Invasive species shifts ontogenetic resource partitioning and microhabitat use of a threatened native amphibian

• 1. Invasive species may have direct effects on native species, such as predation or competition, as well as indirect effects such as altering habitat or the behaviour of a native species. Indirect effects can be difficult to detect, but whole‐system removal of invasive species presents an excellent opportunity for revealing these more subtle effects.
• 2. American bullfrogs were introduced to California in the late 1800s and have been implicated in the declines of native ranid species. Invasive American bullfrogs were removed from a series of 12 ponds to test for changes in microhabitat use of federally threatened California red‐legged frogs, using a neighbouring field site with six ponds as a control.
• 3. There was a marked increase in the total number of adult California red‐legged frogs seen in all of the ponds after the first year of bullfrog removal, suggesting that these adults were in the ponds, but hiding when invaders were present. Ontogenetic partitioning of habitat in this species was documented, as well as a shift in that partitioning and increased hiding behaviour with adult bullfrog presence. California red‐legged frogs used willows significantly more as cover, and were found on bare shores half as often when adult bullfrogs were present.
• 4. These results support recent suggestions that behavioural responses of prey to predators can play a substantial role in total predator effects and suggest that careful management of invasive species may be necessary to accurately evaluate population sizes of this threatened amphibian species.

Copyright © 2009 John Wiley & Sons, Ltd.     

Diet of non‐native northern snakehead (Channa argus) compared to three co‐occurring predators in the lower Potomac River,USA

Abstract – Introductions of large, non‐native, carnivorous fishes continue to occur worldwide and represent a substantial management concern to global biodiversity. One of the most recent non‐native fishes to successfully establish in North America is the northern snakehead (Channa argus), found in the lower Potomac River catchment. Dispersal of the northern snakehead throughout this system has been well documented since its original discovery in May 2004; however, little is known about the foraging habits of this species and its interactions with co‐occurring predators. Here, we quantify northern snakehead diet in comparison with the diets of naturalised largemouth bass (Micropterus salmoides), and native American eel (Anguilla rostrata) and yellow perch (Perca flavescens) collected from tidal freshwaters bordering Virginia and Maryland near Fort Belvoir, Virginia. Over 97% of northern snakehead gut contents were fishes, with fundulid and centrarchid species consumed most frequently. Dietary overlap was biologically significant only between northern snakehead and largemouth bass. Aquatic invertebrates were >10 times more common in native predator diets, reducing dietary overlap with northern snakehead. Ontogenic shifts in adult northern snakehead diet were also detected, which may be explained by optimal foraging rather than true prey specificity. Northern snakehead may be occupying a novel niche based on a piscivorous diet, therefore limiting competition with resident predators in the lower Potomac River. Further research into interactions between largemouth bass and northern snakehead is needed to inform management decisions and understand the ecological impacts of this non‐native species.     

Implications of hypoxia tolerance for wetland refugia use in Lake Nabugabo,Uganda

Aquatic hypoxia can affect predator‐prey interactions by altering the success rate of the predator and/or the vulnerability of prey. For example, in the Lake Victoria basin of East Africa, native prey exploit hypoxic wetlands as refugia from predation by introduced Nile perch (Lates niloticus). Here, it is predicted that species exploitation of wetlands depends on their hypoxia tolerance relative to the heterogeneity of wetland hypoxia. In this study, we compared the hypoxia tolerance of four fish taxa that differ in their use of hypoxic wetlands in Lake Nabugabo, Uganda: the cichlid Pseudocrenilabrus multicolor victoriae that inhabits the dense swamp interior; and three taxa that inhabit wetland ecotones including Nile tilapia (Oreochromis niloticus), L. niloticus and juvenile endemic haplochromine cichlids. We characterised hypoxia tolerance by exposing fish to progressive hypoxia and quantifying variation in aquatic surface respiration (ASR). The effect of body size on tolerance was explored in L. niloticus by quantifying ASR behaviour across a range of size classes. ASR behaviour was also compared between O. niloticus groups from wetland versus open‐water habitats to detect habitat‐associated intraspecific variation. The most tolerant taxon was the swamp specialist P. multicolor, indicated by its low ASR thresholds and small percentage of fish using ASR during the final sample interval. The other three taxa did not differ in ASR behaviour, and no differences were detected between O. niloticus groups. Body size effects were present for L. niloticus suggesting a lower tolerance to hypoxia in larger‐bodied individuals, thus limiting their ability to penetrate wetlands.     

