Development of novel microsatellite markers for the invasive Northern Pacific seastar, Asterias amurensis

The Northern Pacific seastar, Asterias amurensis, is a benthic marine predator, which has recently established several invasive populations in Australian waters. To investigate population structure, diversity and patterns of connectivity, we isolated and characterised 27 microsatellite loci and tested their polymorphism based on 46 individuals from two invasive populations. The mean allelic richness was 4.33; observed heterozygosity was 0.42, while the percentage of polymorphic loci was 92.6%. The polymorphic markers will prove useful in the assessment of population genetic parameters, in both invasive and native A. amurensis populations.

Ecosystem restoration with teeth : what role for predators?

Recent advances highlight the potential for predators to restore ecosystems and confer resilience against globally threatening processes, including climate change and biological invasions. However, releasing the ecological benefits of predators entails significant challenges. Here, we discuss the economic, environmental and social considerations affecting predator-driven ecological restoration programmes, and suggest approaches for reducing the undesirable impacts of predators. Because the roles of predators are context dependent, we argue for increased emphasis on predator functionality in ecosystems and less on the identities and origins of species and genotypes. We emphasise that insufficient attention is currently given to the importance of variation in the social structures and behaviours of predators in influencing the dynamics of trophic interactions. Lastly, we outline experiments specifically designed to clarify the ecological roles of predators and their potential utility in ecosystem restoration.

Introgression of domesticated alleles into a wild trout genotype and the impact on seasonal survival in natural lakes

We tested the fitness consequences of introgression of fast-growing domesticated fish into a wild population. Fry from wild and domesticated rainbow trout (Oncorhynchus mykiss) crosses, F1 hybrids, and first- and second-generation backcrosses were released into two natural lakes. Parentage analysis using microsatellite loci facilitated the identification of survivors, so fitness was estimated in nature from the first-feeding stage. Results indicated that under certain conditions, domesticated fish survived at least as well as wild fish within the same environment. Relative growth and survival of the crosses, however, were highly dependent on environment. During the first summer, fastest-growing crosses had the highest survival, but this trend was reversed after one winter and another summer. Although the F1 hybrids showed evidence of outbreeding depression because of the disruption of local adaptation, there was little evidence of outbreeding depression in the backcrosses, and the second-generation backcrosses exhibited a wild-type phenotype. This information is relevant for assessing the multigenerational risk of escaped or released domesticated fish should they successfully interbreed with wild populations and provides information on how to minimize detrimental impacts of a conservation breeding and/or management programme. These data also further understanding of the selection pressures in nature that maintain submaximal rates of growth.

How the ladybird got its spots : effects of resource limitation on the honesty of aposematic signals

Prey species often possess defences (e.g. toxins) coupled with warning signals (i.e. aposematism). There is growing evidence that the expression of aposematic signals often varies within species and correlates with the strength of chemical defences. This has led to the speculation that such signals may be 'honest', with signal reliability ensured by the costliness of producing or maintaining aposematic traits. We reared larval seven-spot ladybirds (Coccinella septempunctata) on a Low or High aphid diet and measured the effects on warning signal expression (elytral carotenoid pigmentation, conspicuousness, spot size), levels of defensive alkaloids (precoccinelline, coccinelline), and relationships between these traits. High-diet individuals had greater total precoccinelline levels, and elytra carotenoid concentrations at adulthood which was detectable to a typical avian predator. However, larval diet did not significantly affect adult body mass or size, spot size or coccinelline levels. Elytra carotenoid concentrations correlated positively with total precoccinelline levels in both diet groups and sexes. However, the relationship between elytra carotenoid concentrations and total levels of coccinelline depended on sex: in both diet groups, elytra carotenoids and coccinelline levels were positively correlated in females, but negatively correlated in males. Spot size and coccinelline levels correlated positively in Low-diet individuals, but negatively in High-diet individuals. These results point to physiological linkages between components of aposematism, which are modulated by resource (i.e. food) availability and affect the honesty of signals. Developmental diet, but also sex, influenced the relationships between signals and toxin levels. Ladybirds are sexually size dimorphic, and thus in comparison with males, females may be more susceptible to resource limitation and more likely to be honest signallers. © 2012 The Authors. Functional Ecology © 2012 British Ecological Society.

