Effects of host migration, diversity and aquaculture on sea lice threats to Pacific salmon populations

Animal migrations can affect disease dynamics. One consequence of migration common to marine fish and invertebrates is migratory allopatry-a period of spatial separation between adult and juvenile hosts, which is caused by host migration and which prevents parasite transmission from adult to juvenile hosts. We studied this characteristic for sea lice (Lepeophtheirus salmonis and Caligus clemensi) and pink salmon (Oncorhynchus gorbuscha) from one of the Canada's largest salmon stocks. Migratory allopatry protects juvenile salmon from L. salmonis for two to three months of early marine life (2-3% prevalence). In contrast, host diversity facilitates access for C. clemensi to juvenile salmon (8-20% prevalence) but infections appear ephemeral. Aquaculture can augment host abundance and diversity and increase parasite exposure of wild juvenile fish. An empirically parametrized model shows high sensitivity of salmon populations to increased L. salmonis exposure, predicting population collapse at one to five motile L. salmonis per juvenile pink salmon. These results characterize parasite threats of salmon aquaculture to wild salmon populations and show how host migration and diversity are important factors affecting parasite transmission in the oceans.     

Does increased abundance of sea lice influence survival of wild Atlantic salmon post‐smolt?

A synthesis of results from two projects was assessed to analyse possible influence of sea lice Lepeophtheirus salmonis on marine Atlantic salmon Salmo salar survival. During the years 1992–2004, trawling for wild migrating post-smolts was performed in Trondheimsfjord, a fjord in which no Atlantic salmon aquaculture activity is permitted. Prevalence and intensity of sea lice infections on migrating wild post-smolts differed between years. A correlation analysis between 1 sea-winter (SW) Atlantic salmon catch statistics from the River Orkla (a Trondheimsfjord river) and sea lice infections on the migrating smolts in the Trondheimsfjord was not significant. Up to 2% reduction in adult returns due to sea-lice infection was expected. In addition, experimental releases from 1996 to 1998 with individually tagged groups of hatchery-reared Atlantic salmon smolts given protection against sea-lice infection was performed. Higher recaptures of adult Atlantic salmon from 1998 treated smolts compared to the control group may correspond to high abundance of sea lice found on the wild smolt, and may indicate influence on post-smolt mortality. These studies indicate that post-smolt mortality in Trondheimsfjord is marginally influenced by sea lice infection; however, the methods for assessing wild smolt mortality might be insufficient. Higher infections of sea lice farther out in the fjord may indicate more loss in Atlantic salmon returns in some years.     

Reduced growth in wild juvenile sockeye salmon Oncorhynchus nerka infected with sea lice

Daily growth rings were examined in the otoliths of wild juvenile sockeye salmon Oncorhynchus nerka to determine whether infection by ectoparasitic sea lice Caligus clemensi and Lepeophtheirus salmonis was associated with reduced host body growth, an important determinant of survival. Over 98% of the sea lice proved to be C. clemensi and the fish that were highly infected grew more slowly than uninfected individuals. Larger fish also grew faster than smaller fish. Finally, there was evidence of an interaction between body size and infection status, indicating the potential for parasite‐mediated growth divergence.     

Critical thresholds in sea lice epidemics: evidence, sensitivity and subcritical estimation

Host density thresholds are a fundamental component of the population dynamics of pathogens, but empirical evidence and estimates are lacking. We studied host density thresholds in the dynamics of ectoparasitic sea lice (Lepeophtheirus salmonis) on salmon farms. Empirical examples include a 1994 epidemic in Atlantic Canada and a 2001 epidemic in Pacific Canada. A mathematical model suggests dynamics of lice are governed by a stable endemic equilibrium until the critical host density threshold drops owing to environmental change, or is exceeded by stocking, causing epidemics that require rapid harvest or treatment. Sensitivity analysis of the critical threshold suggests variation in dependence on biotic parameters and high sensitivity to temperature and salinity. We provide a method for estimating the critical threshold from parasite abundances at subcritical host densities and estimate the critical threshold and transmission coefficient for the two epidemics. Host density thresholds may be a fundamental component of disease dynamics in coastal seas where salmon farming occurs.     

