Brendan M. Connors

Effects of parasites from salmon farms on productivity of wild salmon

The ecological risks of salmon aquaculture have motivated changes to management and policy designed to protect wild salmon populations and habitats in several countries. In Canada, much attention has focused on outbreaks of parasitic copepods, sea lice (Lepeophtheirus salmonis), on farmed and wild salmon in the Broughton Archipelago, British Columbia. Several recent studies have reached contradictory conclusions on whether the spread of lice from salmon farms affects the productivity of sympatric wild salmon populations. We analyzed recently available sea lice data on farms and spawner–recruit data for pink (Oncorhynchus gorbuscha) and coho (Oncorhynchus kisutch) salmon populations in the Broughton Archipelago and nearby regions where farms are not present. Our results show that sea lice abundance on farms is negatively associated with productivity of both pink and coho salmon in the Broughton Archipelago. These results reconcile the contradictory findings of previous studies and suggest that management and policy measures designed to protect wild salmon from sea lice should yield conservation and fishery benefits.

Fish farms, parasites, and predators: implications for salmon population dynamics

For some salmon populations, the individual and population effects of sea lice (Lepeophtheirus salmonis) transmission from sea cage salmon farms is probably mediated by predation, which is a primary natural source of mortality of juvenile salmon. We examined how sea lice infestation affects predation risk and mortality of juvenile pink (Oncorhynchus gorbuscha) and chum (O. keta) salmon, and developed a mathematical model to assess the implications for population dynamics and conservation. A risk-taking experiment indicated that infected juvenile pink salmon accept a higher predation risk in order to obtain foraging opportunities. In a schooling experiment with juvenile chum salmon, infected individuals had increased nearest-neighbor distances and occupied peripheral positions in the school. Prey selection experiments with cutthroat trout (O. clarkii) predators indicated that infection reduces the ability of juvenile pink salmon to evade a predatory strike. Group predation experiments with coho salmon (O. kisutch) feeding on juvenile pink or chum salmon indicated that predators selectively consume infected prey. The experimental results indicate that lice may increase the rate of prey capture but not the handling time of a predator. Based on this result, we developed a mathematical model of sea lice and salmon population dynamics in which parasitism affects the attack rate in a type II functional response. Analysis of the model indicates that: (1) the estimated mortality of wild juvenile salmon due to sea lice infestation is probably higher than previously thought; (2) predation can cause a simultaneous decline in sea louse abundance on wild fish and salmon productivity that could mislead managers and regulators; and (3) compensatory mortality occurs in the saturation region of the type II functional response where prey are abundant because predators increase mortality of parasites but not overall predation rates. These findings indicate that predation is an important component of salmon-louse dynamics and has implications for estimating mortality, reducing infection, and developing conservation policy.

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.

The false classification of extinction risk in noisy environments

Abundance trends are the basis for many classifications of threat and recovery status, but they can be a challenge to interpret because of observation error, stochastic variation in abundance (process noise) and temporal autocorrelation in that process noise. To measure the frequency of incorrectly detecting a decline (false-positive or false alarm) and failing to detect a true decline (false-negative), we simulated stable and declining abundance time series across several magnitudes of observation error and autocorrelated process noise. We then empirically estimated the magnitude of observation error and autocorrelated process noise across a broad range of taxa and mapped these estimates onto the simulated parameter space. Based on the taxa we examined, at low classification thresholds (30% decline in abundance) and short observation windows (10 years), false alarms would be expected to occur, on average, about 40% of the time assuming density-independent dynamics, whereas false-negatives would be expected to occur about 60% of the time. However, false alarms and failures to detect true declines were reduced at higher classification thresholds (50% or 80% declines), longer observation windows (20, 40, 60 years), and assuming density-dependent dynamics. The lowest false-positive and false-negative rates are likely to occur for large-bodied, long-lived animal species.

Lessons from sea louse and salmon epidemiology

Effective disease management can benefit from mathematical models that identify drivers of epidemiological change and guide decision-making. This is well illustrated in the host–parasite system of sea lice and salmon, which has been modelled extensively due to the economic costs associated with sea louse infections on salmon farms and the conservation concerns associated with sea louse infections on wild salmon. Consequently, a rich modelling literature devoted to sea louse and salmon epidemiology has been developed. We provide a synthesis of the mathematical and statistical models that have been used to study the epidemiology of sea lice and salmon. These studies span both conceptual and tactical models to quantify the effects of infections on host populations and communities, describe and predict patterns of transmission and dispersal, and guide evidence-based management of wild and farmed salmon. As aquaculture production continues to increase, advances made in modelling sea louse and salmon epidemiology should inform the sustainable management of marine resources.