Responses of Australian wading birds to a novel toxic prey type, the invasive cane toad Rhinella marina

The impact of invasive predators on native prey has attracted considerable scientific attention, whereas the reverse situation (invasive species being eaten by native predators) has been less frequently studied. Such interactions might affect invasion success; an invader that is readily consumed by native species may be less likely to flourish in its new range than one that is ignored by those taxa. Invasive cane toads (Rhinella marina) in Australia have fatally poisoned many native predators (e.g., marsupials, crocodiles, lizards) that attempt to ingest the toxic anurans, but birds are more resistant to toad toxins. We quantified prey preferences of four species of wading birds (Nankeen night heron, purple swamphen, pied heron, little egret) in the wild, by offering cane toads and alternative native prey items (total of 279 trays offered, 14 different combinations of prey types). All bird species tested preferred the native prey, avoiding both tadpole and metamorph cane toads. Avoidance of toads was strong enough to reduce foraging on native prey presented in combination with the toads, suggesting that the presence of cane toads could affect predator foraging tactics, and reduce the intensity of predation on native prey species found in association with toads.

Asymmetric impact of piscivorous birds on size-structured fish populations

Fish are frequently considered the top predator in freshwater food web models despite evidence that predatory birds can impact fish populations. In this study, we quantified bird predation rates on experimental populations of rainbow trout (Oncorhynchus mykiss (Walbaum, 1792)) created by stocking nine small lakes in British Columbia, Canada. Combining estimates of fish mortality with estimated bird predation rates allowed us to partition fish mortality into that due to birds versus cannibalism. Our results indicated that bird predators had significant impacts on age-1 trout populations, but little impact on age-0 trout. Common loons (Gavia immer Brunnich, 1764) were the principle predator among eight predatory bird species present, apparently consuming nearly 50% of all stocked age-1 trout and explaining almost 50% of variation in mortality rates. Age-1 trout mortality did not differ significantly from zero in lakes without loons. Birds consumed a small proportion of age-0 trout, and estimated consumption explained none of the variation in age-0 trout mortality among lakes. We conclude that birds affect fish populations by asymmetric predation on different age (size) classes and can be important top predators that should not be ignored when characterizing freshwater food webs in lakes.

Performance of tropical fish recruiting to temperate habitats: role of ambient temperature and implications of climate change

The warming of coastal oceans due to climate change is increasing the overwinter survival of tropical fishes transported to temperate latitudes by ocean currents. However, the processes governing early post-arrival mortality are complex and can result in minimum threshold temperatures for overwinter survival, which are greater than those predicted based upon physiological temperature tolerances alone. This 3.5 mo laboratory study monitored the early performance of a tropical damselfish Abudefduf vaigiensis that occurs commonly during austral summer along the SE Australian coast, under nominal summer and winter water temperatures, and compares results with a co-occurring year-round resident of the same family, Parma microlepis. Survivorship, feeding rate, growth and burst swimming ability (as a measure of predator escape ability) were all reduced for the tropical species at winter water temperatures compared to those in summer, whereas the temperate species experienced no mortality and only feeding rate was reduced at colder temperatures. These results suggest that observed minimum threshold survival temperatures may be greater than predicted by physiology alone, due to lowered food intake combined with increased predation risk (a longer time at vulnerable sizes and reduced escape ability). Overwinter survival is a significant hurdle in pole-ward range expansions of tropical fishes, and a better understanding of its complex processes will allow for more accurate predictions of changes in biodiversity as coastal ocean temperatures continue to increase due to climate change.