Parasites of wrasse (Labridae) in inshore waters of west Scotland stocked as cleaner fish of sea lice (Caligidae) on farmed Atlantic salmon

The prevalence, abundance and intensity of protistan and metazoan parasites were examined in the labrid fishes Ctenolabrus rupestris, Centrolabrus exoletus, Crenilabrus melops, Labrus bergylta and L. mixtus in west Scotland. The 22 parasite species identified do not appear to be a major threat to farmed Atlantic salmon. Few mortalities of wrasse stocked on salmon farms were due to resident parasites or to transfers from salmon.     

Differences in susceptibility to sea lice infection between a sea run and a freshwater resident population of brown trout

Two experimental groups comprising mixed Norwegian sea run and freshwater resident brown trout Salmo trutta were infected with sea lice Lepeophtheirus salmonis in replicate tanks. Comparison of mean abundance and louse development between the sea run and resident groups revealed highly significant differences in lice abundance. The resident trout had an average abundance ± of 6·3±0·37 and 6·6±0·43 lice whilst the sea trout had an average abundance of 3·5 ±0·25 and 3·3 ±0·28 lice 29 days post infection at 9° C. No differences in development of lice, of either sex, were detected between the groups. As host groups were naive to sea lice at the start of the experiment, this suggests that there was a significant difference in susceptibility to sea lice infection between them, which may be genetically determined.     

Patterns of host–parasite associations in tropical lice and their passerine hosts in Cameroon

Coevolutionary processes that drive the patterns of host–parasite associations can be deduced through congruence analysis of their phylogenies. Feather lice and their avian hosts have previously been used as typical model systems for congruence analysis; however, such analyses are strongly biased toward nonpasserine hosts in the temperate zone. Further, in the Afrotropical region especially, cospeciation studies of lice and birds are entirely missing. This work supplements knowledge of host–parasite associations in lice using cospeciation analysis of feather lice (genus Myrsidea and the Brueelia complex) and their avian hosts in the tropical rainforests of Cameroon. Our analysis revealed a limited number of cospeciation events in both parasite groups. The parasite–host associations in both louse groups were predominantly shaped by host switching. Despite a general dissimilarity in phylogeny for the parasites and hosts, we found significant congruence in host–parasite distance matrices, mainly driven by associations between Brueelia lice and passerine species of the Waxbill (Estrildidae) family, and Myrsidea lice and their Bulbul (Pycnonotidae) host species. As such, our study supports the importance of complex biotic interactions in tropical environments.     

Oust the louse: leaping behaviour removes sea lice from wild juvenile sockeye salmon Oncorhynchus nerka

We conducted a manipulative field experiment to determine whether the leaping behaviour of wild juvenile sockeye salmon Oncorhynchus nerka dislodges ectoparasitic sea lice Caligus clemensi and Lepeophtheirus salmonis by comparing sea‐lice abundances between O. nerka juveniles prevented from leaping and juveniles allowed to leap at a natural frequency. Juvenile O. nerka allowed to leap had consistently fewer sea lice after the experiment than fish that were prevented from leaping. Combined with past research, these results imply potential costs due to parasitism and indicate that the leaping behaviour of juvenile O. nerka does, in fact, dislodge sea lice.     

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.     

Coldwater fish in a warm water world: Implications for predation of salmon smolts during estuary transit

1. Predator–prey systems face intensifying pressure from human exploitation and a warming climate with implications for where and how natural resource management can successfully intervene. We hypothesized young salmon migrating to the Pacific Ocean face a seasonally intensifying predator gauntlet when warming water temperature intensifies a multiple predator effect (MPE) from Striped Bass Morone saxatilis and Largemouth Bass Micropterus salmoides. We evaluated this hypothesis using data synthesis and simulation modeling.
2. Contemporary studies based on acoustically tagged fish reaffirmed older observations that Chinook Salmon smolts must transit the Delta before water temperature reaches 20°C or mortality will be nearly 100%. Striped Bass attack rates on tethered smolts were insensitive to distance from shore and water temperature, whereas Largemouth Bass attack rates were highest near shorelines in warm water, supporting the temporal aspect of the hypothesis. Whether the combined effects of the two predators produce an MPE remains unconfirmed due to limitations on quantifying salmon behavior.
3. We used multiple simulation models to try to reconstruct the empirical relationship between smolt survival and water temperature. Simulations reinforced attack rate results, but could not recreate the temperature dependence in smolt survival except at higher than observed temperatures. We propose three hypotheses for why and recommend discerning among them should be a focus of research.
4. We found significant linear relationships between monthly mean inflow to the Delta from each of its two largest tributaries and monthly mean water temperatures along associated salmon migration routes, but these relationships can be nonlinear, with most of the correlation occurring at low inflows when water temperature is largely controlled by air temperature and day length. As the global climate warms, changed circumstances in predator–prey relationships may present important challenges when managing species vulnerable to extinction in addition to presently more abundant species.