An experimental study to evaluate predation threats on two native larval lampreys in the Columbia River Basin,USA

Experimental predation studies were conducted to evaluate and compare the predation threats of 10 species of native and non-native fishes on larvae of Pacific Lamprey, Entosphenus tridentatus, and Western Brook Lamprey, Lampetra richardsoni. The relative predatory threats were examined over four sets of binary factors, including the following: (a) short (2-day) or long (7-day) duration, (b) presence/absence of fine sediment, (c) live or dead larvae and (d) species of lampreys. Our short-term results showed a positive correlation with the sizes of predator fishes and consumed lamprey larvae. Also, most predator fishes had a significantly higher propensity to prey on lamprey larvae when sediment was absent. Conversely, this demonstrated the importance of sediment in protecting lamprey larvae from predation. Based on the predatory behaviour for live and dead larvae, predator fishes were classified into four groups using principal component analysis. Predation rates of larvae in sediment by piscivorous predators including Northern Pikeminnow Ptychocheilus oregonensis and Smallmouth Bass Micropterus dolomieu were lower and showed no differences even when the study duration was extended. In contrast, predation rates by benthic predators including White Sturgeon Acipenser transmontanus and Common Carp Cyprinus carpio, increased when we extended the study duration. This suggests that when given longer duration, benthic predators are more adept at consuming larvae within the sediment. These results provide important context for assessing the potential threat of predation on lampreys in streams, which is a key knowledge gap for lampreys.     

Non‐native rainbow trout (Oncorhynchus mykiss) occupy a different trophic niche to native Breede River redfin (Pseudobarbus burchelli) which they replace in South African headwater streams

Recent research has revealed that non‐native rainbow trout Oncorhynchus mykiss have largely replaced a native cyprinid, the Breede River redfin Pseudobarbus burchelli, as the dominant species of fish in many headwater streams in the Cape Floristic Region (CFR) of South Africa. Moreover, differences in the composition of benthic communities in CFR headwater streams with and without trout suggest that trout do not functionally compensate for the native redfin which they have replaced in these food webs. In this study, we used gut content and stable isotope analyses to characterise and compare the trophic niches and diet compositions of allopatric populations of trout and redfin in six CFR headwater streams (three containing trout, three containing redfin). Results indicate that native redfin exploit a broader trophic niche, and a more omnivorous diet, than do trout. Gut content analyses showed terrestrial invertebrates to be an important prey source for trout, which could potentially offset predation pressure on aquatic invertebrates and explain why benthic invertebrate density in streams with trout is higher than that in streams with no trout. Contrastingly, redfin diet appeared to be dominated by aquatic invertebrates, with terrestrial prey a less important food item in the guts of redfin. That redfin and trout exploit nonequivalent trophic niches may have consequences for benthic community composition in CFR headwater streams, and this study highlights the importance of quantifying how the functional role of predators changes following a predator replacement for understanding and managing the consequences of non‐native predator invasions.     

Disentangling the trophic interactions between American bullfrogs and native anurans: Complications resulting from post‐metamorphic ontogenetic niche shifts

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Effects of predator species,vegetation and prey assemblage on prey preferences of predators with emphasis on vulnerability of age‐0 common carp

