Sex‐selective Predation by Threespine Sticklebacks on Sea Lice: A Novel Cleaning Behaviour

Cleaning interactions have been described in a wide range of fish species and other taxa. We observed a novel cleaning behaviour during a study of the transmission dynamics of sea lice (Lepeophtheirus salmonis) between juvenile pink salmon (Oncorhynchus gorbuscha) and threespine sticklebacks (Gasterosteus aculeatus) in the Broughton Archipelago, British Columbia, Canada. Experiments showed that sticklebacks significantly reduced the number of sea lice on individual juvenile salmon. Adult female lice were preferentially consumed by sticklebacks, and gravid female lice also experienced egg string cropping. Overall, 76% of gravid female lice experienced either consumption, egg string cropping, or both by sticklebacks. This preference by sticklebacks for female parasites may stem from female lice being larger than males and the added nutritional value of egg strings on gravid females. Cleaning by sticklebacks can potentially have an impact on sea louse populations on wild juvenile salmon.     

Allee effects may slow the spread of parasites in a coastal marine ecosystem

Allee effects are thought to mediate the dynamics of population colonization, particularly for invasive species. However, Allee effects acting on parasites have rarely been considered in the analogous process of infectious disease establishment and spread. We studied the colonization of uninfected wild juvenile Pacific salmon populations by ectoparasitic salmon lice (Lepeophtheirus salmonis) over a 4-year period. In a data set of 68,376 fish, we observed 85 occurrences of precopular pair formation among 1,259 preadult female and 613 adult male lice. The probability of pair formation was dependent on the local abundance of lice, but this mate limitation is likely offset somewhat by mate-searching dispersal of males among host fish. A mathematical model of macroparasite population dynamics that incorporates the empirical results suggests a high likelihood of a demographic Allee effect, which can cause the colonizing parasite populations to die out. These results may provide the first empirical evidence for Allee effects in a macroparasite. Furthermore, the data give a rare detailed view of Allee effects in colonization dynamics and suggest that Allee effects may dampen the spread of parasites in a coastal marine ecosystem.     

Sea lice escape predation on their host

Parasites seldom have predators but often fall victim to those of their hosts. How parasites respond to host predation can have important consequences for both hosts and parasites, though empirical investigations are rare. The exposure of wild juvenile salmon to sea lice (Lepeophtheirus salmonis) from salmon farms allowed us to study a novel ecological interaction: the response of sea lice to predation on their juvenile pink and chum salmon hosts by two salmonid predators-coho smolts and cut-throat trout. In approximately 70% of trials in which a predator consumed a parasitized prey, lice escaped predation by swimming or moving directly onto the predator. This trophic transmission is strongly male biased, probably because behaviour and morphology constrain female movement and transmission. These findings highlight the potential for sea lice to be transmitted up marine food webs in areas of intensive salmon aquaculture, with implications for louse population dynamics and predatory salmonid health.     

Influence of host ecology and morphology on the diversity of Neotropical bird lice

Host‐parasite systems can be powerful arenas in which to explore factors influencing community structure. We used a comparative approach to examine the influence of host ecology and morphology on the diversity of chewing lice (Insecta: Phthiraptera) among 52 species of Peruvian birds. For each host species we calculated two components of parasite diversity: 1) cumulative species richness, and 2) mean abundance. We tested for correlations between these parasite indices and 13 host ecological and morphological variables. Host ecological variables included geographic range size, local population density, and microhabitat use. Host morphological variables included body mass, plumage depth, and standard dimensions of bill, foot and toenail morphology, all of which could influence the efficiency of anti‐parasite grooming. Data were analysed using statistical and comparative methods that control for sampling effort and host phylogeny. None of the independent host variables correlated with louse species richness when treated as a dependent variable. When richness was treated as an independent variable, however, it was positively correlated with mean louse abundance. Host body mass was also positively correlated with mean louse abundance. When louse richness and host body mass were held constant, mean louse abundance correlated negatively with the degree to which the upper mandible of the host's bill overhangs the lower mandible. This correlation suggests that birds with longer overhangs are better at controlling lice during preening. We propose a specific functional hypothesis in which preening damages lice by exerting a shearing force between the overhang and the tip of the lower mandible. This study is the first to suggest a parasite‐control function of such a detailed component of bill morphology across species. Avian biologists have traditionally focused almost exclusively on bills as tools for feeding. We suggest that the adaptive radiation of bill morphology should be reinterpreted with both preening and feeding in mind.     