     

Evidence for carry-over effects of predator exposure on pathogen transmission potential

Accumulating evidence indicates that species interactions such as competition and predation can indirectly alter interactions with other community members, including parasites. For example, presence of predators can induce behavioural defences in the prey, resulting in a change in susceptibility to parasites. Such predator-induced phenotypic changes may be especially pervasive in prey with discrete larval and adult stages, for which exposure to predators during larval development can have strong carry-over effects on adult phenotypes. To the best of our knowledge, no study to date has examined possible carry-over effects of predator exposure on pathogen transmission. We addressed this question using a natural food web consisting of the human malaria parasite Plasmodium falciparum, the mosquito vector Anopheles coluzzii and a backswimmer, an aquatic predator of mosquito larvae. Although predator exposure did not significantly alter mosquito susceptibility to P. falciparum, it incurred strong fitness costs on other key mosquito life-history traits, including larval development, adult size, fecundity and longevity. Using an epidemiological model, we show that larval predator exposure should overall significantly decrease malaria transmission. These results highlight the importance of taking into account the effect of environmental stressors on disease ecology and epidemiology.     

Time series covering up to four decades reveals major changes and drivers of marine growth and proportion of repeat spawners in an Atlantic salmon population

1. Wild Atlantic salmon populations have declined in many regions and are affected by diverse natural and anthropogenic factors. To facilitate management guidelines, precise knowledge of mechanisms driving population changes in demographics and life history traits is needed.
2. Our analyses were conducted on (a) age and growth data from scales of salmon caught by angling in the river Etneelva, Norway, covering smolt year classes from 1980 to 2018, (b) extensive sampling of the whole spawning run in the fish trap from 2013 onwards, and (c) time series of sea surface temperature, zooplankton biomass, and salmon lice infestation intensity.
3. Marine growth during the first year at sea displayed a distinct stepwise decline across the four decades. Simultaneously, the population shifted from predominantly 1SW to 2SW salmon, and the proportion of repeat spawners increased from 3 to 7%. The latter observation is most evident in females and likely due to decreased marine exploitation. Female repeat spawners tended to be less catchable than males by anglers.
4. Depending on the time period analyzed, marine growth rate during the first year at sea was both positively and negatively associated with sea surface temperature. Zooplankton biomass was positively associated with growth, while salmon lice infestation intensity was negatively associated with growth.
5. Collectively, these results are likely to be linked with both changes in oceanic conditions and harvest regimes. Our conflicting results regarding the influence of sea surface temperature on marine growth are likely to be caused by long‐term increases in temperature, which may have triggered (or coincided with) ecosystem shifts creating generally poorer growth conditions over time, but within shorter datasets warmer years gave generally higher growth. We encourage management authorities to expand the use of permanently monitored reference rivers with complete trapping facilities, like the river Etneelva, generating valuable long‐term data for future analyses.

     

Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species

The dispersal of parasites is critical for epidemiology, and the interspecific vectoring of parasites when species share resources may play an underappreciated role in parasite dispersal. One of the best examples of such a situation is the shared use of flowers by pollinators, but the importance of flowers and interspecific vectoring in the dispersal of pollinator parasites is poorly understood and frequently overlooked. Here, we use an experimental approach to show that during even short foraging periods of 3 h, three bumblebee parasites and two honeybee parasites were dispersed effectively onto flowers by their hosts, and then vectored readily between flowers by non-host pollinator species. The results suggest that flowers are likely to be hotspots for the transmission of pollinator parasites and that considering potential vector, as well as host, species will be of general importance for understanding the distribution and transmission of parasites in the environment and between pollinators.     

