Rachel A. Paterson

Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach

Invasion ecology urgently requires predictive methodologies that can forecast the ecological impacts of existing, emerging and potential invasive species. We argue that many ecologically damaging invaders are characterised by their more efficient use of resources. Consequently, comparison of the classical ‘functional response’ (relationship between resource use and availability) between invasive and trophically analogous native species may allow prediction of invader ecological impact. We review the utility of species trait comparisons and the history and context of the use of functional responses in invasion ecology, then present our framework for the use of comparative functional responses. We show that functional response analyses, by describing the resource use of species over a range of resource availabilities, avoids many pitfalls of ‘snapshot’ assessments of resource use. Our framework demonstrates how comparisons of invader and native functional responses, within and between Type II and III functional responses, allow testing of the likely population-level outcomes of invasions for affected species. Furthermore, we describe how recent studies support the predictive capacity of this method; for example, the invasive ‘bloody red shrimp’ Hemimysis anomala shows higher Type II functional responses than native mysids and this corroborates, and could have predicted, actual invader impacts in the field. The comparative functional response method can also be used to examine differences in the impact of two or more invaders, two or more populations of the same invader, and the abiotic (e.g. temperature) and biotic (e.g. parasitism) context-dependencies of invader impacts. Our framework may also address the previous lack of rigour in testing major hypotheses in invasion ecology, such as the ‘enemy release’ and ‘biotic resistance’ hypotheses, as our approach explicitly considers demographic consequences for impacted resources, such as native and invasive prey species. We also identify potential challenges in the application of comparative functional responses in invasion ecology. These include incorporation of numerical responses, multiple predator effects and trait-mediated indirect interactions, replacement versus non-replacement study designs and the inclusion of functional responses in risk assessment frameworks. In future, the generation of sufficient case studies for a meta-analysis could test the overall hypothesis that comparative functional responses can indeed predict invasive species impacts.

Length‐mass models for some common New Zealand littoral‐benthic macroinvertebrates, with a note on within‐taxon variability in parameter values among published models

Abstract Regression models are developed and presented to predict dry mass (mg) from two linear dimensions (mm) for 17 benthic macroinvertebrate taxa common to littoral zones of New Zealand lakes. We also provide regression models to predict body length from head capsule width for the major insect taxa. Dry mass was best explained as a power function of all linear dimensions: M = aL b .Parameters are presented in the log10‐transformed linear form of this power function. Body length was a simple linear function of head capsule width for all insect taxa, hence parameters for these models are presented as untransformed values. We also provide family level models for the Chironomidae, and compare our chironomid body length‐mass model with other published Chrionomidae length‐mass models. There was a very high degree of variability in parameter values among published length‐mass models for the family Chironomidae (mean coefficient of variation for mass at length = 148%). We discuss the potential causes and implications of this variability.

Predicting invasive species impacts: a community module functional response approach reveals context dependencies

Summary Predatory functional responses play integral roles in predator–prey dynamics, and their assessment promises greater understanding and prediction of the predatory impacts of invasive species. Other interspecific interactions, however, such as parasitism and higher-order predation, have the potential to modify predator–prey interactions and thus the predictive capability of the comparative functional response approach. We used a four-species community module (higher-order predator; focal native or invasive predators; parasites of focal predators; native prey) to compare the predatory functional responses of native Gammarus duebeni celticus and invasive Gammarus pulex amphipods towards three invertebrate prey species (Asellus aquaticus, Simulium spp., Baetis rhodani), thus, quantifying the context dependencies of parasitism and a higher-order fish predator on these functional responses. Our functional response experiments demonstrated that the invasive amphipod had a higher predatory impact (lower handling time) on two of three prey species, which reflects patterns of impact observed in the field. The community module also revealed that parasitism had context-dependent influences, for one prey species, with the potential to further reduce the predatory impact of the invasive amphipod or increase the predatory impact of the native amphipod in the presence of a higher-order fish predator. Partial consumption of prey was similar for both predators and occurred increasingly in the order A. aquaticus, Simulium spp. and B. rhodani. This was associated with increasing prey densities, but showed no context dependencies with parasitism or higher-order fish predator. This study supports the applicability of comparative functional responses as a tool to predict and assess invasive species impacts incorporating multiple context dependencies.

