasites during their annual cycle. Conversely, migration may have a protective effect since migratory behaviour allows hosts to escape environments presenting a high risk of infection. Haemosporidians are one of the best studied, most prevalent and diverse groups of avian parasites, however the impact of avian host migration on infection by these parasites remains controversial. We tested whether migratory behaviour influenced the prevalence and richness of avian haemosporidian parasites among South American birds. We used a dataset comprising ~ 11,000 bird blood samples representing 260 bird species from 63 localities and Bayesian multi-level models to test the impact of migratory behaviour on prevalence and lineage richness of two avian haemosporidian genera (Plasmodium and Haemoproteus). We found that fully migratory species present higher parasite prevalence and higher richness of haemosporidian lineages. However, we found no difference between migratory and non-migratory species when evaluating prevalence separately for Plasmodium and Haemoproteus, or for the richness of Plasmodium lineages. Nevertheless, our results indicate that migratory behaviour is associated with an infection cost, namely a higher prevalence and greater variety of haemosporidian parasites.     

Timing is crucial for consequences of migratory connectivity

Migratory connectivity can have important consequences for individuals, populations and communities. We argue that most consequences not only depend on which sites are used but importantly also on when these are used and suggest that the timing of migration is characterised by synchrony, phenology, and consistency. We illustrate the importance of these aspects of timing for shaping the consequences of migratory connectivity on individual fitness, population dynamics, gene flow and community dynamics using examples from throughout the animal kingdom. Exemplarily for one specific process that is shaped by migratory connectivity and the timing of migration – the transmission of parasites and the dynamics of diseases – we underpin our arguments with a dynamic epidemiological network model of a migratory population. Here, we quantitatively demonstrate that variations in migration phenology and synchrony yield disease dynamics that significantly differ from a time‐neglecting case. Extending the original definition of migratory connectivity into a spatio‐temporal concept can importantly contribute to understanding the links migratory animals make across the globe and the consequences these may have both for the dynamics of their populations and the communities they visit throughout their journeys. Synthesis Migratory connectivity quantifies the links migrant animals make across the globe and these can have manifold consequences – from individual fitness, population dynamics, gene flow to transmission of pathogens and parasites. We show through the use of empirical examples and a conceptual model that these consequences not only depend on which sites are used but importantly also on when these are used. Therefore, we specify three dimensions of migration timing – phenology, synchrony and consistency, which describe the timing of migration 1) relative to development of key resources; 2) relative to the migration of other individuals; and 3) relative to previous migration events. Each of these dimensions can alter the consequences, but typically through different mechanisms.     

Animal migrations and parasitism: reciprocal effects within a unified framework

Migrations, i.e. the recurring, roundtrip movement of animals between distant and distinct habitats, occur among diverse metazoan taxa. Although traditionally linked to avoidance of food shortages, predators or harsh abiotic conditions, there is increasing evidence that parasites may have played a role in the evolution of migration. On the one hand, selective pressures from parasites can favour migratory strategies that allow either avoidance of infections or recovery from them. On the other hand, infected animals incur physiological costs that may limit their migratory abilities, affecting their speed, the timing of their departure or arrival, and/or their condition upon reaching their destination. During migration, reduced immunocompetence as well as exposure to different external conditions and parasite infective stages can influence infection dynamics. Here, we first explore whether parasites represent extra costs for their hosts during migration. We then review how infection dynamics and infection risk are affected by host migration, thereby considering parasites as both causes and consequences of migration. We also evaluate the comparative evidence testing the hypothesis that migratory species harbour a richer parasite fauna than their closest free-living relatives, finding general support for the hypothesis. Then we consider the implications of host migratory behaviour for parasite ecology and evolution, which have received much less attention. Parasites of migratory hosts may achieve much greater spatial dispersal than those of non-migratory hosts, expanding their geographical range, and providing more opportunities for host-switching. Exploiting migratory hosts also exerts pressures on the parasite to adapt its phenology and life-cycle duration, including the timing of major developmental, reproduction and transmission events. Natural selection may even favour parasites that manipulate their host's migratory strategy in ways that can enhance parasite transmission. Finally, we propose a simple integrated framework based on eco-evolutionary feedbacks to consider the reciprocal selection pressures acting on migratory hosts and their parasites. Host migratory strategies and parasite traits evolve in tandem, each acting on the other along two-way causal paths and feedback loops. Their likely adjustments to predicted climate change will be understood best from this coevolutionary perspective.     

