Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions

We present a framework for explaining variation in predator invasion success and predator impacts on native prey that integrates information about predator–prey naïveté, predator and prey behavioral responses to each other, consumptive and non-consumptive effects of predators on prey, and interacting effects of multiple species interactions. We begin with the ‘naïve prey’ hypothesis that posits that naïve, native prey that lack evolutionary history with non-native predators suffer heavy predation because they exhibit ineffective antipredator responses to novel predators. Not all naïve prey, however, show ineffective antipredator responses to novel predators. To explain variation in prey response to novel predators, we focus on the interaction between prey use of general versus specific cues and responses, and the functional similarity of non-native and native predators. Effective antipredator responses reduce predation rates (reduce consumptive effects of predators, CEs), but often also carry costs that result in non-consumptive effects (NCEs) of predators. We contrast expected CEs versus NCEs for non-native versus native predators, and discuss how differences in the relative magnitudes of CEs and NCEs might influence invasion dynamics. Going beyond the effects of naïve prey, we discuss how the ‘naïve prey’, ‘enemy release’ and ‘evolution of increased competitive ability’ (EICA) hypotheses are inter-related, and how the importance of all three might be mediated by prey and predator naïveté. These ideas hinge on the notion that non-native predators enjoy a ‘novelty advantage’ associated with the naïveté of native prey and top predators. However, non-native predators could instead suffer from a novelty disadvantage because they are also naïve to their new prey and potential predators. We hypothesize that patterns of community similarity and evolution might explain the variation in novelty advantage that can underlie variation in invasion outcomes. Finally, we discuss management implications of our framework, including suggestions for managing invasive predators, predator reintroductions and biological control.

Effects of an extreme temperature event on the behavior and age structure of an estuarine top predator, Carcharhinus leucas

The frequency of extreme environmental events is predicted to increase in the future. Understanding the short- and long-term impacts of these extreme events on large-bodied predators will provide insight into the spatial and temporal scales at which acute environmental disturbances in top-down processes may persist within and across ecosystems. Here, we use long-term studies of movements and age structure of an estuarine top predator—juvenile bull sharks Carcharhinus leucas—to identify the effects of an extreme ‘cold snap’ from 2 to 13 January 2010 over short (weeks) to intermediate (months) time scales. Juvenile bull sharks are typically year-round residents of the Shark River Estuary until they reach 3 to 5 yr of age. However, acoustic telemetry revealed that almost all sharks either permanently left the system or died during the cold snap. For 116 d after the cold snap, no sharks were detected in the system with telemetry or captured during longline sampling. Once sharks returned, both the size structure and abundance of the individuals present in the nursery had changed considerably. During 2010, individual longlines were 70% less likely to capture any sharks, and catch rates on successful longlines were 40% lower than during 2006−2009. Also, all sharks caught after the cold snap were young-of-the-year or neonates, suggesting that the majority of sharks in the estuary were new recruits and several cohorts had been largely lost from the nursery. The longer-term impacts of this change in bull shark abundance to the trophic dynamics of the estuary and the importance of episodic disturbances to bull shark population dynamics will require continued monitoring, but are of considerable interest because of the ecological roles of bull sharks within coastal estuaries and oceans.

A Suite of Prey Traits Determine Predator and Nutrient Enrichment Effects in a Tri-Trophic Food Chain

Predation, predation risk, and resource quality affect suites of prey traits that collectively impact individual fitness, population dynamics, and community structure. However, studies of multi-trophic level effects generally focus on a single prey trait, failing to capture trade-offs among suites of covarying traits that govern population responses and emergent community patterns. We used structural equation models (SEM) to summarize the non-lethal and lethal effects of crayfish, Procambarus fallax, and phosphorus (P) addition, which affected prey food quality (periphyton), on the interactive effects of behavioral, morphological, developmental, and reproductive traits of snails, Planorbella duryi. Univariate and multivariate analyses suggested trade-offs between production (growth, reproduction) and defense (foraging behavior, shell shape) traits of snails in response to non-lethal crayfish and P addition, but few lethal effects. SEM revealed that non-lethal crayfish effects indirectly limited per capita offspring standing stock by increasing refuge use, slowing individual growth, and inducing snails to produce thicker, compressed shells. The negative effects of non-lethal crayfish on snails were strongest with P addition; snails increased allocation to shell defense rather than growth or reproduction. However, compared to ambient conditions, P addition with non-lethal crayfish still yielded greater per capita offspring standing stock by speeding individual snail growth enabling them to produce more offspring that also grew faster. Increased refuge use in response to non-lethal crayfish led to a non-lethal trophic cascade that altered the spatial distribution of periphyton. Independent of crayfish effects, snails stimulated periphyton growth through nutrient regeneration. These findings illustrate the importance of studying suites of traits that reveal costs associated with inducing different traits and how expressing those traits impacts population and community level processes.