Abstract Predation is an important force structuring aquatic communities, but predator–prey interactions are complex and regulated by multiple factors. Invasive fishes may interact with native fishes to alter predator–prey preferences and community dynamics. For example, common carp, Cyprinus carpio L., is an invasive species that can become abundant and negatively affect aquatic ecosystems. Juvenile common carp are occasionally found in predator diets, but predator preferences for common carp compared with alternative prey remains unknown. Prey selection and feeding behaviour of five piscivores (flathead catfish, Pylodictis olivaris (Rafinesque); largemouth bass, Micropterus salmoides (Lacepède); smallmouth bass, M. dolomieu Lacepède; walleye, Sander vitreus (Mitchill); and northern pike, Esox lucius L.) foraging on juvenile common carp and two alternative prey (fathead minnow, Pimephales promelas Rafinesque, and yellow perch, Perca flavescens Mitchill) at variable densities and habitats were evaluated. Common carp and fathead minnow were generally selected for or neutrally selected across predator species, habitat types and prey assemblages. By contrast, yellow perch was generally selected against. Common carp were easily captured but difficult to manipulate and ingest compared with other prey. These results reveal that common carp are vulnerable to a variety of predators, suggesting control of this detrimental invader may be possible through biomanipulation.     

Trophic structure of a pond community dominated by an invasive alien species: Insights from stomach content and stable isotope analyses

1. Invaders affect native species across multiple trophic levels, influencing the structure and stability of freshwater communities. Based on the ‘trophic position hypothesis’, invaders at the top of the food web are more harmful to native species via direct and indirect effects than trophically analogous native predators are.
2. However, introduced and native predators can coexist, especially when non-native species have no ecological and behavioural similarities with natives, occupy an empty niche, or natives show generalist anti-predator strategies that are effective at the community level.
3. At present, conservation efforts are focused on eradicating invaders; however, their removal may lead to unwanted and unexpected outcomes, especially when invaders are well established and strongly interspersed with natives. This highlights the need to consider invaders in a whole-ecosystem context and to consider the evolutionary history and behavioural ecology of natives and invaders before active management is applied.
4. Here, stomach content and stable isotope analyses were combined to investigate a pond system dominated by invaders in order to understand the effects of the interactions among upper level predators and lower level members of the food web on the whole community structure.
5. Both diet and isotope analyses showed that several invaders contributed to the diet of natives and invaders. A significant isotope overlap was found among upper level predators. However, stomach content analysis suggested that predators reduced the potential competition differentiating the food spectrum by including additional prey in their diet. Both native and non-native upper level predators, by preying on invaders, seem not to exert a strong suppressive effect through predation and competition on native species.
6. This research confirms the importance of studying food webs to identify ecological conditions that forecast the potential for deleterious impacts before management is applied. In cases where invaders cannot be eradicated, management efforts should follow a conciliatory approach promoting the coexistence of native species with invaders.

     

Multispecies functional responses reveal reduced predation at high prey densities and varied responses among and within trophic groups

Understanding predator–prey interactions is critical for marine fisheries and ecosystem management as they shape community structure, regulate prey populations and present energy demands critical for community sustainability. We examined multispecies functional responses of 17 fishes (48 predator‐size combinations) spanning piscivores, planktivores and benthivores for the northeast US continental shelf. Similar to previous work, linear relationships between predation and prey density (Holling type I response) were not supported, since model estimates of handling time were greater than zero for the prey considered. Instead, a clear majority of the predators sampled were Holling type III feeders (sigmoidal; prey switching or learning). For piscivores, nearly all responses were Holling type III with the exception of one being Holling type II (hyperbolic; satiation). Planktivores and benthivores exhibited a combination of type IV (feeding confusion at high prey density) and Holling type III responses. The relationships were predator‐ and prey‐dependent, which is counter to assumptions that are often made of trophic groups. Decreased predation at high prey densities (type IV response) present among planktivores and benthivores suggests an overestimation of predation can occur if ignored. This contrasts with fish and squid prey which primarily invoked a Holling type III response. Functional responses are key to modelling trophic interactions for multispecies and ecosystem models. By refining these inputs in a multispecies context with empirical data, we can advance our understanding of whole‐shelf ecology and improve decision‐making tools for resource management.     