Nematomorph parasites indirectly alter the food web and ecosystem function of streams through behavioural manipulation of their cricket hosts

Nematomorph parasites manipulate crickets to enter streams where the parasites reproduce. These manipulated crickets become a substantial food subsidy for stream fishes. We used a field experiment to investigate how this subsidy affects the stream community and ecosystem function. When crickets were available, predatory fish ate fewer benthic invertebrates. The resulting release of the benthic invertebrate community from fish predation indirectly decreased the biomass of benthic algae and slightly increased leaf break-down rate. This is the first experimental demonstration that host manipulation by a parasite can reorganise a community and alter ecosystem function. Nematomorphs are common, and many other parasites have dramatic effects on host phenotypes, suggesting that similar effects of parasites on ecosystems might be widespread.     

Detecting shifts of transmission areas in avian blood parasites: a phylogenetic approach

We investigated the degree of geographical shifts of transmission areas of vector-borne avian blood parasites (Plasmodium, Haemoproteus and Leucocytozoon) over ecological and evolutionary timescales. Of 259 different parasite lineages obtained from 5886 screened birds sampled in Europe and Africa, only two lineages were confirmed to have current transmission in resident bird species in both geographical areas. We used a phylogenetic approach to show that parasites belonging to the genera Haemoproteus and Leucocytozoon rarely change transmission area and that these parasites are restricted to one resident bird fauna over a long evolutionary time span and are not freely spread between the continents with the help of migratory birds. Lineages of the genus Plasmodium seem more freely spread between the continents. We suggest that such a reduced transmission barrier of Plasmodium parasites is caused by their higher tendency to infect migratory bird species, which might facilitate shifting of transmission area. Although vector-borne parasites of these genera apparently can shift between a tropical and a temperate transmission area and these areas are linked with an immense amount of annual bird migration, our data suggest that novel introductions of these parasites into resident bird faunas are rather rare evolutionary events.     

Being there and getting there: balancing the costs of migration against the benefits of changing habitat for North Sea plaice

To improve survival and reproductive success, many fish species have evolved migratory life‐histories, showing ontogenetic and/or seasonal changes in habitat use. Individuals move between different areas, each of which is 'best' for a particular activity, such as feeding, growing or spawning. The benefits of moving to a different habitat, however, have to be balanced against the costs of migration, so any behaviour that reduces the cost of movement would be expected to expand the migratory range and thereby increase the range of habitats that can be exploited.
Previous tracking experiments in the southern North Sea have shown that plaice selectively exploit the tidal streams to aid their spawning migration. Here we examine whether this behaviour is primarily (1) an energy‐saving strategy, or (2) a transport mechanism by which fish that are unable to navigate over long distances can be carried reliably between feeding and spawning grounds. Because selective tidal stream transport requires that fish remain stationary on the sea‐bed during the 'non‐transporting' tide, energetic calculations predict that this behaviour is beneficial only when the current speed exceeds a critical, size‐dependent, value. We have used detailed information about migratory behaviour from individual fish to calculate the metabolic costs and the likely reproductive benefits of different migratory strategies. Our results show that plaice use selective tidal stream transport only in areas where the tidal streams are suitably fast, indicating that this behaviour is primarily an energy saving strategy.     

Role of cellular response in elimination of the monogenean Neoheterobothrium hirame in Japanese flounder Paralichthys olivaceus

Adult worms of the blood-feeding monogenean parasite Neoheterobothrium hirame, which cause anemia in the Japanese flounder Paralichthys olivaceus, attach to the host fish by embedding their posterior part deeply into the host tissue. To investigate the possibility that cellular responses of the host fish can eliminate N. hirame, flounder were experimentally infected with N. hirame larvae and reared in either fed or starved conditions. Mature parasites were identified on the buccal cavity wall of the fish 33 d post-infection (Day 33). Monocytes/macrophages and granulocytes increased rapidly in the blood and infected sites after the appearance of mature parasites. These cells adhered to the tegument of the parasites. In addition, a few cells with large electron-dense granules (DGCs) were observed in the inflammatory foci. On Day 47, the tegument of some parasites collapsed partially and were phagocytosed by the infiltrated host cells. Some infiltrated cells adhered directly to the inner tissues of the parasites. On Day 54, in the fed fish group, the loss of the tegument led to damage of the parasites' inner tissue by a large number of infiltrated cells. In this group, the elimination of the parasites was noted from Day 47 to 54. These observations probably suggest that the cellular response of the host fish destructed the parasite's posterior part embedded in the tissue, thereby eliminating the parasites. On the other hand, a high mortality was observed in the starved group. The starved fish developed much more severe anemia than the fed fish, and the elimination of the parasites was not observed in this group. The results of the present study suggest that flounder can eliminate N. hirame if they are fed sufficiently.     