Ratio-dependent response of a temperate Australian estuarine system to sustained nitrogen loading

Classical resource- and the less studied ratio-dependent models of predator–prey relationships provide divergent predictions as to the sustained ecological effects of bottom-up forcing. While resource-dependent models, which consider only instantaneous prey density in modelling predator responses, predict community responses that are dependent on the number of trophic levels in a system, ratio-dependent models, which consider the number of prey per consumer, predict proportional increase in each level irrespective of chain length. The two models are only subtly different for systems with two or three trophic levels but in the case of four trophic levels, predict opposite effects of enrichment on primary producers. Despite the poor discriminatory power of tests of the models in systems with two or three trophic levels, field tests in estuarine and marine systems with four trophic levels have been notably absent. Sampling of phytoplankton, macroinvertebrates, invertebrate-feeding fishes, piscivorous fishes in Kooloonbung Creek, Hastings River estuary, eastern Australia, subject to over 20 years of sewage discharge, revealed increased abundances in all four trophic levels at the disturbed location relative to control sites. Increased abundance of phytoplankton at the disturbed site was counter to the predictions of resource-dependent models, which posit a reduction in the first trophic level in response to enrichment. By contrast, the increase in abundance of this first trophic level and the proportionality of increases in abundances of each of the four trophic groups to nitrogen loading provided strong support for ratio dependency. This first evidence of ratio dependence in an estuarine system with four trophic levels not only demonstrates the applicability of ecological theory which seeks to simplify the complexity of systems, but has implications for management. Although large nutrient inputs frequently induce mortality of invertebrates and fish, we have shown that smaller inputs may in fact enhance biomass of all trophic levels.

Trophic cul-de-sac, Pyrazus ebeninus, limits trophic transfer through an estuarine detritus-based food web

The importance to food-webs of trophic cul-de-sacs, species that channel energy flow away from higher trophic levels, is seldom considered outside of the pelagic systems in which they were first identified. On intertidal mudflats, inputs of detritus from saltmarshes, macroalgae or microphytobenthos are generally regarded as a major structuring force underpinning food-webs and there has been no consideration of trophic cul-de-sacs to date. A fully orthogonal three-factor experiment manipulating the density of the abundant gastropod, Pyrazus ebeninus, detritus and macrobenthic predators on a Sydney mudflat revealed large deleterious effects of the gastropod, irrespective of detrital loading or the presence of predators. Two months after experimental manipulation, the standing-stock of microphytobenthos in plots with high (44 per m²) densities of P. ebeninus was 20% less than in plots with low (4 per m²) densities. Increasing densities of P. ebeninus from low to high halved the abundance of macroinvertebrates and the average number of species. In contrast, the addition of detritus had differing effects on microphytobenthos (positively affected) and macroinvertebrates (negatively affected). Over the two-months of our experiment, no predatory mortality of P. ebeninus was observed and high densities of P. ebeninus decreased impacts of predators on macroinvertebrate abundances. Given that the dynamics of southeast Australian mudflats are driven more by disturbance than seasonality in predators and their interactions with prey, it is likely that Pyrazus would be similarly resistant to predation and have negative effects on benthic assemblages at other times of the year, outside of our study period. Thus, in reducing microphytobenthos and the abundance and species richness of macrofauna, high abundances of the detritivore P. ebeninus may severely limit the flow of energy up the food chain to commercially-important species. This study therefore suggests that trophic cul-de-sacs are not limited to the eutrophied pelagic systems in which they were first identified, but may exist in other systems as well.