Predation on wild and hatchery salmon by non‐native brown trout (Salmo trutta) in the Trinity River,California

Non‐native predators may interfere with conservation efforts for native species. For example, fisheries managers have recently become concerned that non‐native brown trout may impede efforts to restore native salmon and trout in California's Trinity River. However, the extent of brown trout predation on these species is unknown. We quantified brown trout predation on wild and hatchery‐produced salmon and trout in the Trinity River in 2015. We first estimated the total biomass of prey consumed annually by brown trout using a bioenergetics model and measurements of brown trout growth and abundance over a 64‐km study reach. Then, we used stable isotope analysis and gastric lavage to allocate total consumption to specific prey taxa. Although hatchery‐produced fish are primarily released in the spring, hatchery fish accounted for most of the annual consumption by large, piscivorous brown trout (>40 cm long). In all, the 1579 (95% CI 1,279–1,878) brown trout >20 cm long in the study reach ate 5,930 kg (95% CI 3,800–8,805 kg) of hatchery fish in 2015. Brown trout predation on hatchery fish was ca. 7% of the total biomass released from the hatchery. Brown trout only ate 924 kg (95% CI 60–3,526 kg) of wild fish in 2015, but this was potentially a large proportion of wild salmon production because wild fish were relatively small. As large brown trout rely heavily on hatchery‐produced fish, modifying hatchery practices to minimise predation may enhance survival of hatchery fish and potentially reduce the abundance of predatory brown trout.     

Could native predators help to control invasive fishes? Microcosm experiments with the Neotropical characid,Brycon orbignyanus

Abstract –  The potential of the native characid, Brycon orbignyanus , to help to control some invasive fish species currently present in the Paraná River basin was addressed through microcosm experiments. Juveniles of three invasive ( Cichla piquiti , Oreochromis niloticus and Ictalurus punctatus ) and two native ( Astyanax altiparanae and Prochilodus lineatus ) fish species were offered as prey to B. orbignyanus in 300-l aquarium trials with three habitat complexity treatments (0%, 50% and 100% structure). Prey survival was much more variable among species ( I. punctatus  <  C. piquiti  <  O. niloticus ∼ P. lineatus ∼ A. altiparanae ) than through time, and B. orbignyanus predation was clearly mediated by habitat complexity, with lower prey survival in low-complexity treatments. The lower survival observed for C. piquiti could be partially explained by its less active behaviour and its preference for a surface microhabitat and less structured areas. Prey size also affected predation rates, as for the three less consumed species the largest individuals were significantly preyed on. Our results suggest that preserving and restoring the populations of B. orbignyanus might help to control some fish species introduced to the Paraná River basin, particularly I. punctatus and C. piquiti .     

Piscivory in larval perch (Perca fluviatilis): mechanisms structuring larval roach (Rutilus rutilus) cohorts

Abstract – Perch ( Perca fluviatilis ) can act as a piscivore from larval stage VI (body size 10.3 mm) on newly hatched larval roach ( Rutilus rutilus ), bream ( Abramis brama ) and smaller siblings of its own cohort. Consumption rates at this stage were approx. 0.5 prey/perch*h at 21°C. Larval perch predation was strongly gap-limited, and the maximum size of roach consumed by perch (perch length interval 10.3–62.0 mm) under experimental conditions followed the linear regression, P_prey-max.=0.478*L_Pred.+1.829 ( r ²=0.99, P <0.001, n =12). Under experimental conditions, predatory 0⁺ perch substantially affected the size distributions of 0⁺ roach prey cohorts, since smaller prey individuals were predated more frequently than larger ones. In both unimodal and bimodal size distributions of prey roach, the distributions changed according to the maximum prey size consumed by the added predatory perch. Unimodal prey distributions were positively skewed when piscivorous perch were added compared with controls without predators. According to the size distributions of lake-living 0⁺ roach and 0⁺ perch and the relative size difference between prey and predator, the vulnerability of 0⁺ roach cohort to 0⁺ perch predation changed from June to September. Prey vulnerability was extremely sensitive to the relative size difference between predator and prey. Therefore differences in hatching time and growth rates between the two species will strongly influence the potential for predator-prey interactions. ^Note     