Vertebrate diets derived from trophically transmitted fish parasites in the Bothnian Bay

Parasites that are transmitted through predator–prey interactions may be used as indicators of trophic relationships between organisms. Yet, they are rarely used as such in the construction of topological (predator–prey) food webs. We constructed food webs of vertebrate trophic interactions using observed diet alone, trophically transmitted parasites alone, and the combination of the two based on data from 31 species of fish from the Bothnian Bay, Finland. The fish food web contained 530 links derived from observed diet, 724 links inferred from parasitism, and 1,058 links calculated from a combination of both stomach contents and parasites. This sub-web constructed from stomach contents had a mean of 17.1 links per fish species, while that using parasites had 23.4 links per fish. Combining the two diet indicators yielded 34.1 links per fish species, illustrating the complementarity of the two methods. Mean number of prey species per fish species was 12.5 using observed diet items, 15.8 using parasites, and 24.5 using both measures together. Mean number of predators per fish species was 7.4 using observed diet, 11.7 using parasites and 15.0 using both. A positive correlation was found between the mean number of parasites and the number of prey taxa in the diet among the fishes. Omnivorous fish had the highest diversity of both parasite species and prey items, while benthophagous fish had among the lowest. Mean total abundance and mean total prevalence of parasites correlated positively with fish size, with piscivores being the largest with the highest abundance and prevalence, while planktivores and benthivores had the lowest. Trophically transmitted parasites may be used to help construct vertebrate sub-webs and derive information about food web processes. Parasites alone provided equivalent if not more information than observed diet. However, resolution is improved by using parasites and observed diet together.     

Dominant parasites of fish in Georgia, USSR

Intensive fish breeding in artificial freshwater reservoirs and ponds is often accompanied by epidemics of invasive parasitic diseases. In the USSR, much attention is given to the study of fish parasites and diseases, revealing a range of protozoan and helminth parasites that can cause significant economic losses to the fish industry (Table I ; Refs 1-5).     

Ecosystem consequences of fish parasites*

In most aquatic ecosystems, fishes are hosts to parasites and, sometimes, these parasites can affect fish biology. Some of the most dramatic cases occur when fishes are intermediate hosts for larval parasites. For example, fishes in southern California estuaries are host to many parasites. The most common of these parasites, Euhaplorchis californiensis, infects the brain of the killifish Fundulus parvipinnis and alters its behaviour, making the fish 10–30 times more susceptible to predation by the birds that serve as its definitive host. Parasites like E. californiensis are embedded in food webs because they require trophic transmission. In the Carpinteria Salt Marsh estuarine food web, parasites dominate the links and comprise substantial amount of biomass. Adding parasites to food webs alters important network statistics such as connectance and nestedness. Furthermore, some free‐living stages of parasites are food items for free‐living species. For instance, fishes feed on trematode cercariae. Being embedded in food webs makes parasites sensitive to changes in the environment. In particular, fishing and environmental disturbance, by reducing fish populations, may reduce parasite populations. Indirect evidence suggests a decrease in parasites in commercially fished species over the past three decades. In addition, environmental degradation can affect fish parasites. For these reasons, parasites in fishes may serve as indicators of environmental impacts.     

Damage due to parasites in Mediterranean teleosts

Evaluation of damages by parasites in teleosts, even if underextimated in the past, is today one of the most used methods to understand the effective impact of a parasite on a certain ichtyc species. The damage caused by a parasite on the host could be classified into direct, with tissue changes, or indirect, with a decrease of the productive performances. Based on this, a preliminary difference could be traced distinguishing parasites that show a coevolution with their host species, characterized by a low damage, and those parasites that can occasionally infect new host species, showing a high degree of damage. In consideration of the damage, parasites can have different actions on the host: subtractive, irritative, mechanical, traumatic, toxic, dismetabolic, antigenic and foretic. Those parasites able to cause tissue changes must be furtherly classified considering the type of inflammation they evoke on tissues: ulcerous, catarral, haemorrhagic, necrotic and granulomatous. Some parasites are encysted in tissues without any host reaction. The fish response against parasite can be inflammatory, the most frequent, but also hyperplastic, metaplastic, neoplastic and immunitary. The paper goes through different tissue changes due to the main parasites of Mediterranean teleosts.     

A simple molecular technique for identifying marine host fish by sequencing blood-feeding parasites

Gnathiid isopods are common ectoparasites of fish on the Great Barrier Reef, Australia. While screening for appropriate markers for phylogenetic studies of gnathiids, we found that primers for 12S and 16S rDNA preferentially amplified the host fish DNA instead of gnathiid DNA. This amplification occurred even when using gnathiids that were not engorged with host blood and adult gnathiids that do not feed on fish blood. This method could be used in host-parasite studies to identify hosts without having to sample parasites directly from the host (which can be costly and requires considerable skill in a marine environment). Target ribosomal DNA sequences can be amplified from total DNA extracted from parasites that are captured in funnel traps or plankton tows. Sequence data from these can be used to identify the hosts that gnathiids were feeding on before capture.     