Sea lice and salmon population dynamics: effects of exposure time for migratory fish

The ecological impact of parasite transmission from fish farms is probably mediated by the migration of wild fishes, which determines the period of exposure to parasites. For Pacific salmon and the parasitic sea louse, Lepeophtheirus salmonis, analysis of the exposure period may resolve conflicting observations of epizootic mortality in field studies and parasite rejection in experiments. This is because exposure periods can differ by 2–3 orders of magnitude, ranging from months in the field to hours in experiments. We developed a mathematical model of salmon–louse population dynamics, parametrized by a study that monitored naturally infected juvenile salmon held in ocean enclosures. Analysis of replicated trials indicates that lice suffer high mortality, particularly during pre-adult stages. The model suggests louse populations rapidly decline following brief exposure of juvenile salmon, similar to laboratory study designs and data. However, when the exposure period lasts for several weeks, as occurs when juvenile salmon migrate past salmon farms, the model predicts that lice accumulate to abundances that can elevate salmon mortality and depress salmon populations. The duration of parasite exposure is probably critical to salmon–louse population dynamics, and should therefore be accommodated in coastal planning and management where fish farms are situated on wild fish migration routes.     

Sea louse infection of juvenile sockeye salmon in relation to marine salmon farms on Canada's west coast

Background

Pathogens are growing threats to wildlife. The rapid growth of marine salmon farms over the past two decades has increased host abundance for pathogenic sea lice in coastal waters, and wild juvenile salmon swimming past farms are frequently infected with lice. Here we report the first investigation of the potential role of salmon farms in transmitting sea lice to juvenile sockeye salmon (Oncorhynchus nerka).

Methodology/Principal Findings

We used genetic analyses to determine the origin of sockeye from Canada''s two most important salmon rivers, the Fraser and Skeena; Fraser sockeye migrate through a region with salmon farms, and Skeena sockeye do not. We compared lice levels between Fraser and Skeena juvenile sockeye, and within the salmon farm region we compared lice levels on wild fish either before or after migration past farms. We matched the latter data on wild juveniles with sea lice data concurrently gathered on farms. Fraser River sockeye migrating through a region with salmon farms hosted an order of magnitude more sea lice than Skeena River populations, where there are no farms. Lice abundances on juvenile sockeye in the salmon farm region were substantially higher downstream of farms than upstream of farms for the two common species of lice: Caligus clemensi and Lepeophtheirus salmonis, and changes in their proportions between two years matched changes on the fish farms. Mixed-effects models show that position relative to salmon farms best explained C. clemensi abundance on sockeye, while migration year combined with position relative to salmon farms and temperature was one of two top models to explain L. salmonis abundance.

Conclusions/Significance

This is the first study to demonstrate a potential role of salmon farms in sea lice transmission to juvenile sockeye salmon during their critical early marine migration. Moreover, it demonstrates a major migration corridor past farms for sockeye that originated in the Fraser River, a complex of populations that are the subject of conservation concern.     

A model of salmon louse production in Norway: effects of increasing salmon production and public management measures.