Long-term variation in influenza A virus prevalence and subtype diversity in migratory mallards in northern Europe

Data on long-term circulation of pathogens in wildlife populations are seldom collected, and hence understanding of spatial–temporal variation in prevalence and genotypes is limited. Here, we analysed a long-term surveillance series on influenza A virus (IAV) in mallards collected at an important migratory stopover site from 2002 to 2010, and characterized seasonal dynamics in virus prevalence and subtype diversity. Prevalence dynamics were influenced by year, but retained a common pattern for all years whereby prevalence was low in spring and summer, but increased in early autumn with a first peak in August, and a second more pronounced peak during October–November. A total of 74 haemagglutinin (HA)/neuraminidase (NA) combinations were isolated, including all NA and most HA (H1–H12) subtypes. The most common subtype combinations were H4N6, H1N1, H2N3, H5N2, H6N2 and H11N9, and showed a clear linkage between specific HA and NA subtypes. Furthermore, there was a temporal structuring of subtypes within seasons based on HA phylogenetic relatedness. Dissimilar HA subtypes tended to have different temporal occurrence within seasons, where the subtypes that dominated in early autumn were rare in late autumn, and vice versa. This suggests that build-up of herd immunity affected IAV dynamics in this system.     

Biology of parasite populations: population dynamics of bothriocephalids (Cestoda-Pseudophyllidea) in teleostean fish

Relationships between sympatric populations of four species of Cestoda belonging to the genus Bothriocephalus ( B. barbarus. B. gregarius, B. funiculus and B. scorpii ) and populations of their respective hosts Scophthalmus rhombus, Pserra maxima, Ciliata mustela and Myoxocephalus scorpius were investigated. The parasites were overdispersed within their host populations. The mean intensities of B. burbarus were 1.59 ( s.d. =0.83) in the Mediterranean (Gulf of Lions) and 1.25 ( s.d. =0.53) in the Atlantic (coasts of Brittany). The mean intensities of B. gregarius were 62.3 ( s.d. =49.7) in the Mediterranean and 14.06 ( s.d. =18.48) in the Atlantic, compared to 1.78 ( s.d. =0.3) for B. funiculus and 21.6 ( s.d. =17.3) for B. scorpii .
The distribution of prevalence of B. gregarius corresponded to a lognormal distribution while those of B. barbatus and B. fwticulus corresponded to negative binomials. No differences in infection could be related to host sex. The parasitization of B. gregariusdepended on host size. In brill, infection by E. barbatus was independent of host size and remained stable after the fish reached 180mm in length. Parasitization of turbot by E. gregarius was lower in young fish (≤110–150 mm) and increased with the host size. Compared to the Atlantic populations of B. gregarius and B. barbatus, the Mediterranean populations were more frequently and intensively infected. The differences in the population dynamics of B. gregarius and B. barbarus would appear to depend on whether or not the life cycle involves a paratenic host.     

Host–parasite coevolution: Partitioning the effects of natural selection and environmental change using coupled Price equations

George Price showed how the effects of natural selection and environmental change could be mathematically partitioned. This partitioning may be especially useful for understanding host–parasite coevolution, where each species represents the environment for the other species. Here, we use coupled Price equations to study this kind of antagonistic coevolution. We made the common assumption that parasites must genetically match their host''s genotype to avoid detection by the host''s self/nonself recognition system, but we allowed for the possibility that non‐matching parasites have some fitness. Our results show how natural selection on one species results in environmental change for the other species. Numerical iterations of the model show that these environmental changes can periodically exceed the changes in mean fitness due to natural selection, as suggested by R.A. Fisher. Taken together, the results give an algebraic dissection of the eco‐evolutionary feedbacks created during host–parasite coevolution.     