Origin of facultative heterochromatin in the endosperm of Gagea lutea (Liliaceae)

Peer reviewed

Origin of facultative heterochromatin in the endosperm of Gagea lutea (Liliaceae)

Peer reviewed

Spatial Relationships among Hydroacoustic, Hydrographic and Top Predator Patterns: Cetacean Distributions in the Mid-Atlantic Bight

Effective conservation and management of top predators requires a comprehensive understanding of their distributions and of the underlying biological and physical processes that affect these distributions. The Mid-Atlantic Bight shelf break system is a dynamic and productive region where at least 32 species of cetaceans have been recorded through various systematic and opportunistic marine mammal surveys from the 1970s through 2012. My dissertation characterizes the spatial distribution and habitat of cetaceans in the Mid-Atlantic Bight shelf break system by utilizing marine mammal line-transect survey data, synoptic multi-frequency active acoustic data, and fine-scale hydrographic data collected during the 2011 summer Atlantic Marine Assessment Program for Protected Species (AMAPPS) survey. Although studies describing cetacean habitat and distributions have been previously conducted in the Mid-Atlantic Bight, my research specifically focuses on the shelf break region to elucidate both the physical and biological processes that influence cetacean distribution patterns within this cetacean hotspot.

In Chapter One I review biologically important areas for cetaceans in the Atlantic waters of the United States. I describe the study area, the shelf break region of the Mid-Atlantic Bight, in terms of the general oceanography, productivity and biodiversity. According to recent habitat-based cetacean density models, the shelf break region is an area of high cetacean abundance and density, yet little research is directed at understanding the mechanisms that establish this region as a cetacean hotspot.

In Chapter Two I present the basic physical principles of sound in water and describe the methodology used to categorize opportunistically collected multi-frequency active acoustic data using frequency responses techniques. Frequency response classification methods are usually employed in conjunction with net-tow data, but the logistics of the 2011 AMAPPS survey did not allow for appropriate net-tow data to be collected. Biologically meaningful information can be extracted from acoustic scattering regions by comparing the frequency response curves of acoustic regions to theoretical curves of known scattering models. Using the five frequencies on the EK60 system (18, 38, 70, 120, and 200 kHz), three categories of scatterers were defined: fish-like (with swim bladder), nekton-like (e.g., euphausiids), and plankton-like (e.g., copepods). I also employed a multi-frequency acoustic categorization method using three frequencies (18, 38, and 120 kHz) that has been used in the Gulf of Maine and Georges Bank which is based the presence or absence of volume backscatter above a threshold. This method is more objective than the comparison of frequency response curves because it uses an established backscatter value for the threshold. By removing all data below the threshold, only strong scattering information is retained.

In Chapter Three I analyze the distribution of the categorized acoustic regions of interest during the daytime cross shelf transects. Over all transects, plankton-like acoustic regions of interest were detected most frequently, followed by fish-like acoustic regions and then nekton-like acoustic regions. Plankton-like detections were the only significantly different acoustic detections per kilometer, although nekton-like detections were only slightly not significant. Using the threshold categorization method by Jech and Michaels (2006) provides a more conservative and discrete detection of acoustic scatterers and allows me to retrieve backscatter values along transects in areas that have been categorized. This provides continuous data values that can be integrated at discrete spatial increments for wavelet analysis. Wavelet analysis indicates significant spatial scales of interest for fish-like and nekton-like acoustic backscatter range from one to four kilometers and vary among transects.

In Chapter Four I analyze the fine scale distribution of cetaceans in the shelf break system of the Mid-Atlantic Bight using corrected sightings per trackline region, classification trees, multidimensional scaling, and random forest analysis. I describe habitat for common dolphins, Risso’s dolphins and sperm whales. From the distribution of cetacean sightings, patterns of habitat start to emerge: within the shelf break region of the Mid-Atlantic Bight, common dolphins were sighted more prevalently over the shelf while sperm whales were more frequently found in the deep waters offshore and Risso’s dolphins were most prevalent at the shelf break. Multidimensional scaling presents clear environmental separation among common dolphins and Risso’s dolphins and sperm whales. The sperm whale random forest habitat model had the lowest misclassification error (0.30) and the Risso’s dolphin random forest habitat model had the greatest misclassification error (0.37). Shallow water depth (less than 148 meters) was the primary variable selected in the classification model for common dolphin habitat. Distance to surface density fronts and surface temperature fronts were the primary variables selected in the classification models to describe Risso’s dolphin habitat and sperm whale habitat respectively. When mapped back into geographic space, these three cetacean species occupy different fine-scale habitats within the dynamic Mid-Atlantic Bight shelf break system.