Variability and stability in predation landscapes: A cross‐ecosystem comparison on the potential for predator control in temperate marine ecosystems

Predation can play an important role in population, community and ecosystem processes. When predator guilds are diverse, fluctuations in individual predator populations may have small influences on the guild at large, suggesting that predator diversity stabilizes the amount of predation prey experience. The strength of this phenomenon depends on how synchronously populations within predator assemblages vary and whether all predators are equally important consumers. We utilized a database of biomasses of fish species across ten temperate marine ecosystems paired with diet composition and feeding rate information from mass‐balance food web models to develop a predation index that weights the importance of predators on a prey based on predator feeding habits. Using the index, we asked how diverse sources of predation in these ecosystems are and how much diversity stabilizes variability in predation. Predator assemblages displayed a wide range of diversity; in one‐third of assemblages, a single predator group accounted for over half of all predation. Abundances of predator populations within assemblages generally varied independently of one another (neither synchronously nor asynchronously), implying an intermediate stabilization on predation intensity by predator diversity. Accounting for interaction strength (versus mere presence) is critical for interpreting the predator landscape; doing so led to a wider range in predator assemblage diversity and less synchronous assemblages. This work challenges conventional notions that marine food webs are diverse and therefore less susceptible to predator control. Future work should consider the temporal variability of the predator assemblages and account for differences in mortality induced by each predator population.     

Interactions between Unionida and non‐native species: A global meta‐analysis

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Foraging arena theory

There is a critical need for quantitative models that can help evaluate trade‐off decisions related to the impacts of harvesting and protection of aquatic ecosystems within an ecosystem context. Ecosystem models used to evaluate such trade‐offs need to have the capability of capturing the dynamic stability that can arise when predator‐prey interactions are restricted to spatial and temporal arenas. Foraging arenas appear common in aquatic systems and are created by a wide range of mechanisms, ranging from restrictions of predator distributions in response to predation risk caused by their own predators, to risk‐sensitive foraging behaviour by their prey. Foraging arenas partition the prey in each predator‐prey interaction in a food web into vulnerable and invulnerable states, with exchange between these states potentially limiting overall trophic flow. Inclusion of vulnerability exchange processes in models for recruitment processes and food web responses to disturbances like harvesting leads to very different predictions about dynamic stability, trophic cascades and maintenance of ecological diversity than do models based on large‐scale mass action (random mixing) interactions between prey and predators. Although a number of methods to estimate these critical exchange rates are presented, none are considered fully satisfactory. The most important challenge for the practical application of models that incorporate foraging arena theory today is not only developing new or improved methods for measuring exchange rates but also evaluating how such rates vary in responses to major fishery‐induced changes in abundances of predators.     

Modelling spatial exclusion of a vulnerable native fish by introduced trout in rivers using landscape features: a new tool for conservation management

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Effects of simulated light intensity,habitat complexity and forage type on predator–prey interactions in walleye Sander vitreus

Predator‐prey interactions can be influenced by the behaviour of individual species as well as environmental factors. We conducted laboratory experiments to test for the influences of two abiotic factors (light intensity and habitat complexity) on predator–prey interactions between walleye Sander vitreus and two prey species, bluegill Lepomis macrochirus and golden shiner Notemigonus crysoleucas. Three light intensities were simulated (day, twilight and night) in the presence or absence of simulated vegetation. Observations of predator behaviour indicated that walleye increased activity and foraging success with decreasing light levels and had most success capturing dispersed, closer prey. While schooling could not be maintained as light levels diminished, prey decreased predation vulnerability by moving into vegetation or higher in the water column. Throughout all treatments, bluegill were more evasive to capture as the number of strikes was similar on both prey but capture rates were higher for golden shiner. Although light intensity and simulated habitat complexity affected predator and prey behaviour, these factors did not interact to influence foraging success of walleye. To fully understand predator and prey behaviours in fishes, an understanding of species‐specific responses to abiotic and biotic factors is necessary.     