Mechanisms for climate-induced mortality of fish populations in whole-lake experiments

The effects of climate change on plant and animal populations are widespread and documented for many species in many areas of the world. However, projections of climate impacts will require a better mechanistic understanding of ecological and behavioral responses to climate change and climate variation. For vertebrate animals, there is an absence of whole-system manipulative experiments that express natural variation in predator and prey behaviors. Here we investigate the effect of elevated water temperature on the physiology, behavior, growth, and survival of fish populations in a multiple whole-lake experiment, by using 17 lake-years of data collected over 2 years with differing average temperatures. We found that elevated temperatures in excess of the optimum reduced the scope for growth through reduced maximum consumption and increased metabolism in young rainbow trout, Oncorhynchus mykiss. Increased metabolism at high temperatures resulted in increased feeding activity (consumption) by individuals to compensate and maintain growth rates similar to that observed at cooler (optimum) temperatures. However, greater feeding activity rates resulted in greater vulnerability to predators that reduced survival to only half that of the cooler year. Our work therefore identifies temperature-dependent physiology and compensatory feeding behavior as proximate mechanisms for substantial climate-induced mortality in fish populations at the scale of entire populations and waterbodies.

Assessing effects of diel period, gear selectivity and predation on patterns of microhabitat use by fish in a mangrove dominated system in SE Australia

The relative value of temperate mangroves to fish, and the processes driving patterns of microhabitat use within this habitat, are unknown. There are 3 quickly identifiable microhabitats within temperate Australian mangroves: (1) forest (the area of mangroves with trees); (2) pneumatophores (the area directly seaward of the forest without trees but with pneumatophores [aerial roots]); and (3) channel (the area directly seaward of the pneumatophores without gross structural attributes such as trees or pneumatophores). Duplicate fyke and gill nets were both initially used to sample fish in the 3 microhabitats described above. Sampling took place across the seaward edge of mangroves on 10 sampling occasions (5 night and 5 day), in a large estuarine system in SE Australia. Fish assemblages (693 fish from 20 species and 15 families) varied significantly (p < 0.05) between the forest and the channel, and between diel periods for each gear (net type), but there was little difference in the assemblage structure of fish between forest–pneumatophore or pneumatophore–channel microhabitats. Juvenile lifestages (61% of all fish) and commercially important taxa (76%) were common. Abundance, biomass and species richness of fish were generally lower in the forest than the other microhabitats, but this pattern varied significantly (p < 0.05) between diel periods, among sampling occasions, and with water depth. Highly quantitative pop nets provided a preliminary assessment of whether differential gear selectivity caused patterns between microhabitats, but less rich fish assemblages were again recorded in forests than in pneumatophores. The importance of predation in structuring fish assemblages across microhabitats was assessed by measuring survival of juvenile fish tethered in 3 predation treatments (predator exclusion, cage control, and uncaged). Survival rates were high across the predator treatments and did not vary among microhabitats. The variation in fish assemblages across microhabitats within mangroves was not consistent with a model of mangrove structure providing a refuge for juvenile fish from predation, but instead could indicate differences in efficiency of gear types among microhabitats and/or other ‘edge effect’-driven processes such as the provision of food and/or shelter.

Changes in muscle composition during the development of diving ability in the Australian fur seal

During development the Australian fur seal transitions from a terrestrial, maternally dependent pup to an adult marine predator. Adult seals have adaptations that allow them to voluntarily dive at depth for long periods, including increased bradycardic control, increased myoglobin levels and haematocrit. To establish whether the profile of skeletal muscle also changes in line with the development of diving ability, biopsy samples were collected from the trapezius muscle of pups, juveniles and adults. The proportions of different fibre types and their oxidative capacity were determined. Only oxidative fibre types (Type I and IIa) were identified, with a significant change in proportions from pup to adult. There was no change in oxidative capacity of Type I and IIa fibres between pups and juveniles but there was a two-fold increase between juveniles and adults. Myoglobin expression increased between pups and juveniles, suggesting improved oxygen delivery, but with no increase in oxidative capacity, oxygen utilisation within the muscle may still be limited. Adult muscle had the highest oxidative capacity, suggesting that fibres are able to effectively utilise available oxygen during prolonged dives. Elevated levels of total creatine in the muscles of juveniles may act as an energy buffer when fibres are transitioning from a fast to slow fibre type.