Starvation reveals the cause of infection-induced castration and gigantism

Parasites often induce life-history changes in their hosts. In many cases, these infection-induced life-history changes are driven by changes in the pattern of energy allocation and utilization within the host. Because these processes will affect both host and parasite fitness, it can be challenging to determine who benefits from them. Determining the causes and consequences of infection-induced life-history changes requires the ability to experimentally manipulate life history and a framework for connecting life history to host and parasite fitness. Here, we combine a novel starvation manipulation with energy budget models to provide new insights into castration and gigantism in the Daphnia magna–Pasteuria ramosa host–parasite system. Our results show that starvation primarily affects investment in reproduction, and increasing starvation stress reduces gigantism and parasite fitness without affecting castration. These results are consistent with an energetic structure where the parasite uses growth energy as a resource. This finding gives us new understanding of the role of castration and gigantism in this system, and how life-history variation will affect infection outcome and epidemiological dynamics. The approach of combining targeted life-history manipulations with energy budget models can be adapted to understand life-history changes in other disease systems.     

Sexual antagonism for resistance and tolerance to infection in Drosophila melanogaster

A critical task in evolutionary genetics is to explain the persistence of heritable variation in fitness-related traits such as immunity. Ecological factors can maintain genetic variation in immunity, but less is known about the role of other factors, such as antagonistic pleiotropy, on immunity. Sexually dimorphic immunity—with females often being more immune-competent—may maintain variation in immunity in dioecious populations. Most eco-immunological studies assess host resistance to parasites rather than the host''s ability to maintain fitness during infection (tolerance). Distinguishing between resistance and tolerance is important as they are thought to have markedly different evolutionary and epidemiological outcomes. Few studies have investigated tolerance in animals, and the extent of sexual dimorphism in tolerance is unknown. Using males and females from 50 Drosophila melanogaster genotypes, we investigated possible sources of genetic variation for immunity by assessing both resistance and tolerance to the common bacterial pathogen Pseudomonas aeruginosa. We found evidence of sexual dimorphism and sexual antagonism for resistance and tolerance, and a trade-off between the two traits. Our findings suggest that antagonistic pleiotropy may be a major contributor to variation in immunity, with implications for host–parasite coevolution.     

The dynamics of preferential host switching: Host phylogeny as a key predictor of parasite distribution*

Parasites often jump to and become established in a new host species. There is much evidence that the probability of such host shifts decreases with increasing phylogenetic distance between donor and recipient hosts, but the consequences of such preferential host switching remain little explored. We develop a computational model to investigate the dynamics of parasite host shifts in the presence of this phylogenetic distance effect. In this model, a clade of parasites evolves on an evolving clade of host species where parasites can cospeciate with their hosts, switch to new hosts, speciate within hosts or become extinct. Our model predicts that host phylogenies are major determinants of parasite distributions across trees. In particular, we predict that trees consisting of few large clades of host species and those with fast species turnover should harbor more parasites than trees with many small clades and those that diversify more slowly. Within trees, large clades are predicted to exhibit a higher fraction of infected species than small clades. We discuss our results in the light of recent cophylogenetic studies in a wide range of host–parasite systems.     

Immunization of Atlantic salmon against the salmon louse: identification of antigens and effects on louse fecundity

Injection of extracts derived from adult caligid copepods induced a partial immunity to Lepeophtheirus salmonis in Atlantic salmon. Antigens were derived from the supernatant of adult lice extracts and were partially purified by Con A affinity chromatography. The antigens were also present in the pellet derived from adult lice extracts, Immunohistochemistry showed that antibodies present in the serum of rats immunized with the Con A purified extract bound predominantly to the gut of L. salmonis. Components of apparent sizes > 205 000, 165 000, 133 000, 130 000, 125 000, 114 000, 110 000, 96 000, 82 000, 78 000, 65 000, 46 000, 35 000, 31 000 and < 29 000 were present in the extract. Although the numbers of attached lice were initially higher on those fish in the immunized group, throughout the course of the challenge experiment the total numbers of lice did not vary greatly between the immunized or control groups of fish. Initially, an overall average of about 17 attached stages were recorded from each fish sampled and by the end of the experiment this figure had fallen to about five adult lice per fish. However, compared with control fish fewer gravid female lice were present on immunized fish and furthermore these lice possessed fewer eggs (P<0.01). No major differences in egg hatching success were recorded. Further exploitation of this would require the isolation and purification of the antigens responsible for the observed effects. The possibilities for the development of a salmon louse vaccine are promising.