Eco‐evolutionary experience in novel species interactions

A better understanding of how ecological novelty influences interactions in new combinations of species is key for predicting interaction outcomes, and can help focus conservation and management efforts on preventing the introduction of novel organisms or species (including invasive species, GMOs, synthetic organisms, resurrected species and emerging pathogens) that seem particularly ‘risky’ for resident species. Here, we consider the implications of different degrees of eco‐evolutionary experience of interacting resident and non‐resident species, define four qualitative risk categories for estimating the probability of successful establishment and impact of novel species and discuss how the effects of novelty change over time. Focusing then on novel predator–prey interactions, we argue that novelty entails density‐dependent advantages for non‐resident species, with their largest effects often being at low prey densities. This is illustrated by a comparison of predator functional responses and prey predation risk curves between novel species and ecologically similar resident species, and raises important issues for the conservation of endangered resident prey species.     

Predation and avoidance behaviour in aphid‐ladybird interactions of native and invasive ladybirds in Europe

1. While detrimental effects of invasive predators on native species are well documented, we often lack a mechanistic understanding of the invasion success. Lack of prey avoidance behaviour can lead to higher consumption rates by invasive predators compared to native predators. This competitive advantage is expected to contribute to the invasion success of non‐native predators.
2. We compared aphid consumption and cue avoidance behaviour of aphids between four native ladybird species (Coccinella septempunctata, Adalia bipunctata, Propylea quatuordecimpunctata, and Hippodamia variegata) and the invasive Asian ladybird Harmonia axyridis.
3. The invasive H. axyridis and the native C. septempunctata consumed more aphids than the three smaller native ladybird species. In line with our expectations, aphids avoided leaves bearing cues of most native ladybird species but not of the invasive H. axyridis.
4. Our results indicate that body size rather than ladybird origin determined aphid predation rates. The lack of aphid avoidance behaviour towards cues of H. axyridis indicates that they were not able to recognise the chemical cues of the invasive predator.
5. Relatively large body size and the absence of cue avoidance in aphids might benefit the invasive H. axyridis, particularly in comparison to smaller native ladybird species. The absence of avoidance behaviour in aphids might lead to even higher predation rates of H. axyridis under more natural conditions.

     

Out of the pot and into the fire: Explaining the vulnerability of an endangered small headwater stream fish to black‐bass Micropterus spp. invasion

Introduced predatory fishes have had consistently severe consequences for native fishes in stream environments around the world, although the drivers of these effects are often unclear. In the Swartkops River headwaters in South Africa, native Eastern Cape redfin Pseudobarbus afer were always absent from sites occupied by non‐native black basses Micropterus salmoides and Micropterus dolomieu, but generally co‐occurred with the native predators Anguilla marmorata and Anguilla mossambica. A natural experiment provided by flood‐mediated recolonization of black‐bass occupied sites by P. afer demonstrated depletion in black‐bass invaded sites. Field behavioural observations of P. afer indicated that they foraged among benthic cover during the day, but suspended in open water at night. As the nocturnal A. marmorata and A. mossambica foraged actively within structural cover at night and M. dolomieu and M. salmoides are diurnal or crepuscular predators, P .afer is thus optimized to avoid predation by native anguillid predators and not the functionally unique predatory black basses. The integration of distributional, temporal population dynamics and behavioural data suggests that the severe effects of Micropterus spp. are probably a consequence of prey naïveté and behaviour evolved to evade native predators.     

Systematic deviations from linear size spectra of lake fish communities are correlated with predator–prey interactions and lake‐use intensity

Size structure of organisms at logarithmic scale (i.e. size spectrum) can often be described by a linear function with a negative slope; however, substantial deviations from linearity have often been found in natural systems. Theoretical studies suggest that greater nonlinearity in community size spectrum is associated with high predator–prey size ratios but low predator–prey abundance ratios; however, empirical evaluation of the effects of predator–prey interactions on nonlinear structures remains scarce. Here, we aim to empirically explore the pattern of the size‐specific residuals (i.e. deviations from the linear regression between the logarithmic fish abundance and the logarithmic mean fish size) by using size spectra of fish communities in 74 German lakes. We found that nonlinearity was strong in lakes with high predator–prey abundance ratios but at low predator–prey size ratios. More specifically, our results suggest that only large predators, even if occurring in low abundances, can control the density of prey fishes in a broad range of size classes in a community and thus promote linearity in the size spectrum. In turn, the lack of large predator fishes may cause high abundances of fish in intermediate size classes, resulting in nonlinear size spectra in these lakes. Moreover, these lakes were characterized by a more intense human use including high fishing pressure and high total phosphorus concentrations, which have negative impacts on the abundance of large, predatory fish. Our findings indicate that nonlinear size spectra may reflect dynamical processes potentially caused by predator–prey interactions. This opens a new perspective in the research on size spectrum, and can be relevant to further quantify the efficiency of energy transfer in aquatic food webs.     