Salmon lice Lepeophtheirus salmonis Kr?yer have caused disease problems in farmed Atlantic salmon Salmo salar L. since the mid-1970s in Norway. High infection intensities and premature return of wild sea trout Salmo trutta L. were first reported in 1992. Later emaciated wild Atlantic salmon smolts carrying large amounts of lice have been observed both in fjords and offshore. The Norwegian Animal Health Authority regulations to control the problem, which came into operation in 1998, included compulsory louse level monitoring in farms and maximum legal numbers of lice per fish. Here, we present a model of salmon louse egg production in Norway and show that the effect of the current public management strategy is critically dependent on the yearly increase in salmon production. This is because the infection pressure is the product of the number of fish in the system, and the number of lice per fish. Due to the much larger number of farmed than wild salmonids, it is highly likely that lice originating from farmed salmon infect wild stock. Estimated tolerance limits for wild salmonids vary widely, and the level of louse egg production in farms which would be needed to decimate wild populations is not known. Two possible thresholds for total lice egg production are investigated: (1) 1986 to 1987 level (i.e. before adverse effects on sea trout were recorded), and (2) a level corresponding to a doubling of the estimated natural infection pressure. The farm lice per fish limits that would have to be observed to keep louse production within the 2 thresholds are calculated for the period 1986 to 2005. A steady decrease in the permitted number of lice per fish may keep the total louse production stable, but the number of salmon required for verification of lice numbers will increase as the prevalence to be verified is decreased. At threshold (2), the model estimated that lice limits should have been 0.05 louse per fish in 1999. This would require 60 fish from each pen to be collected, anaesthetised and examined for a good estimate at a confidence level of 95%. Such sample numbers are likely to be opposed by farmers. The use of national delousing programs to solve the problem is discussed.     

The characteristics of epidemics and invasions with thresholds

In this paper we report the development of a highly efficient numerical method for determining the principal characteristics (velocity, leading edge width, and peak height) of spatial invasions or epidemics described by deterministic one-dimensiohal reaction-diffusion models whose dynamics include a threshold or Allee effect. We prove that this methodology produces the correct results for single-component models which are generalizations of the Fisher model, and then demonstrate by numerical experimentation that analogous methods work for a wide class of epidemic and invasion models including the S-I and S-E-I epidemic models and the Rosenzweig-McArthur predator-prey model. As examplary application of this approach we consider the atto-fox effect in the classic reaction-diffusion model of rabies in the European fox population and show that the appropriate threshold for this model is within an order of magnitude of the peak disease incidence and thus has potentially significant effects on epidemic properties. We then make a careful re-parameterisation of the model and show that the velocities calculated with realistic thresholds differ surprisingly little from those calculated from threshold-free models. We conclude that an appropriately thresholded reaction-diffusion model provides a robust representation of the initial epidemic wave and thus provides a sound basis on which to begin a properly mechanistic modelling enterprise aimed at understanding the long-term persistence of the disease.     

Chemoreception in the salmon louse Lepeophtheirus salmonis: an electrophysiology approach

The search for effective and long-term solutions to the problems caused by salmon lice Lepeophtheirus salmonis (Kr?yer, 1837) has increasingly included biological/ecological mechanisms to combat infestation. One aspect of this work focuses on the host-associated stimuli that parasites use to locate and discriminate a compatible host. In this study we used electrophysiological recordings made directly from the antennule of adult lice to investigate the chemosensitivity of L. salmonis to putative chemical attractants from fish flesh, prepared by soaking whole fish tissue in seawater. There was a clear physiological response to whole fish extract (WFX) with threshold sensitivity at a dilution of 10 . When WFX was size fractionated, L. salmonis showed the greatest responses to the water-soluble fractions containing compounds between 1 and 10 kDa. The results suggest that the low molecular weight, water-soluble compounds found in salmon flesh may be important in salmon lice host choice.     

Evolution of virulence under intensive farming: salmon lice increase skin lesions and reduce host growth in salmon farms

Parasites rely on resources from a host and are selected to achieve an optimal combination of transmission and virulence. Human‐induced changes in parasite ecology, such as intensive farming of hosts, might not only favour increased parasite abundances, but also alter the selection acting on parasites and lead to life‐history evolution. The trade‐off between transmission and virulence could be affected by intensive farming practices such as high host density and the use of antiparasitic drugs, which might lead to increased virulence in some host–parasite systems. To test this, we therefore infected Atlantic salmon (Salmo salar) smolts with salmon lice (Lepeophtheirus salmonis) sampled either from wild or farmed hosts in a laboratory experiment. We compared growth and skin damage (i.e. proxies for virulence) of hosts infected with either wild or farmed lice and found that, compared to lice sampled from wild hosts in unfarmed areas, those originating from farmed fish were more harmful; they inflicted more skin damage to their hosts and reduced relative host weight gain to a greater extent. We advocate that more evolutionary studies should be carried out using farmed animals as study species, given the current increase in intensive food production practices that might be compared to a global experiment in parasite evolution.     

