Altered neuronal activity in the visual processing region of eye-fluke-infected fish.

Fish, like most vertebrates, are dependent on vision to varying degrees for a variety of behaviours such as predator avoidance and foraging. Disruption of this key sensory system therefore should have some impact on the ability of fish to execute these tasks. Eye-flukes, such as Tylodelphys darbyi, often infect fish where they are known to inflict varying degrees of visual impairment. In New Zealand, T. darbyi infects the eyes of Gobiomorphus cotidianus, a freshwater fish, where it resides in the vitreous chamber between the lens and retina. Here, we investigate whether the presence of the parasite in the eye has an impact on neuronal information transfer using the c-Fos gene as a proxy for neuron activation. We hypothesized that the parasite would reduce visual information entering the eye and therefore result in lower c-Fos expression. Interestingly, however, c-Fos expression increased with T. darbyi intensity when fish were exposed to flashes of light. Our results suggest a mechanism for parasite-induced visual disruption when no obvious pathology is caused by infection. The more T. darbyi present the more visual stimuli the fish is presented with, and as such may experience difficulties in distinguishing various features of its external environment.

Hunger games: foraging behaviour and shelter use in fish under the context-dependent influence of parasitism.

Diseases, and the parasitic organisms that cause them, can impact aspects of ecosystems ranging from altering food web connectivity to population dynamics. Apart from interspecific interactions, parasites can affect how their hosts behave with conspecifics, such as during competition for resources. Fish are important hosts to a variety of parasite taxa that can, through physical impairment or invasion of sense organs, affect how they interact with conspecifics for food, territory, or mates. In New Zealand, the common bully Gobiomorphus cotidianus plays host to a variety of parasites, encysting throughout the body (Apatemon sp.) or residing within the eyes (Tylodelphys darbyi). We hypothesized that fish with lower levels of infection would secure territories closer to a food patch and be more likely to tolerate sharing that territory. Our experiments show that parasites infecting different areas may have variable impacts on how far the host positions itself from a food patch and the likelihood that it shares its territory. Fish with higher intensities of T. darbyi tended to be closer to the food patch, but Apatemon sp. did not show a similar pattern. Higher infection levels of both parasites were statistically associated with bullies being less likely to share territory. Further, bigger fish were less likely to share their territory at higher intensities infection, and we observed individual variation in a fish's response between trials. Our findings support that parasites matter in ecological interactions but also emphasize the context dependence of their effects.

Risky business: influence of eye flukes on use of risky microhabitats and conspicuousness of a fish host.

A prerequisite for a parasitic manipulation to be considered adaptive is that it confers a fitness benefit to the parasite, such as increased transmission to another host. These manipulations can involve alterations to a wide range of host phenotypic traits, including microhabitat choice. Eye flukes of the trematode family Diplostomidae use fish as intermediate hosts and must be transmitted by predation to a piscivorous bird. In New Zealand, the diplostomid Tylodelphys darbyi infects the eyes of a widespread endemic freshwater fish, the common bully Gobiomorphus cotidianus. Within the eye, T. darbyi metacercariae achieve large sizes and move freely about the aqueous and vitreous humors of the eye. We hypothesized that higher intensities of T. darbyi would (i) cause bullies to show increased activity and spend more time moving about in open space (i.e., more conspicuous, risky microhabitat) and (ii) reduce their ability to compete for shelter with fish harboring lower infection levels. Our experiments showed that heavily infected fish were more active and spent more time in the open, although the effect was age-dependent, with immature fish displaying decreases in activity and time spent in the open with increasing intensities of infection. We also demonstrated that heavily infected female bullies have a lower probability of using shelter, but males show the opposite pattern. It is possible that using more risky microhabitats increases the likelihood of the fish being eaten by the parasite's predatory avian definitive hosts. However, our findings indicate that age- and sex-dependent effects call for a more nuanced interpretation.

Parasitological research in the molecular age.

New technological methods, such as rapidly developing molecular approaches, often provide new tools for scientific advances. However, these new tools are often not utilized equally across different research areas, possibly leading to disparities in progress between these areas. Here, we use empirical evidence from the scientific literature to test for potential discrepancies in the use of genetic tools to study parasitic vs non-parasitic organisms across three distinguishable molecular periods, the allozyme, nucleotide and genomics periods. Publications on parasites constitute only a fraction (<5%) of the total research output across all molecular periods and are dominated by medically relevant parasites (especially protists), particularly during the early phase of each period. Our analysis suggests an increasing complexity of topics and research questions being addressed with the development of more sophisticated molecular tools, with the research focus between the periods shifting from predominantly species discovery to broader theory-focused questions. We conclude that both new and older molecular methods offer powerful tools for research on parasites, including their diverse roles in ecosystems and their relevance as human pathogens. While older methods, such as barcoding approaches, will continue to feature in the molecular toolbox of parasitologists for years to come, we encourage parasitologists to be more responsive to new approaches that provide the tools to address broader questions.

DISTRIBUTION AND DIVERSITY OF DIPLOSTOMIDS IN NEW ZEALAND.

Parasitism is one of the most common consumer strategies and contributes a large portion to biological diversity. Trematodes in the family Diplostomidae are common in freshwater ecosystems worldwide, often residing in the eyes or brain of fish and then infecting fish-eating birds as adults. As a result, some species have broad geographic distributions due to the bird host's motility. In contrast to the cosmopolitan nature of diplostomids, only a single species, Tylodelphys darbyi, has been identified in New Zealand to date, and only from the South Island. Tylodelphys darbyi has a 3-host life cycle consisting of an unidentified snail, a freshwater fish (Gobiomorphus cotidianus), and the Australasian crested grebe (Podiceps cristatus australis). To date, T. darbyi has been found in 2 locations, Lake Hayes, in the eyes of G. cotidianus, and Lake Wanaka, adults recovered from grebes. Considering the near ubiquity of the fish host in New Zealand, it is likely the bird, listed as nationally vulnerable, is the limiting factor in the range of T. darbyi. Up to 10 G. cotidianus were sampled from 10 mountain lakes known to have populations of grebe in the Otago and Canterbury regions of New Zealand's South Island. The eyes of all fish were examined and any metacercariae present were set aside for genetic analysis. In addition to expanding the known range of T. darbyi to at least 4 water bodies across the South Island, 2 new taxa of diplostomid were identified. A lens-infecting metacercariae clustered with Diplostomum spathaceum, while the metacercariae from the humor clustered with Diplostomum baeri.

Temporal dynamics of species associations in the parasite community of European eels, Anguilla anguilla, from a coastal lagoon.

The resilience of biological communities is of central importance in ecology, but is difficult to investigate in nature. Parasite communities in individual hosts provide good model systems, as they allow a level of replication usually not possible with free-living communities. Here, using temporal data (2005-2017) on the communities of endohelminth parasites in European eels, Anguilla anguilla, from brackish-water lagoons in Italy, we test the resilience of interspecific associations to changes in the abundance of some parasite species and the disappearance of others. While most parasite species displayed changes in abundance over time, three trematodes that were present in the early years, two of which at high abundance, completely disappeared from the parasite community by the end of the study period. Possibly other host species required for the completion of their life cycles have declined in abundance, perhaps due to environmental changes. However, despite these marked changes to the overall community, pairwise correlations in abundance among the three most common parasite species (all trematodes) were stable over time and remained mostly unaffected by what happened to other species. We explore possible reasons for these resilient species associations within a temporally unstable parasite community inhabiting a mostly stable host population.