Predator–prey interactions in the canopy

Small mammal abundances are frequently limited by resource availability, but predators can exert strong lethal (mortality) and nonlethal (e.g., nest abandonment) limitations. Artificially increasing resource availability for uncommon small mammals provides a unique opportunity to examine predator–prey interactions. We used remote cameras to monitor 168 nest platforms placed in the live tree canopy (n = 23 young forest stands), primarily for arboreal red tree voles (tree voles; Arborimus longicaudus), over 3 years (n = 15,510 monitoring‐weeks). Tree voles frequently built nests and were detected 37% of monitoring‐weeks, whereas flying squirrels (Glaucomys oregonensis) built nests infrequently but were detected 45% of monitoring‐weeks. Most nest predators were detected infrequently (<1% of monitoring‐weeks) and were positively correlated with tree vole presence. Weasels (Mustela spp.) were highly effective predators of tree voles (n = 8 mortalities; 10% of detections) compared to owls (n = 1), flying squirrels (n = 2), and Steller's jays (n = 1). Tree vole activity decreased from 84.1 (95% confidence interval [CI]: 56.2, 111.9) detections/week 1‐week prior to a weasel detection to 4.7 detections/week (95% CI: 1.7, 7.8) 1‐week postdetection and remained low for at least 12 weeks. Interpretations of predator–prey interactions were highly sensitive to how we binned continuously collected data and model results from our finest bin width were biologically counter‐intuitive. Average annual survival of female tree voles was consistent with a previous study (0.14; 95% CI: ?0.04 [0.01], 0.32) and high compared to many terrestrial voles. The relative infrequency of weasel detections and inefficiency of other predators did not provide strong support for the hypothesis that predation per se limited populations. Rather, predation pressure, by reducing occupancy of already scarce nest sites through mortality and nest abandonment, may contribute to long‐term local instability of tree vole populations in young forests. Additional monitoring would be needed to assess this hypothesis.     

Messy eaters: Swabbing prey DNA from the exterior of inconspicuous predators when foraging cannot be observed

Complex coevolutionary relationships among competitors, predators, and prey have shaped taxa diversity, life history strategies, and even the avian migratory patterns we see today. Consequently, accurate documentation of prey selection is often critical for understanding these ecological and evolutionary processes. Conventional diet study methods lack the ability to document the diet of inconspicuous or difficult‐to‐study predators, such as those with large home ranges and those that move vast distances over short amounts of time, leaving gaps in our knowledge of trophic interactions in many systems. Migratory raptors represent one such group of predators where detailed diet studies have been logistically challenging. To address knowledge gaps in the foraging ecology of migrant raptors and provide a broadly applicable tool for the study of enigmatic predators, we developed a minimally invasive method to collect dietary information by swabbing beaks and talons of raptors to collect trace prey DNA. Using previously published COI primers, we were able to isolate and reference gene sequences in an open‐access barcode database to identify prey to species. This method creates a novel avenue to use trace molecular evidence to study prey selection of migrating raptors and will ultimately lead to a better understanding of raptor migration ecology. In addition, this technique has broad applicability and can be used with any wildlife species where even trace amounts of prey debris remain on the exterior of the predator after feeding.     