Can reduced predation offset negative effects of sea louse parasites on chum salmon

The impact of parasites on hosts is invariably negative when considered in isolation, but may be complex and unexpected in nature. For example, if parasites make hosts less desirable to predators then gains from reduced predation may offset direct costs of being parasitized. We explore these ideas in the context of sea louse infestations on salmon. In Pacific Canada, sea lice can spread from farmed salmon to migrating juvenile wild salmon. Low numbers of sea lice can cause mortality of juvenile pink and chum salmon. For pink salmon, this has resulted in reduced productivity of river populations exposed to salmon farming. However, for chum salmon, we did not find an effect of sea louse infestations on productivity, despite high statistical power. Motivated by this unexpected result, we used a mathematical model to show how a parasite-induced shift in predation pressure from chum salmon to pink salmon could offset negative direct impacts of sea lice on chum salmon. This shift in predation is proposed to occur because predators show an innate preference for pink salmon prey. This preference may be more easily expressed when sea lice compromise juvenile salmon hosts, making them easier to catch. Our results indicate how the ecological context of host–parasite interactions may dampen, or even reverse, the expected impact of parasites on host populations.

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.

Durability of environment-recruitment relationships in aquatic ecosystems: insights from long-term monitoring in a highly modified estuary and implications for management

The environment can strongly influence the survival of aquatic organisms and their resulting dynamics. Our understanding of these relationships, typically based on correlations, underpins many contemporary resource management decisions and conservation actions. However, such relationships can break down over time as ecosystems evolve. Even when durable, they may not be very useful for management if they exhibit high variability, context dependency, or non-stationarity. Here, we systematically review the literature to identify trends across environment-recruitment relationships for aquatic taxa from California’s San Francisco Bay and Sacramento-San Joaquin Delta Estuary. This is one of the most heavily modified aquatic ecosystems in North America, and home to numerous species of concern whose relationships with the environment inform regulatory actions and constraints. We retested 23 of these relationships spanning 9 species using data that have accumulated in the years since they were first published (9-40 additional years) to determine whether they persisted. Most relationships were robust (i.e., same or stronger in magnitude) to the addition of new data, but the ability to predict how a species will respond to environmental change did not generally improve with more data. Instead, prediction error generally increased over time and in some cases very quickly, suggesting a rapid regime shift. Our results suggest that more data alone will not necessarily improve the ability of these relationships to inform decision making. We conclude by synthesizing emerging insights from the literature on best practices for the analysis, use, and refinement of environment-recruitment relationships to inform decision making in dynamic ecosystems.

Collapse, Tipping Points, and Spatial Demographic Structure Arising from the Adopted Migrant Life History

The roles of dispersal and recruitment have long been a focal point in ecology and conservation. The adopted migrant hypothesis proposes a life history in which social learning transmits migratory knowledge between generations of iteroparous fish. Specifically, juveniles disperse from the parental spawning site, encounter and recruit to a local adult population, and learn migration routes between spawning and foraging habitats by following older, experienced fish. Although the adopted migrant life history may apply to many species of pelagic marine fishes, there is scant theoretical or empirical work on the consequent population dynamics. We developed and analyzed a mathematical model of this life history in which the recruitment of juveniles depends on the relative abundance of the local populations and recruitment overlap, which measures the ease with which juveniles are recruited by a nonparental population. We demonstrate that the adopted migrant life history can maintain spatial demographic structure among local populations, that it can also predispose local populations to collapse when a tipping point is crossed, and that recovery after collapse is impaired by reduced recruitment at small local population sizes.

Correction to: Can reduced predation offset negative effects of sea louse parasites on chum salmon?

[ Proc. R. Soc. B 281 , 20132913. (7 February 2014; Published online 18 December 2013) ([doi:10.1098/rspb.2013.2913][2])][2] In a study of sea louse parasites on chum salmon [[1][2]], we presented a host–parasite model that incorporates the effect of parasite-mediated predation on host