Predator cue studies reveal strong trait-mediated effects in communities despite variation in experimental designs ☆

Nonconsumptive or trait-mediated effects of predators on their prey often outweigh density-mediated interactions where predators consume prey. For instance, predator presence can alter prey behaviour, physiology, morphology and/or development. Despite a burgeoning literature, our ability to identify general patterns in prey behavioural responses may be influenced by the inconsistent methodologies of predator cue experiments used to assess trait-mediated effects. We therefore conducted a meta-analysis to highlight variables (e.g. water type, predator husbandry, exposure time) that may influence invertebrate prey’s behavioural responses to fish predator cues. This revealed that changes in prey activity and refuge use were remarkably consistent overall, despite wide differences in experimental methodologies. Our meta-analysis shows that invertebrates altered their behaviour to predator cues of both fish that were fed the focal invertebrate and those that were fed other prey types, which suggests that invertebrates were not responding to specific diet information in the fish cues. Invertebrates also altered their behaviour regardless of predator cue addition regimes and fish satiation levels. Cue intensity and exposure time did not have significant effects on invertebrate behaviour. We also highlight that potentially confounding factors, such as parasitism, were rarely recorded in sufficient detail to assess the

frair: an R package for fitting and comparing consumer functional responses

Summary Consumer-resource interactions (i.e. the functional response) underpin decades of ecological advancements. However, selecting, fitting and comparing functional response models using appropriate methods remains a non-trivial endeavour. The R package frair provides tools for selecting and differentiating various forms of consumer functional response models, a consistent interface for fitting and visualising response curves, and a selection of statistically robust methods for comparing fitted parameters. Using real data from crustacean predator-prey systems, we demonstrate the utility of frair, highlighting best practice and common analytical mistakes.

Do different parasite species interact in their effects on host fitness? A case study on parasites of the amphipod Paracalliope fluviatilis

There is a gap in our understanding of the relative and interactive effects of different parasite species on the same host population. Here we examine the effects of the acanthocephalan Acanthocephalus galaxii, an unidentified cyclophyllidean cestode, and the trematodes Coitocaecum parvum and Microphallus sp. on several fitness components of the amphipod Paracalliope fluviatilis, using a combination of infection surveys and both survival and behavioural trials. In addition to significant relationships between specific parasites and measures of amphipod survival, maturity, mating success and behaviour, interactions between parasite species with respect to amphipod photophilia were also significant. While infection by either A. galaxii or C. parvum was associated with increased photophilia, such increases were negated by co-infection with Microphallus sp. We hypothesize that this is due to the more subtle manipulative effect of A. galaxii and C. parvum being impaired by Microphallus sp. We conclude that the low frequency at which such double infections occur in our sampled population means that such interactions are unlikely to be important beyond the scale of the host individual. Whether or not this is generally true, implying that parasitological models and theory based on single parasite species studies do generally hold, requires cross-species meta-analytical studies.

Native fish avoid parasite spillback from multiple exotic hosts: consequences of host density and parasite competency

Disease-mediated impacts of exotic species on their native counterparts are often ignored when parasite-free individuals are translocated. However, native parasites are frequently acquired by exotic species, thus providing a mechanism through which native host-parasite dynamics may be altered. In Argentina, multiple exotic salmonids are host to the native fish acanthocephalan parasite Acanthocephalus tumescens. Field evidence suggests that rainbow trout, Oncorhynchus mykiss, may be a major contributor to the native parasite’s population. We used a combination of experimental infections (cystacanth—juvenile worm transmission from amphipod to fish; post-cyclic—adult worm transmission between definitive fish hosts) and dynamic population modelling to determine the extent to which exotic salmonid hosts may alter A. tumescens infections in native freshwater fish. Experimental cystacanth infections demonstrated that although A. tumescens establishes equally well in native and exotic hosts, parasite growth and maturity is superior in exotic O. mykiss. Experimental post-cyclic infections also showed greater establishment success of A. tumescens in O. mykiss, though post-cyclic transmission did not result in greater parasite size or maturity. Dynamic population modelling, however, suggested that exotic salmonids may have a very limited influence on the A. tumescens population overall, due to the majority of A. tumescens individuals being maintained by more abundant native hosts. This research highlights the importance of considering both a host’s relative density and its competency for parasites when evaluating whether exotic species can modify native host-parasite dynamics.

