Keith D. Farnsworth

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.

Ecological impacts of an invasive predator explained and predicted by comparative functional responses

Forecasting the ecological impacts of invasive species is a major challenge that has seen little progress, yet the development of robust predictive approaches is essential as new invasion threats continue to emerge. A common feature of ecologically damaging invaders is their ability to rapidly exploit and deplete resources. We thus hypothesized that the ‘functional response’ (the relationship between resource density and consumption rate) of such invasive species might be of consistently greater magnitude than those of taxonomically and/or trophically similar native species. Here, we derived functional responses of the predatory Ponto-Caspian freshwater ‘bloody red’ shrimp, Hemimysis anomala, a recent and ecologically damaging invader in Europe and N. America, in comparison to the local native analogues Mysis salemaai and Mysis diluviana in Ireland and Canada, respectively. This was conducted in a novel set of experiments involving multiple prey species in each geographic location and a prey species that occurs in both regions. The predatory functional responses of the invader were generally higher than those of the comparator native species and this difference was consistent across invaded regions. Moreover, those prey species characterized by the strongest and potentially de-stabilizing Type II functional responses in our laboratory experiments were the same prey species found to be most impacted by H. anomala in the field. The impact potential of H. anomala was further indicated when it exhibited similar or higher attack rates, consistently lower prey handling times and higher maximum feeding rates compared to those of the two Mysis species, formerly known as ‘Mysis relicta’, which itself has an extensive history of foodweb disruption in lakes to which it has been introduced. Comparative functional responses thus merit further exploration as a methodology for predicting severe community-level impacts of current and future invasive species and could be entered into risk assessment protocols.

Comparison of the functional responses of invasive and native amphipods

While we can usually understand the impacts of invasive species on recipient communities, invasion biology lacks methodologies that are potentially more predictive. Such tools should ideally be straightforward and widely applicable. Here, we explore an approach that compares the functional responses (FRs) of invader and native amphipod crustaceans. Dikerogammarus villosus is a Ponto-Caspian amphipod currently invading Europe and poised to invade North America. Compared with other amphipods that it actively replaces in freshwaters, D. villosus exhibited significantly greater predation, consuming significantly more prey with a higher type II FR. This corroborates the known dramatic field impacts of D. villosus on invaded communities. In another species, FRs were nearly identical in invasive and native ranges. We thus propose that if FRs of other taxa and trophic groups follow such general patterns, this methodology has potential in predicting future invasive species impacts.

How do grazers achieve their distribution? A continuum of models from random diffusion to the ideal free distribution using biased random walks

A conceptual model is described for generating distributions of grazing animals, according to their searching behavior, to investigate the mechanisms animals may use to achieve their distributions. The model simulates behaviors ranging from random diffusion, through taxis and cognitively aided navigation (i.e., using memory), to the optimization extreme of the Ideal Free Distribution. These behaviors are generated from simulation of biased diffusion that operates at multiple scales simultaneously, formalizing ideas of multiple‐scale foraging behavior. It uses probabilistic bias to represent decisions, allowing multiple search goals to be combined (e.g., foraging and social goals) and the representation of suboptimal behavior. By allowing bias to arise at multiple scales within the environment, each weighted relative to the others, the model can represent different scales of simultaneous decision‐making and scale‐dependent behavior. The model also allows different constraints to be applied to the animals ability (e.g., applying food‐patch accessibility and information limits). Simulations show that foraging‐decision randomness and spatial scale of decision bias have potentially profound effects on both animal intake rate and the distribution of resources in the environment. Spatial variograms show that foraging strategies can differentially change the spatial pattern of resource abundance in the environment to one characteristic of the foraging strategy.

Parasitism may enhance rather than reduce the predatory impact of an invader

Invasive species can have profound impacts on communities and it is increasingly recognized that such effects may be mediated by parasitism. The ‘enemy release’ hypothesis posits that invaders may be successful and have high impacts owing to escape from parasitism. Alternatively, we hypothesize that parasites may increase host feeding rates and hence parasitized invaders may have increased community impacts. Here, we investigate the influence of parasitism on the predatory impact of the invasive freshwater amphipod Gammarus pulex. Up to 70 per cent of individuals are infected with the acanthocephalan parasite Echinorhynchus truttae, but parasitized individuals were no different in body condition to those unparasitized. Parasitized individuals consumed significantly more prey (Asellus aquaticus; Isopoda) than did unparasitized individuals. Both parasitized and unparasitized individuals displayed Type-II functional responses (FRs), with the FR for parasitized individuals rising more steeply, with a higher asymptote, compared with unparasitized individuals. While the parasite reduced the fitness of individual females, we predict a minor effect on population recruitment because of low parasite prevalence in the peak reproductive period. The parasite thus has a large per capita effect on predatory rate but a low population fitness effect, and thus may enhance rather than reduce the impact of this invader.

Grassland‐Herbivore Interactions: How Do Grazers Coexist?