In Chapter Five I present a summary of the previous chapters and present potential analytical steps to address ecological questions pertaining the dynamic shelf break region. Taken together, the results of my dissertation demonstrate the use of opportunistically collected data in ecosystem studies; emphasize the need to incorporate middle trophic level data and oceanographic features into cetacean habitat models; and emphasize the importance of developing more mechanistic understanding of dynamic ecosystems.

Elevated CO2 affects predator-prey interactions through altered performance

Recent research has shown that exposure to elevated carbon dioxide (CO2) affects how fishes perceive their environment, affecting behavioral and cognitive processes leading to increased prey mortality. However, it is unclear if increased mortality results from changes in the dynamics of predator-prey interactions or due to prey increasing activity levels. Here we demonstrate that ocean pCO2 projected to occur by 2100 significantly effects the interactions of a predator-prey pair of common reef fish: the planktivorous damselfish Pomacentrus amboinensis and the piscivorous dottyback Pseudochromis fuscus. Prey exposed to elevated CO2 (880 µatm) or a present-day control (440 µatm) interacted with similarly exposed predators in a cross-factored design. Predators had the lowest capture success when exposed to elevated CO2 and interacting with prey exposed to present-day CO2. Prey exposed to elevated CO2 had reduced escape distances and longer reaction distances compared to prey exposed to present-day CO2 conditions, but this was dependent on whether the prey was paired with a CO2 exposed predator or not. This suggests that the dynamics of predator-prey interactions under future CO2 environments will depend on the extent to which the interacting species are affected and can adapt to the adverse effects of elevated CO2.

Predator nonconsumptive effects on prey recruitment weaken with recruit density, supplementary material

We investigated the nonconsumptive effects (NCEs) of predatory dogwhelks (Nucella lapillus) on intertidal barnacle (Semibalanus balanoides) recruitment through field experiments on the Gulf of St. Lawrence coast and the Atlantic coast of Nova Scotia, Canada. We studied the recruitment seasons (May-June) of 2011 and 2013. In 2011, the Gulf coast had five times more nearshore phytoplankton (food for barnacle larvae and recruits) during the recruitment season and yielded a 58% higher barnacle recruit density than the Atlantic coast at the end of the recruitment season. In 2013, phytoplankton levels and barnacle recruit density were similar on both coasts and also lower than for the Gulf coast in 2011. Using the comparative-experimental method, the manipulation of dogwhelk presence (without allowing physical contact with prey) revealed that dogwhelk cues limited barnacle recruitment under moderate recruit densities (Atlantic 2011/2013 and Gulf 2013) but had no effect under a high recruit density (Gulf 2011). Barnacle recruits attract settling larvae through chemical cues. Thus, the highest recruit density appears to have neutralized dogwhelk effects. This study suggests that the predation risk perceived by settling larvae may decrease with increasing recruit density and that prey food supply may indirectly influence predator NCEs on prey recruitment.

The effects of the non-native invertebrate predator Bythotrephes longimanus and declining aqueous calcium on crustacean zooplankton communities in Canadian Shield lakes

Over the last several decades, human activities have resulted in environmental changes that have increased the number of stressors that can act on a single environment. In Canadian Shield lakes, two recent stressors, the invasion of Bythotrephes longimanus and calcium decline, have been documented. Widespread acidification of hundreds of North American lakes has resulted in the precipitous decline of lake water calcium concentration. Crustacean zooplankton with high calcium demands are likely to be vulnerable to calcium decline, especially <1.5 mg Ca/L, where survival and reproduction rates are reduced. These taxa are also vulnerable to predation by Bythotrephes that has been implicated in the loss of pelagic biodiversity in soft water lakes. Despite laboratory and field studies aimed at understanding the independent impact of these stressors, it is unclear how their co-occurrence will influence community response. Using a combination of data from a large regional lake survey and field experiments, I examined the individual and joint effects of Bythotrephes and calcium decline on native zooplankton community structure. Results demonstrated that much is known about Bythotrephes and our findings of reduced total zooplankton and species richness, due to the loss of Cladocera, are consistent with field surveys and other experimental studies. While we did not detect strong evidence for an effect of calcium on zooplankton using the lowest calcium concentration among invaded lakes (1.2 mg Ca/L), there is evidence that, as lake water calcium concentrations fall <1 mg Ca/L, per capita growth rates of a broad variety of taxa are expected to decline. At the regional scale, negative effects of Bythotrephes and calcium on abundances of small cladocerans and Daphnia pulicaria, respectively, were in agreement with my experimental observations. We also observed significant interactions between Bythotrephes and calcium for a broad variety of taxa. As Bythotrephes continues to spread and invade lakes that are also declining in aqueous calcium, both stressors are likely to amplify negative effects on Cladocera that appear the most vulnerable. Loss of these important zooplankton in response to both Bythotrephes and calcium decline, is likely to lower zooplankton productivity, with potential effects on phytoplankton and higher trophic levels.