Escaping peril: perceived predation risk affects migratory propensity

Although migratory plasticity is increasingly documented, the ecological drivers of plasticity are not well understood. Predation risk can influence migratory dynamics, but whether seasonal migrants can adjust their migratory behaviour according to perceived risk is unknown. We used electronic tags to record the migration of individual roach (Rutilus rutilus), a partially migratory fish, in the wild following exposure to manipulation of direct (predator presence/absence) and indirect (high/low roach density) perceived predation risk in experimental mesocosms. Following exposure, we released fish in their lake summer habitat and monitored individual migration to connected streams over an entire season. Individuals exposed to increased perceived direct predation risk (i.e. a live predator) showed a higher migratory propensity but no change in migratory timing, while indirect risk (i.e. roach density) affected timing but not propensity showing that elevated risk carried over to alter migratory behaviour in the wild. Our key finding demonstrates predator-driven migratory plasticity, highlighting the powerful role of predation risk for migratory decision-making and dynamics.     

Flounder Parasites as Biological Tags

The use of fish-parasites as biological tags may become an efficient method of tracing the origin of some migratory fish. The helminth parasites of flounders Platichthys flesus (L.) from 2 estuaries and from the sea within a 40 mile range were recorded, and an attempt was made to explain the level of infestation of each species of parasite in the 3 localities in relation to their life-history and the physical nature of the environment. The flounders from the 3 localities were shown to have dissimilar parasite-faunas, and, therefore, it was possible to characterize the parasite-fauna for each of the 3 groups of flounders. Individual fish from each locality could be recognized by its parasite-fauna and especially by the level of certain indicator-parasites. Similarly, "foreign" flounders moving into a flounder population could be picked out by the markedly different composition of their parasite-fauna. Podocotyle sp. and Zoogonoides viviparus were useful indicator-parasites in this instance.     

Flying with diverse passengers: greater richness of parasitic nematodes in migratory birds

Environmental changes are simultaneously affecting parasitic diseases and animal migrations, making it important to understand the disease dynamics of migratory species, including their range of infections and investment into defences. There is an urgent need for such knowledge because migratory animals, especially birds, are important for pathogen transmission and also particularly sensitive to environmental changes. Here we compare the nematode species richness and relative immune investment (via relative spleen size) of almost 200 migratory and non‐migratory species within three diverse groups of birds (Anseriformes, Accipitriformes and Turdidae) with worldwide distributions and varied ecology. Our results provide the first large‐scale demonstration that migratory birds face greater challenge from macroparasites as they have significantly dissimilar nematode fauna and higher nematode species richness compared to non‐migratory species. Even though birds with relatively large spleens had more nematode species, there was no difference in relative spleen size between migratory and non‐migratory bird species. The physiological stress of migration can be exacerbated by the potential range of pathologies induced by their richer nematode communities, particularly in combination with environmental perturbations. Altered migration stemming from global changes can also have important consequences for nematode transmission. Synthesis Most studies on parasites of migratory birds versus non‐migratory birds focus upon blood parasites; here we compared the diversity of another important parasite group – nematodes (roundworms) in three orders of birds. We found for any given order, migratory species and species with proportionally larger spleens generally have a wider range of nematodes. It is unclear why migratory species harbour more nematode species. Global climate change is expected to influence both bird migration patterns and infectious diseases, which may increase host susceptibility to parasitism and also introduce diverse nematodes to new areas and potential hosts.     

Using "travel time" data to characterize the behavior of migrating animals

For migratory species, duration of migration, or "travel time," is often a critical variable in determining the cost of migration. Observed travel times are the result of both environmental factors such as air or water currents and the behavior of individuals. In an effort to distinguish among these components, I developed a migration model based on an advection-diffusion equation that characterizes population movements in terms of two biologically meaningful parameters: migration rate and rate of population spread. I applied the model to travel time data from juvenile chinook salmon (Onchorhynchus tshawytscha), which were tagged during their seaward migration. The tagged fish originated from three separate evolutionarily significant units (ESUs) as classified by the U. S. National Marine Fisheries Service. The model was expanded by allowing migration and diffusion rates to vary with fish length and river flow. Variability in travel times explained by these factors was strikingly similar from year to year within ESUs, and the migratory behavior revealed by the analysis was consistent with the life-history patterns that distinguish the ESUs. The approach presented here is easily adaptable to a wide range of migratory species and may be particularly useful for predicting how at-risk populations respond to variable conditions in regulated or otherwise disturbed migration habitats.