Spine and dine: A key defensive trait promotes ecological success in spiny ants

A key focus of ecologists is explaining the origin and maintenance of morphological diversity and its association with ecological success. We investigate potential benefits and costs of a common and varied morphological trait, cuticular spines, for foraging behavior, interspecific competition, and predator–prey interactions in naturally co‐occurring spiny ants (Hymenoptera: Formicidae: Polyrhachis) in an experimental setting. We expect that a defensive trait like spines might be associated with more conspicuous foraging, a greater number of workers sent out to forage, and potentially increased competitive ability. Alternatively, consistent with the ecological trade‐off hypothesis, we expect that investment in spines for antipredator defense might be negatively correlated with these other ecological traits. We find little evidence for any costs to ecological traits, instead finding that species with longer spines either outperform or do not differ from species with shorter spines for all tested metrics, including resource discovery rate and foraging effort as well as competitive ability and antipredator defense. Spines appear to confer broad antipredator benefits and serve as a form of defense with undetectable costs to key ecological abilities like resource foraging and competitive ability, providing an explanation for both the ecological success of the study genus and the large number of evolutionary origins of this trait across all ants. This study also provides a rare quantitative empirical test of ecological effects related to a morphological trait in ants.     

Revolution in food web analysis and trophic ecology: diet analysis by DNA and stable isotope analysis

Characterization of energy flow in ecosystems is one of the primary goals of ecology, and the analysis of trophic interactions and food web dynamics is key to quantifying energy flow. Predator‐prey interactions define the majority of trophic interactions and food web dynamics, and visual analysis of stomach, gut or fecal content composition is the technique traditionally used to quantify predator‐prey interactions. Unfortunately such techniques may be biased and inaccurate due to variation in digestion rates ( Sheppard & Hardwood 2005 ); however, those limitations can be largely overcome with new technology. In the last 20 years, the use of molecular genetic techniques in ecology has exploded ( King et al. 2008 ). The growing availability of molecular genetic methods and data has fostered the use of PCR‐based techniques to accurately distinguish and identify prey items in stomach, gut and fecal samples. In this month’s issue of Molecular Ecology Resources, Corse et al. (2010) describe and apply a new approach to quantifying predator‐prey relationships using an ecosystem‐level genetic characterization of available and consumed prey in European freshwater habitats ( Fig. 1a ). In this issue of Molecular Ecology, Hardy et al. (2010) marry the molecular genetic analysis of prey with a stable isotope (SI) analysis of trophic interactions in an Australian reservoir community ( Fig. 1b ). Both papers demonstrate novel and innovative approaches to an old problem – how do we effectively explore food webs and energy movement in ecosystems?

Figure 1 Open in figure viewer PowerPoint The aquatic habitats used for two studies of diet and trophic interactions that employed molecular genetic and stable isotope analyses. Panel a: Example of Rhone basin habitat (France) where fish diet was determined using PCR to classify prey to a series of ecological clades (photo by Emmanuel Corse). Panel b: A weir pool on the lower Murray River (Australia) where food web and prey use was evaluated using a combination of advanced molecular genetic and stable isotope analyses (photo credit: CSIRO).     

Sea‐ice loss boosts visual search: fish foraging and changing pelagic interactions in polar oceans

Light is a central driver of biological processes and systems. Receding sea ice changes the lightscape of high‐latitude oceans and more light will penetrate into the sea. This affects bottom‐up control through primary productivity and top‐down control through vision‐based foraging. We model effects of sea‐ice shading on visual search to develop a mechanistic understanding of how climate‐driven sea‐ice retreat affects predator–prey interactions. We adapt a prey encounter model for ice‐covered waters, where prey‐detection performance of planktivorous fish depends on the light cycle. We use hindcast sea‐ice concentrations (past 35 years) and compare with a future no‐ice scenario to project visual range along two south–north transects with different sea‐ice distributions and seasonality, one through the Bering Sea and one through the Barents Sea. The transect approach captures the transition from sub‐Arctic to Arctic ecosystems and allows for comparison of latitudinal differences between longitudes. We find that past sea‐ice retreat has increased visual search at a rate of 2.7% to 4.2% per decade from the long‐term mean; and for high latitudes, we predict a 16‐fold increase in clearance rate. Top‐down control is therefore predicted to intensify. Ecological and evolutionary consequences for polar marine communities and energy flows would follow, possibly also as tipping points and regime shifts. We expect species distributions to track the receding ice‐edge, and in particular expect species with large migratory capacity to make foraging forays into high‐latitude oceans. However, the extreme seasonality in photoperiod of high‐latitude oceans may counteract such shifts and rather act as a zoogeographical filter limiting poleward range expansion. The provided mechanistic insights are relevant for pelagic ecosystems globally, including lakes where shifted distributions are seldom possible but where predator–prey consequences would be much related. As part of the discussion on photoperiodic implications for high‐latitude range shifts, we provide a short review of studies linking physical drivers to latitudinal extent.     