Size matters for lice on birds: Coevolutionary allometry of host and parasite body size

Body size is one of the most fundamental characteristics of all organisms. It influences physiology, morphology, behavior, and even interspecific interactions such as those between parasites and their hosts. Host body size influences the magnitude and variability of parasite size according to Harrison's rule (HR: positive relationship between host and parasite body sizes) and Poulin's Increasing Variance Hypothesis (PIVH: positive relationship between host body size and the variability of parasite body size). We analyzed parasite–host body size allometry for 581 species of avian lice (～15% of known diversity) and their hosts. We applied phylogenetic generalized least squares (PGLS) methods to account for phylogenetic nonindependence controlling for host and parasite phylogenies separately and variance heterogeneity. We tested HR and PIVH for the major families of avian lice (Ricinidae, Menoponidae, Philopteridae), and for distinct ecological guilds within Philopteridae. Our data indicate that most families and guilds of avian lice follow both HR and PIVH; however, ricinids did not follow PIVH and the “body lice” guild of philopterid lice did not follow HR or PIVH. We discuss mathematical and ecological factors that may be responsible for these patterns, and we discuss the potential pervasiveness of these relationships among all parasites on Earth.     

Modeling Parasite Dynamics on Farmed Salmon for Precautionary Conservation Management of Wild Salmon

Conservation management of wild fish may include fish health management in sympatric populations of domesticated fish in aquaculture. We developed a mathematical model for the population dynamics of parasitic sea lice (Lepeophtheirus salmonis) on domesticated populations of Atlantic salmon (Salmo salar) in the Broughton Archipelago region of British Columbia. The model was fit to a seven-year dataset of monthly sea louse counts on farms in the area to estimate population growth rates in relation to abiotic factors (temperature and salinity), local host density (measured as cohort surface area), and the use of a parasiticide, emamectin benzoate, on farms. We then used the model to evaluate management scenarios in relation to policy guidelines that seek to keep motile louse abundance below an average three per farmed salmon during the March–June juvenile wild Pacific salmon (Oncorhynchus spp.) migration. Abiotic factors mediated the duration of effectiveness of parasiticide treatments, and results suggest treatment of farmed salmon conducted in January or early February minimized average louse abundance per farmed salmon during the juvenile wild salmon migration. Adapting the management of parasites on farmed salmon according to migrations of wild salmon may therefore provide a precautionary approach to conserving wild salmon populations in salmon farming regions.     

Pigments,Parasites and Personalitiy: Towards a Unifying Role for Steroid Hormones?

A surging interest in the evolution of consistent trait correlations has inspired research on pigment patterns as a correlate of behavioural syndromes, or "animal personalities". Associations between pigmentation, physiology and health status are less investigated as potentially conserved trait clusters. In the current study, lice counts performed on farmed Atlantic salmon Salmo salar naturally infected with ectoparasitic sea lice Lepeophtheirus salmonis showed that individual fish with high incidence of black melanin-based skin spots harboured fewer female sea lice carrying egg sacs, compared to less pigmented fish. There was no significant association between pigmentation and lice at other developmental stages, suggesting that host factors associated with melanin-based pigmentation may modify ectoparasite development to a larger degree than settlement. In a subsequent laboratory experiment a strong negative correlation between skin spots and post-stress cortisol levels was revealed, with less pigmented individuals showing a more pronounced cortisol response to acute stress. The observation that lice prevalence was strongly increased on a fraction of sexually mature male salmon which occurred among the farmed fish further supports a role for steroid hormones as mediators of reduced parasite resistance. The data presented here propose steroid hormones as a proximate cause for the association between melanin-based pigmentation and parasites. Possible fundamental and applied implications are discussed.     

