School of BioSciences - Research Publications
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ItemIdentifying the most effective behavioural assays and predator cues for quantifying anti-predator responses in mammals: a systematic review protocol(BMC, 2021-12-18)Abstract Background Mammals, globally, are facing population declines. Strategies increasingly employed to recover threatened mammal populations include protecting populations inside predator-free havens, and translocating animals from one site to another, or from a captive breeding program. These approaches can expose predator-naïve animals to predators they have never encountered and as a result, many conservation projects have failed due to the predation of individuals that lacked appropriate anti-predator responses. Hence robust ways to measure anti-predator responses are urgently needed to help identify naïve populations at risk, to select appropriate animals for translocation, and to monitor managed populations for trait change. Here, we outline a protocol for a systematic review that collates existing behavioural assays developed for the purpose of quantifying anti-predator responses, and identifies assay types and predator cues that provoke the greatest behavioural responses. Methods We will retrieve articles from academic bibliographic databases and grey literature sources (such as government and conservation management reports), using a Boolean search string. Each article will be screened for the satisfaction of eligibility criteria determined using the PICO (Population—Intervention—Comparator—Outcome) framework, to yield the final article pool. Using metadata extracted from each article, we will map all known behavioural assays for quantifying anti-predator responses in mammals and will then examine the context in which each assay has been implemented (e.g. species tested, predator cue characteristics). Finally, with mixed effects modelling, we will determine which of these assays and predator cue types elicit the greatest behavioural responses (standardised difference in response between treatment and control groups). The final review will highlight the most robust methodology, will reveal promising techniques on which to focus future assay development, and will collate relevant information for conservation managers.
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ItemEffects of learning and adaptation on population viability(WILEY, 2021-08)Cultural adaptation is one means by which conservationists may help populations adapt to threats. A learned behavior may protect an individual from a threat, and the behavior can be transmitted horizontally (within generations) and vertically (between generations), rapidly conferring population-level protection. Although possible in theory, it remains unclear whether such manipulations work in a conservation setting; what conditions are required for them to work; and how they might affect the evolutionary process. We examined models in which a population can adapt through both genetic and cultural mechanisms. Our work was motivated by the invasion of highly toxic cane toads (Rhinella marina) across northern Australia and the resultant declines of endangered northern quolls (Dasyurus hallucatus), which attack and are fatally poisoned by the toxic toads. We examined whether a novel management strategy in which wild quolls are trained to avoid toads can reduce extinction probability. We used a simulation model tailored to quoll life history. Within simulations, individuals were trained and a continuous evolving trait determined innate tendency to attack toads. We applied this model in a population viability setting. The strategy reduced extinction probability only when heritability of innate aversion was low (<20%) and when trained mothers trained >70% of their young to avoid toads. When these conditions were met, genetic adaptation was slower, but rapid cultural adaptation kept the population extant while genetic adaptation was completed. To gain insight into the evolutionary dynamics (in which we saw a transitory peak in cultural adaptation over time), we also developed a simple analytical model of evolutionary dynamics. This model showed that the strength of natural selection declined as the cultural transmission rate increased and that adaptation proceeded only when the rate of cultural transmission was below a critical value determined by the relative levels of protection conferred by genetic versus cultural mechanisms. Together, our models showed that cultural adaptation can play a powerful role in preventing extinction, but that rates of cultural transmission need to be high for this to occur.
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ItemThe push and pull between theory and data in understanding the dynamics of invasion(Peer Community In, 2020-12-15)
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ItemFarmed salmonids drive the abundance, ecology and evolution of parasitic salmon lice in Norway(INTER-RESEARCH, 2021)Sea cage fish farming is typically open to the environment, with disease transmission possible between farmed and wild hosts. In salmonid aquaculture, salmon louse Lepeophtheirus salmonis infestations cause production losses, reduce welfare for farmed fish and increase infestation rates for wild fish populations. The high density of hosts in farms likely also shifts the coevolutionary arms race between host and parasite, with ecological and evolutionary consequences for the salmon louse. Using farm-reported salmon and louse abundances and publicly reported estimates of wild salmonid host abundances and the salmon lice they carry, we estimated (1) the relative abundance of farmed and wild salmonid hosts and (2) the relative importance of each for the abundance of salmon lice for the coastal zone of Norway from 1998 to 2017. Farmed hosts increased in importance over time with the expansion of the industry. From 2013 to 2017, farmed salmonids outnumbered wild salmonids by 267-281:1. By 2017, farmed salmonids accounted for 99.6% of available hosts and produced 99.1% of adult female salmon lice and 97.6% of mated (ovigerous) adult female salmon lice in Norwegian coastal waters. The persistent dominance of farmed hosts has clear implications: (1) management decisions that aim to limit lice abundance can be guided by lice data from farms alone, as lice on wild salmonids make a trivial contribution to the national lice population; and (2) strategies to prevent or treat lice infestations are vulnerable to the evolution of resistance, as the pool of wild hosts is inconsequential and will not act as a refuge large enough to stem the evolution of resistance. As the Norwegian salmon industry expands and salmon lice infestations continue, farmed salmon will drive the ecology and evolution of salmon lice.