Scale-dependent to scale-free: daily behavioural switching and optimized searching in a marine predator

Highlights • We study diel behavioural differences in activity patterns in bigeye tuna. • Daytime activity patterns showed scale free movements consistent with searching. • Night-time activity showed simpler movements indicative of rich patch exploitation. • The results confirm predictions of the Lévy foraging hypothesis.

Scale-dependent to scale-free: daily behavioural switching and optimized searching in a marine predator

Highlights • We study diel behavioural differences in activity patterns in bigeye tuna. • Daytime activity patterns showed scale free movements consistent with searching. • Night-time activity showed simpler movements indicative of rich patch exploitation. • The results confirm predictions of the Lévy foraging hypothesis.

Repeated, long-distance migrations by a philopatric predator targeting highly contrasting ecosystems

Long-distance movements of animals are an important driver of population spatial dynamics and determine the extent of overlap with area-focused human activities, such as fishing. Despite global concerns of declining shark populations, a major limitation in assessments of population trends or spatial management options is the lack of information on their long-term migratory behaviour. For a large marine predator, the tiger shark Galeocerdo cuvier, we show from individuals satellite-tracked for multiple years (up to 1101 days) that adult males undertake annually repeated, round-trip migrations of over 7,500 km in the northwest Atlantic. Notably, these migrations occurred between the highly disparate ecosystems of Caribbean coral reef regions in winter and high latitude oceanic areas in summer, with strong, repeated philopatry to specific overwintering insular habitat. Partial migration also occurred, with smaller, immature individuals displaying reduced migration propensity. Foraging may be a putative motivation for these oceanic migrations, with summer behaviour showing higher path tortuosity at the oceanic range extremes. The predictable migratory patterns and use of highly divergent ecosystems shown by male tiger sharks appear broadly similar to migrations seen in birds, reptiles and mammals, and highlight opportunities for dynamic spatial management and conservation measures of highly mobile sharks.

Repeated, long-distance migrations by a philopatric predator targeting highly contrasting ecosystems

Long-distance movements of animals are an important driver of population spatial dynamics and determine the extent of overlap with area-focused human activities, such as fishing. Despite global concerns of declining shark populations, a major limitation in assessments of population trends or spatial management options is the lack of information on their long-term migratory behaviour. For a large marine predator, the tiger shark Galeocerdo cuvier, we show from individuals satellite-tracked for multiple years (up to 1101 days) that adult males undertake annually repeated, round-trip migrations of over 7,500 km in the northwest Atlantic. Notably, these migrations occurred between the highly disparate ecosystems of Caribbean coral reef regions in winter and high latitude oceanic areas in summer, with strong, repeated philopatry to specific overwintering insular habitat. Partial migration also occurred, with smaller, immature individuals displaying reduced migration propensity. Foraging may be a putative motivation for these oceanic migrations, with summer behaviour showing higher path tortuosity at the oceanic range extremes. The predictable migratory patterns and use of highly divergent ecosystems shown by male tiger sharks appear broadly similar to migrations seen in birds, reptiles and mammals, and highlight opportunities for dynamic spatial management and conservation measures of highly mobile sharks.

Rabbits, stoats and the predator problem: Why a strong animal rights position need not call for human intervention to protect prey from predators

Animal rights positions face the ‘predator problem’: the suggestion that if the rights of nonhuman animals are to be protected, then we are obliged to interfere in natural ecosystems to protect prey from predators. Generally, rather than embracing this conclusion, animal ethicists have rejected it, basing this objection on a number of different arguments. This paper considers but challenges three such arguments, before defending a fourth possibility. Rejected are Peter Singer’s suggestion that interference will lead to more harm than good, Sue Donaldson and Will Kymlicka’s suggestion that respect for nonhuman sovereignty necessitates non-interference in normal circumstances, and Alasdair Cochrane’s solution based on the claim that predators cannot survive without killing prey. The possibility defended builds upon Tom Regan’s suggestion that predators, as moral patients but not moral agents, cannot violate the rights of their prey, and so the rights of the prey, while they do exist, do not call for intervention. This idea is developed by a consideration of how moral agents can be more or less responsible for a given event, and defended against criticisms offered by thinkers including Alasdair Cochrane and Dale Jamieson.