We develop a new approach to modeling grazing systems that links foraging characteristics (intake and digestive constraints) with resource dynamics via the probability of encounter with different grass heights. Three complementary models are presented: the generation of a grass height structure through selective grazing; investigating the conditions for consumer coexistence; and, using a simplified resource structure, the consequences for consumer abundance. The main finding is that coexistence between grazers differing in body size is possible if a single‐resource type becomes differentiated in its height structure. Large grazers can facilitate food availability for smaller species but with the latter being competitively dominant. The relative preference given to different resource partitions is important in determining the nature of population interactions. Large‐body and small‐body grazer populations can interact through competitive, parasitic, commensalist, or amensalist relationships, depending on the way they partition the resource as well as their relative populations and the dynamics of resource renewal. The models provide new concepts of multispecies carrying capacity (stock equilibrium) in grazed systems with implications for conservation and management. We conclude that consumer species are not substitutable; therefore, the use of rangeland management concepts such as “livestock units” may be inappropriate.

Animal foraging from an individual perspective : an object orientated model

A model system, HOOFS (Hierarchical Object Orientated Foraging Simulator), has been developed to study foraging by animals in a complex environment. The model is implemented using an individual-based object-orientated structure. Different species of animals inherit their general properties from a generic animal object which inherits from the basic dynamic object class. Each dynamic object is a separate program thread under the control of a central scheduler. The environment is described as a map of small hexagonal patches, each with their own level of resources and a patch-specific rate of resource replenishment. Each group of seven patches (0th order) is grouped into a 1st order super-patch with seven nth order super-patches making up a n+1th order super-patch for n up to a specified value. At any time each animal is associated with a single patch. Patch choice is made by combining the information on the resources available within different order patches and super-patches along with information on the spatial location of other animals. The degree of sociality of an animal is defined in terms of optimal spacing from other animals and by the weighting of patch choice based on social factors relative to that based on food availability. Information, available to each animal, about patch resources diminishes with distance from that patch. The model has been used to demonstrate that social interactions can constrain patch choice and result in a short-term reduction of intake and a greater degree of variability in the level of resources in patches. We used the model to show that the effect of this variability on the animal’s intake depends on the pattern of patch replenishment.

How optimal life history changes with the community size-spectrum

This paper derives optimal life histories for fishes or other animals in relation to the size spectrum of the ecological community in which they are both predators and prey. Assuming log-linear size-spectra and well known scaling laws for feeding and mortality, we first construct the energetics of the individual. From these we find, using dynamic programming, the optimal allocation of energy between growth and reproduction as well as the trade-off between offspring size and numbers. Optimal strategies were found to be strongly dependent on size spectrum slope. For steep size spectra (numbers declining rapidly with size), determinate growth was optimal and allocation to somatic growth increased rapidly with increasing slope. However, restricting reproduction to a fixed mating season changed optimal allocations to give indeterminate growth approximating a von Bertalanffy trajectory. The optimal offspring size was as small as possible given other restrictions such as newborn starvation mortality. For shallow size spectra, finite optimal maturity size required a decline in fitness for large size or age. All the results are compared with observed size spectra of fish communities to show their consistency and relevance.

Assessing the sensitivity and specificity of fish community indicators to management action

We assessed ten trophodynamic indicators of ecosystem status for their sensitivity and specificity to fishing man- agement using a size-resolved multispecies fish community model. The responses of indicators to fishing depended on effort and the size selectivity (sigmoid or Gaussian) of fishing mortality. The highest specificity against sigmoid (trawl-like) size selection was seen from inverse fishing pressure and the large fish indicator, but for Gaussian size selection, the large spe- cies indicator was most specific. Biomass, mean trophic level of the community and of the catch, and fishing in balance had the lowest specificity against both size selectivities. Length-based indicators weighted by biomass, rather than abun- dance, were more sensitive and specific to fishing pressure. Most indicators showed a greater response to sigmoid than Gaussian size selection. Indicators were generally more sensitive at low levels of effort because of nonlinear sensitivity in trophic cascades to fishing mortality. No single indicator emerged as superior in all respects, so given available data, multi- ple complementary indicators are recommended for community monitoring in the ecosystem approach to fisheries manage- ment.

Allometric analysis of Sitka spruce branches : mechanical versus hydraulic design principles

The geometry of tree branches can have considerable effect on their efficiency in terms of carbon export per unit carbon investment in structure. The purpose of this study was to evaluate different design criteria using data describing the form of Picea sitchensis branches. Allometric analysis of the data suggests that resources are distributed to favour shoots with the greatest opportunity for extension into new space, with priority to the extension of the leader. The distribution of allometric relations of links (branch elements) was tested against two models: the pipe model, based on hydraulic transport requirements, and a static load model based on the requirement of shoots to provide mechanical resistance to static loads. Static load resistance required the load parameter to be proportional to the link radius raised to the power of 4. This was shown to be true within a 95% statistical confidence limit. The pipe model would require total distal length to be proportional to link radius squared but the measured branches did not conform well to this model. The comparison suggests that the diameters of branch elements were more related to the requirements for mechanical load. The cost of following a hydraulic design principle (the pipe model) in terms of mechanical efficiency was estimated and suggested that the pipe model branch would not be mechanically compromised but would use structural resources inefficiently. Resource allocation among branch elements was found to be consistent with mechanical stability criteria but also indicated the possibility of allocation based on other criteria, such as potential light interception by shoots. The evidence suggests that whilst branch topology increments by reiteration of units of morphogenesis, the geometry follows a functional design pattern.