Predation on native fish eggs by invasive round goby revealed by species‐specific gut content DNA analyses

1. Conservation of riverine fish often aims to improve access to spawning grounds and restore longitudinal connectivity by removing migration barriers, and involves substantial investments. However, these investments also enable non‐native predators to invade upstream into spawning areas and potentially adversely affect the recruitment of threatened freshwater fish through egg or fry predation.
2. Detecting egg predation is often challenging. Visual inspections of fish gut contents may underestimate predation of soft materials such as eggs and fry, which limits the discovery of predators preying upon these life‐stages. DNA‐based detection assays may offer a more sensitive tool to assess predation of soft materials.
3. A conservation issue was confirmed by developing and applying a species‐specific DNA‐based detection assay: invasive round goby (Neogobius melanostomus) prey on the eggs or fry of the threatened common nase (Chondrostoma nasus) in Switzerland.
4. DNA‐based detection assays were also developed for five other valuable native fish species, including endangered salmonid and cyprinid river spawners. The applicability of the assays was confirmed in a series of laboratory and field feeding experiments involving eggs and fish tissue. In addition, this work provides a guiding framework for conservation managers regarding the use and applicability of different DNA‐based detection approaches for gut content analysis.
5. The results of this study could inform local conservation measures – such as temporary reductions in the density of round goby at spawning sites prior to spawning – and demonstrate how targeted application of species‐specific molecular markers may advance freshwater fish management.

     

Turbidity‐induced changes in emergent effects of multiple predators with different foraging strategies

Abstract – In natural systems, prey frequently interact with multiple predators and the outcome often cannot be predicted by summing the effects of individual predator species. Multiple predator interactions can create emergent effects for prey, but how those change across environmental gradients is poorly understood. Turbidity is an environmental factor in aquatic systems that may influence multiple predator effects on prey. Interactions between a cruising predator (largemouth bass Micropterus salmoides) and an ambush predator (muskellunge Esox masquinongy) and their combination foraging on a shared prey (bluegill Lepomis macrochirus) were examined across a turbidity gradient. Turbidity modified multiple predator effects on prey. In clear water, combined predators consumed in total more prey than expected from individual predator treatments, suggesting risk enhancement for prey. In moderately turbid water, the predators consumed fewer prey together than expected, suggesting a risk reduction for prey. At high turbidity, there were no apparent emergent effects; however, the cruising predator consumed more prey than the ambush predator, suggesting an advantage for this predator. Understanding multiple predator traits across a gradient of turbidity increases our understanding of how complex natural systems function.     

Foraging behaviour of juvenile pink salmon (Oncorhynchus gorbuscha) and size‐dependent predation risk

Two hypotheses related to effects of juvenile pink salmon (Oncorhynchus gorbuscha) foraging behaviour and size on their predation risk were evaluated using field data collected in Prince William Sound, Alaska 1 995–97. My results supported the hypothesis that low macrozooplankton density leads to dispersion of juvenile salmon from shallow nearshore habitats and greater predation risk, but zooplankton type was an important factor. When the biomass of large copepods (primarily Neocalanus spp.) declined, salmon dispersed from shallow nearshore habitats, and mean daily individual predator consumption of salmon increased by a factor of 5. A concomitant five‐fold increase in the probability of occurrence of salmon in predator stomachs supported the notion that increased predation on salmon was caused by a greater overlap between predator and prey when salmon dispersed offshore, not an increase in the number of salmon consumed per feeding bout. The results also generally supported the hypothesis that the timing of predation events modifies the nature of size‐dependent predation losses of salmon to different predator groups (small and large planktivores and piscivores). Size‐dependent vulnerabilities of salmon to predators were a function of both predator and prey sizes. When simulated predation was shifted from May to June, the vulnerability of salmon became more dependent on their growth than initial size. But, the size‐ and growth‐dependent vulnerabilities of salmon differed more among predator groups than between May and June, suggesting that changes in the composition of predator fields could more strongly affect the nature of size‐dependent predation than changes in the timing of predation losses.