Relative competence of native and exotic fish hosts for two generalist native trematodes

Exotic fish species frequently acquire native parasites despite the absence of closely related native hosts. They thus have the potential to affect native counterparts by altering native host-parasite dynamics. In New Zealand, exotic brown trout Salmo trutta and rainbow trout Oncorhynchus mykiss have acquired two native trematodes (Telogaster opisthorchis and Stegodexamene anguillae) from their native definitive host (the longfin eel Anguilla dieffenbachii). We used a combination of field surveys and experimental infections to determine the relative competence of native and exotic fish hosts for these native parasites. Field observations indicated that the longfin eel was the superior host for both parasites, although differences between native and exotic hosts were less apparent for S. anguillae. Experimental infections indicated that both parasites had poorer establishment and survival in salmonids, although some worms matured and attained similar sizes to those in eels before dying. Overall, the field surveys and experimental infections indicate that these exotic salmonids are poor hosts of both native trematodes and their presence may decrease native parasite flow to native hosts.

Eaten alive: cannibalism is enhanced by parasites

Cannibalism is ubiquitous in nature and especially pervasive in consumers with stage-specific resource utilization in resource-limited environments. Cannibalism is thus influential in the structure and functioning of biological communities. Parasites are also pervasive in nature and, we hypothesize, might affect cannibalism since infection can alter host foraging behaviour. We investigated the effects of a common parasite, the microsporidian Pleistophora mulleri, on the cannibalism rate of its host, the freshwater amphipod Gammarus duebeni celticus. Parasitic infection increased the rate of cannibalism by adults towards uninfected juvenile conspecifics, as measured by adult functional responses, that is, the rate of resource uptake as a function of resource density. This may reflect the increased metabolic requirements of the host as driven by the parasite. Furthermore, when presented with a choice, uninfected adults preferred to cannibalize uninfected rather than infected juvenile conspecifics, probably reflecting selection pressure to avoid the risk of parasite acquisition. By contrast, infected adults were indiscriminate with respect to infection status of their victims, probably owing to metabolic costs of infection and the lack of risk as the cannibals were already infected. Thus parasitism, by enhancing cannibalism rates, may have previously unrecognized effects on stage structure and population dynamics for cannibalistic species and may also act as a selective pressure leading to changes in resource use.

Hook, Line and Infection: A Guide to Culturing Parasites, Establishing Infections and Assessing Immune Responses in the Three-Spined Stickleback

The three-spined stickleback (Gasterosteus aculeatus) is a model organism with an extremely well-characterized ecology, evolutionary history, behavioural repertoire and parasitology that is coupled with published genomic data. These small temperate zone fish therefore provide an ideal experimental system to study common diseases of coldwater fish, including those of aquacultural importance. However, detailed information on the culture of stickleback parasites, the establishment and maintenance of infections and the quantification of host responses is scattered between primary and grey literature resources, some of which is not readily accessible. Our aim is to lay out a framework of techniques based on our experience to inform new and established laboratories about culture techniques and recent advances in the field. Here, essential knowledge on the biology, capture and laboratory maintenance of sticklebacks, and their commonly studied parasites is drawn together, highlighting recent advances in our understanding of the associated immune responses. In compiling this guide on the maintenance of sticklebacks and a range of common, taxonomically diverse parasites in the laboratory, we aim to engage a broader interdisciplinary community to consider this highly tractable model when addressing pressing questions in evolution, infection and aquaculture.