Size‐based interactions across trophic levels in food webs of shallow Mediterranean lakes

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Overcoming prey naiveté: Free‐living marsupials develop recognition and effective behavioral responses to alien predators in Australia

Naiveté in prey arises from novel ecological mismatches in cue recognition systems and antipredator responses following the arrival of alien predators. The multilevel naiveté framework suggests that animals can progress through levels of naiveté toward predator awareness. Alternatively, native prey may be preadapted to recognize novel predators via common constituents in predator odors or familiar predator archetypes. We tested predictions of these competing hypotheses on the mechanisms driving behavioral responses of native species to alien predators by measuring responses of native free‐living northern brown bandicoots (Isoodon macrourus) to alien red fox (Vulpes vulpes) odor. We compared multiple bandicoot populations either sympatric or allopatric with foxes. Bandicoots sympatric with foxes showed recognition and appropriate antipredator behavior toward fox odor via avoidance. On the few occasions bandicoots did visit, their vigilance significantly increased, and their foraging decreased. In contrast, bandicoots allopatric with foxes showed no recognition of this predator cue. Our results suggest that vulnerable Australian mammals were likely naïve to foxes when they first arrived, which explains why so many native mammals declined soon after fox arrival. Our results also suggest such naiveté can be overcome within a relatively short time frame, driven by experience with predators, thus supporting the multilevel naiveté framework.     

Impacts of an invasive ant species on roosting behavior of an island endemic flying‐fox

Introduced species can cause major disruptions to ecosystems, particularly on islands. On Christmas Island, the invasive yellow crazy ant (Anoplolepis gracilipes) has detrimental impacts on many animals ranging from the iconic red crabs (Gecarcoidea natalis) to the Christmas Island Thrush (Turdus poliocephalus erythropleurus). However, the full extent of its effects on the island's fauna is not yet known. In this study, we investigated the impact of the yellow crazy ants on the island's last native mammal: the Christmas Island flying‐fox (Pteropus natalis). This species has been described as a keystone species, but has recently experienced substantial population decline to the extent that it is now listed as Critically Endangered. We examined the impacts of the yellow crazy ants on the roosting behavior of the Christmas Island flying‐fox, and on its local and island‐wide distribution patterns. We showed that the crazy ants increased behaviors in the flying‐foxes that were associated with avoidance of noxious stimuli and decreased behaviors associated with resting. Roost tree selection and roost site location were not related to variation in the abundance of crazy ants on the island. Our results indicate that the crazy ants interfere with the activity budgets of the flying‐foxes. However, the flying‐foxes failed to relocate to ant‐free roost trees or roost sites when confronted with the noxious ant, suggesting that the flying‐foxes are either not sufficiently disturbed to override strong cultural attachment to roosts, or, are behaving maladaptively due to ecological naïveté.     

Temperature and prey density jointly influence trophic and non‐trophic interactions in multiple predator communities

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Phenotypic plasticity in oysters (Crassostrea virginica) mediated by chemical signals from predators and injured prey

Prey organisms reduce predation risk by altering their behavior, morphology, or life history. Avoiding or deterring predators often incurs costs, such as reductions in growth or fecundity. Prey minimize costs by limiting predator avoidance or deterrence to situations that pose significant risk of injury or death, requiring them to gather information regarding the relative threat potential predators pose. Chemical cues are often used for risk evaluation, and we investigated morphological responses of oysters (Crassostrea virginica) to chemical cues from injured conspecifics, from heterospecifics, and from predatory blue crabs (Callinectes sapidus) reared on different diets. Previous studies found newly settled oysters reacted to crab predators by growing heavier, stronger shells, but that adult oysters did not. We exposed oysters at two size classes (newly settled oyster spat and juveniles ~2.0 cm) to predation risk cue treatments including predator or injured prey exudates and to seawater controls. Since both of the size classes tested can be eaten by blue crabs, we hypothesized that both would react to crab exudates by producing heavier, stronger shells. Oyster spat grew heavier shells that required significantly more force to break, an effective measure against predatory crabs, when exposed to chemical exudates from blue crabs as compared to controls. When exposed to chemical cues from injured conspecifics or from injured clams (Mercenaria mercenaria), a sympatric bivalve, shell mass and force were intermediate between predator treatments and controls, indicating that oysters react to injured prey cues but not as strongly as to cues released by predators. Juvenile oysters of ~ 2.0 cm did not significantly alter their shell morphology in any of the treatments. Thus, newly settled oysters can differentiate between predatory threats and adjust their responses accordingly, with the strongest responses being to exudates released by predators, but oysters of 2.0 cm and larger do not react morphologically to predatory threats.     