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ItemParasite management in aquaculture exerts selection on salmon louse behaviour(WILEY, 2021-08)The evolution of pest resistance to management strategies is a major challenge for farmed systems. Mitigating the effects of pest adaptation requires identifying the selective pressures imposed by these strategies. In Atlantic salmon (Salmo salar) aquaculture, barriers are used to prevent salmon louse (Lepeophtheirus salmonis) larvae (copepodids) from entering salmon cages. These barriers are effective against shallow-swimming copepodids, but those swimming deeper can pass underneath and infest salmon. Laboratory experiments suggest that depth regulation in copepodids is a variable behavioural trait with a genetic basis. We used biological-hydrodynamic dispersal models to assess how this trait variation alters the dispersion of lice through the ocean environment and into farms. The dispersal of copepodids with 3 behavioural phenotypes (deep, mean or shallow) was modelled over winter-spring and spring-summer periods in a Norwegian fjord system with intensive aquaculture. The infestation pressure of each phenotype on barrier cages was estimated from their modelled depth distributions: copepodids deeper than 10 m were predicted to successfully pass underneath barriers. The deep phenotype was the most abundant below 10 m and reached infestation pressures 3 times higher than that of the mean phenotype. In contrast, the shallow phenotype infestation pressure reached less than half that of the mean phenotype. These differences in relative fitness indicate that barriers can impose strong directional selection on the swimming behaviour of copepodids. The strength of this selection varied seasonally and geographically, with selection for the deep phenotype stronger in winter-spring and at coastal locations than in spring-summer and within fjords. These findings can be applied across farms to slow louse adaptation, by limiting barriers during situations of strong selection, although this must be balanced against trade-offs to short-term efficacy. More broadly, our study highlights new ways in which dispersal models can address evolutionary questions crucial for sustainable parasite management in aquaculture.
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ItemEnergetic scaling across different host densities and its consequences for pathogen proliferation(WILEY, 2021-02)The spread of infectious disease is determined by the ability of a pathogen to proliferate within and spread between susceptible hosts. Processes that limit the performance of a pathogen thus occur at two scales: varying with both the availability of energy within a host, and the number of susceptible hosts in a patch. When the rate at which a host intakes and expends energy is density‐dependent, these two processes are intimately linked. By modifying how hosts compete for and expend resources, a shift in population density may contribute to differences in the flow of energy in a host–pathogen system, both in terms of the energy available for a host to grow, reproduce and fight infection, as well as the energy available for a pathogen to exploit. Energy flux, therefore, connects the two contrasting scales of within‐ and between‐host dynamics by directly linking the proliferation of a pathogen to the number of hosts circulating within a patch. We use the host Daphnia magna to explore the relationship between energy intake and expenditure at various population densities, as estimated by feeding and metabolic rates respectively. By infecting hosts with the bacterial pathogen Pasteuria ramosa, we then explore how infection changes the relative balance of energy intake and expenditure, and how this energy scope translates into production of transmission spores. Our work demonstrates that energy intake declines at a faster rate with density than does metabolic rate, leaving more excess energy (i.e. discretionary energy) available for both hosts and their dependent pathogens at low population densities. This energetic advantage translates positively into host and pathogen growth, with the production of mature transmission spores benefiting most from correlated changes in host body size, as well as a direct connection between energy scope and spore loads. Our findings reinforce how patch quality for a pathogen operates at two contrasting scales, with the within‐host proliferation of a pathogen being optimised in energy rich, low density host populations and opportunities for between‐host transmission likely maximised in dense populations. A free Plain Language Summary can be found within the Supporting Information of this article.
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ItemNo behavioral syndromes or sex-specific personality differences in the southern rainforest sunskink (Lampropholis similis)(WILEY, 2021-02)Behavioral syndromes, when individuals within a population express consistent behavioral differences across time and context, are widespread in animal taxa. For many species, males and females experience different selective pressures after maturation, resulting in the divergence of life‐history and behavioral traits. However, the potential for sex‐specific differences in individual behaviors and behavioral syndromes has rarely been assessed. Here, we tested for sex‐specific differences in behavior (activity, exploration, sociability) and personality in the southern rainforest sunskink, Lampropholis similis. We found that most behaviors in L. similis did not differ between sexes, the exception being sociality which was higher in females than males. In terms of consistency among behaviors, activity and exploration, but not sociability, were repeatable, and there were no sex‐specific differences in repeatability of behavioral traits. Although a behavioral syndrome among these three traits is present in a congener (L. delicata), we found no evidence for such a syndrome in either sex of L. similis. Our study is consistent with the results of studies on other Lampropholis skinks that have found only limited sexual differences in behavior. More broadly, our study demonstrates there can be considerable differences in the presence or absence of behavioral syndromes in closely related species.
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ItemUsing Biophysical Models to Improve Survey Efficiency for Cryptic Ectotherms(WILEY, 2020-06-13)