How do toxicants affect epidemiological dynamics?

Populations are formed of their constituent interacting individuals, each with their own respective within‐host biological processes. Infection not only spreads within the host organism but also spreads between individuals. Here we propose and study a multilevel model which links the within‐host statuses of immunity and parasite density to population epidemiology under sublethal and lethal toxicant exposure. We analyse this nested model in order to better understand how toxicants impact the spread of disease within populations. We demonstrate that outbreak of infection within a population is completely determined by the level of toxicant exposure, and that it is maximised by intermediate toxicant dosage. We classify the population epidemiology into five phases of increasing toxicant exposure and calculate the conditions under which disease will spread, showing that there exists a threshold toxicant level under which epidemics will not occur. In general, higher toxicant load results in either extinction of the population or outbreak of infection. The within‐host statuses of the individual host also determine the outcome of the epidemic at the population level. We discuss applications of our model in the context of environmental epidemiology, predicting that increased exposure to toxicants could result in greater risk of epidemics within ecological systems. We predict that reducing sublethal toxicant exposure below our predicted safe threshold could contribute to controlling population level disease and infection.     

Transmission dynamics of parasitic sea lice from farm to wild salmon

Marine salmon farming has been correlated with parasitic sea lice infestations and concurrent declines of wild salmonids. Here, we report a quantitative analysis of how a single salmon farm altered the natural transmission dynamics of sea lice to juvenile Pacific salmon. We studied infections of sea lice (Lepeophtheirus salmonis and Caligus clemensi) on juvenile pink salmon (Oncorhynchus gorbuscha) and chum salmon (Oncorhynchus keta) as they passed an isolated salmon farm during their seaward migration down two long and narrow corridors. Our calculations suggest the infection pressure imposed by the farm was four orders of magnitude greater than ambient levels, resulting in a maximum infection pressure near the farm that was 73 times greater than ambient levels and exceeded ambient levels for 30 km along the two wild salmon migration corridors. The farm-produced cohort of lice parasitizing the wild juvenile hosts reached reproductive maturity and produced a second generation of lice that re-infected the juvenile salmon. This raises the infection pressure from the farm by an additional order of magnitude, with a composite infection pressure that exceeds ambient levels for 75 km of the two migration routes. Amplified sea lice infestations due to salmon farms are a potential limiting factor to wild salmonid conservation.     

Exocrine glands of Lepeophtheirus salmonis (Copepoda: Caligidae): Distribution,developmental appearance,and site of secretion

Exocrine glands of blood‐feeding parasitic copepods are believed to be important in host immune response modulation and inhibition of host blood coagulation, but also in the production of substances for integument lubrication and antifouling. In this study, we aimed to characterize the distribution of different types of salmon louse (Lepeophtheirus salmonis) exocrine glands and their site of secretion. The developmental appearance of each gland type was mapped and genes specifically expressed by glands were identified. Three types of tegumental (teg 1–3) glands and one labial gland type were found. The first glands to appear during development were teg 1 and teg 2 glands. They have ducts extending both dorsally and ventrally suggested to be important in lubricating the integument. Teg 1 glands were found to express two astacin metallopeptidases and a gene with fibronectin II domains, while teg 2 glands express a heme peroxidase. The labial glands were first identified in planktonic copepodids, with reservoirs that allows for storage of glandular products. The last gland type to appear during development was named teg 3 and was not seen before the preadult I stage when the lice become more virulent. Teg 3 glands have ducts ending ventrally at the host‐parasite contact area, and may secrete substances important for the salmon lice virulence. Salmon lice teg 3 and labial glands are thus likely to be especially important in the host‐parasite interaction. Proteins secreted from the salmon louse glands to its salmonid host skin or blood represents a potential interface where the host immune system can meet and elicit effective responses to sea lice antigens. The present study thus represents a fundamental basis for further functional studies and identification of possible vaccine candidates. J. Morphol. 277:1616–1630, 2016. © 2016 Wiley Periodicals, Inc.     