Diversity and coexistence are influenced by time‐dependent species interactions in a predator–prey system

Although numerous studies show that communities are jointly influenced by predation and competitive interactions, few have resolved how temporal variability in these interactions influences community assembly and stability. Here, we addressed this challenge in experimental microbial microcosms by employing empirical dynamic modelling tools to: (1) detect causal interactions between prey species in the absence and presence of a predator; (2) quantify the time‐varying strength of these interactions and (3) explore stability in the resulting communities. Our findings show that predators boost the number of causal interactions among community members, and lead to reduced dynamic stability, but higher coexistence among prey species. These results correspond to time‐varying changes in species interactions, including emergence of morphological characteristics that appeared to reduce predation, and indirectly facilitate growth of predator‐susceptible species. Jointly, our findings suggest that careful consideration of both context and time may be necessary to predict and explain outcomes in multi‐trophic systems.     

Little evidence of a road‐effect zone for nocturnal,flying insects

Roads and traffic may be contributing to global declines of insect populations. The ecological effects of roads often extend far into the surrounding habitat, over a distance known as the road‐effect zone. The quality of habitat in the road‐effect zone is generally degraded (e.g., due to edge effects, noise, light, and chemical pollution) and can be reflected in species presence, abundance, or demographic parameters. Road‐effect zones have been quantified for some vertebrate species but are yet to be quantified for insects. Investigating the road‐effect zone for insects will provide a better understanding of how roads impact ecosystems, which is particularly important given the role insects play as pollinators, predators, and prey for other species. We quantified the road‐effect zone for nocturnal flying insects along three major freeways in agricultural landscapes in southeast Australia. We collected insects using light traps at six points along 2‐km transects perpendicular to each highway (n = 17). We sorted the samples into order, and dried and weighed each order to obtain a measure of dry biomass. Using regression models within a Bayesian framework of inference, we estimated the change in biomass of each order with distance from the road, while accounting for environmental variables such as temperature, moon phase, and vegetation structure. The biomass of nine of the ten orders sampled did not change with distance from the freeway. Orthoptera (i.e., grasshoppers and crickets) was the only order whose biomass increased with distance from the freeway. From our findings, we suggest that the impacts of roads on insects are unlikely extending into the surrounding landscape over a distance of 2 km. Therefore, if there are impacts of roads on insects, these are more likely to be concentrated at the road itself, or on finer taxonomic scales such as family or genus level.     

Little evidence for morphological change in a resilient endemic species following the introduction of a novel predator

Human activities, such as species introductions, are dramatically and rapidly altering natural ecological processes and often result in novel selection regimes. To date, we still have a limited understanding of the extent to which such anthropogenic selection may be driving contemporary phenotypic change in natural populations. Here, we test whether the introduction of the piscivorous Nile perch, Lates niloticus, into East Africa's Lake Victoria and nearby lakes coincided with morphological change in one resilient native prey species, the cyprinid fish Rastrineobola argentea. Drawing on prior ecomorphological research, we predicted that this novel predator would select for increased allocation to the caudal region in R. argentea to enhance burst‐swimming performance and hence escape ability. To test this prediction, we compared body morphology of R. argentea across space (nine Ugandan lakes differing in Nile perch invasion history) and through time (before and after establishment of Nile perch in Lake Victoria). Spatial comparisons of contemporary populations only partially supported our predictions, with R. argentea from some invaded lakes having larger caudal regions and smaller heads compared to R. argentea from uninvaded lakes. There was no clear evidence of predator‐associated change in body shape over time in Lake Victoria. We conclude that R. argentea have not responded to the presence of Nile perch with consistent morphological changes and that other factors are driving observed patterns of body shape variation in R. argentea.