Individual fish tank arrays in studies of Lepeophtheirus salmonis and lice loss variability

In studies of the salmon louse Lepeophtheirus salmonis (Kr?yer, 1837), experimental design is complicated by a highly variable and unpredictable lice loss among common experimental tanks and a substantial rate of host transfer within tanks. When fish hosting L. salmonis are maintained in individual tanks, unspecific effects such as host transfer, louse predation by cohabitant hosts and agonistic host interactions are excluded. This study suggests that it is possible to maintain Atlantic salmon Salmo salar infected with L. salmonis in an array of small, single fish tanks and, by doing so, provide an experimental system in which the loss of motile pre-adult and adult stages of L. salmonis is predictable. Here, lice can be collected shortly after detachment for detailed studies or to provide mortality curves of lice from individual fish. This represents an experimental approach improving precision in studies of L. salmonis, such as drug and vaccine efficacy assays, RNA interference (RNAi) studies and host-parasite interactions. The natural loss of pre-adult/adult L. salmonis from the system was higher for males than females. The loss of females appeared to be a process somewhat selective against large individuals. Inherent qualities of the host appeared to be of little significance in explaining the variability in loss of preadult/adult lice.     

Sea-lice infection models for fishes

As free-living sea-lice larvae are difficult to sample directly, lice abundances on fish have recently been used to study larvae in the water. In the KLV problem, juvenile wild salmon migrate past a salmon farm, and the change of infection with distance along the migration route is used to estimate larvae production from the farm. In the farm problem, time-varying infection of sea-cage fish is used to estimate the time-variation of free-living larvae in waters near the farm. Both inverse problems require good forward models for infection. In the farm problem, hosts are relatively large and lice pathogenesis is seldom mortal, whereas in the KLV problem hosts are small and lice-induced host mortality can affect lice abundance; thus, infection models for the farm problem are special cases of models for the KLV problem. Here I give an infection model for the KLV problem that explicitly includes lice clumping and host mortality, showing that Krkosek et al. (Proc R Soc B 272:689-696, 2005) (KLV) probably underestimated larvae production by the salmon farm, and further, that if lice development rates were known from laboratory data, lice abundance field data could be directly inverted for lice-induced host mortality during migration. If lice-induced host mortality is negligible, or if lice are Poisson distributed, infection models of arbitrary complexity reduce to Erlang models. I give two useful Erlang models with their solutions for non-zero initial conditions.     

Phoretic dispersal influences parasite population genetic structure

Dispersal is a fundamental component of the life history of most species. Dispersal influences fitness, population dynamics, gene flow, genetic drift and population genetic structure. Even small differences in dispersal can alter ecological interactions and trigger an evolutionary cascade. Linking such ecological processes with evolutionary patterns is difficult, but can be carried out in the proper comparative context. Here, we investigate how differences in phoretic dispersal influence the population genetic structure of two different parasites of the same host species. We focus on two species of host‐specific feather lice (Phthiraptera: Ischnocera) that co‐occur on feral rock pigeons (Columba livia). Although these lice are ecologically very similar, “wing lice” (Columbicola columbae) disperse phoretically by “hitchhiking” on pigeon flies (Diptera: Hippoboscidae), while “body lice” (Campanulotes compar) do not. Differences in the phoretic dispersal of these species are thought to underlie observed differences in host specificity, as well as the degree of host–parasite cospeciation. These ecological and macroevolutionary patterns suggest that body lice should exhibit more genetic differentiation than wing lice. We tested this prediction among lice on individual birds and among lice on birds from three pigeon flocks. We found higher levels of genetic differentiation in body lice compared to wing lice at two spatial scales. Our results indicate that differences in phoretic dispersal can explain microevolutionary differences in population genetic structure and are consistent with macroevolutionary differences in the degree of host–parasite cospeciation.