Vulnerability of an Australian anuran tadpole assemblage to the toxic eggs of the invasive cane toad (Bufo marinus)

The invasion of cane toads (Bufo marinus) across tropical Australia has fatally poisoned many native predators; the most frequent victims may be tadpoles of native frogs, which die when they consume the toxic eggs of the toads. Field studies have documented high and species‐specific mortality of tadpoles following toad spawning. To clarify the determinants of tadpole vulnerability, we conducted 1593 laboratory trials in which single tadpoles were exposed to 10 toad eggs, either with or without an alternative food source (lettuce). At least some tadpoles within all 15 species tested consumed toad eggs. Interspecific variance in survival rates (from 0 to >70%) was driven by feeding responses not by physiological tolerance to toxins: almost all native tadpoles that consumed eggs died rapidly. Tadpole mortality was decreased by the presence of an alternative food source in four species, increased in two species, and not affected in seven species. In three of four taxa where we tested both small (early‐stage) and large (late‐stage) tadpoles, both mean survival rates and the effects of alternative food on survival shifted with tadpole body size. Trials with one species (Limnodynastes convexiusculus) showed no significant inter‐clutch variation in feeding responses or tolerance to toxins. Overall, our data show that cane toad eggs are highly toxic to native anuran tadpoles, but that whether or not a tadpole is killed by encountering toad eggs depends upon a complex interaction between the native anuran's species, its body size, and whether or not alternative food was present. In nature, larval vulnerability also depends upon the seasonal timing and location of spawning events, and habitat selection and foraging patterns of the tadpoles. Our results highlight the complexity of vulnerability determinants, and identify ecological factors (rather than physiology or feeding behaviour) as the primary determinants of cane toad impact on native tadpoles.     

Behavioural responses of carnivorous marsupials (Planigale maculata) to toxic invasive cane toads (Bufo marinus)

The arrival of a toxic invasive species may impose selection on local predators to avoid consuming it. Feeding responses may be modified via evolutionary changes to behaviour, or via phenotypic plasticity (e.g. learning, taste aversion). The recent arrival of cane toads (Bufo marinus) in the Northern Territory of Australia induced rapid aversion learning in a predatory marsupial (the common planigale, Planigale maculata). Here, we examine the responses of planigales to cane toads in north‐eastern Queensland, where they have been sympatric for over 60 years, to investigate whether planigale responses to cane toads have been modified by long‐term exposure. Responses to toads were broadly similar to those documented for toad‐naïve predators. Most Queensland planigales seized (21 of 22) and partially consumed (11 of 22) the first toad they were offered, but were likely to ignore toads in subsequent trials. However, unlike their toad‐naïve conspecifics from the Northern Territory, the Queensland planigales all survived ingestion of toad tissue without overt ill effects and continued to attack toads in a substantial proportion of subsequent trials. Our data suggest that (i) learning by these small predators is sufficiently rapid and effective that selection on behaviour has been weak; and (ii) physiological tolerance to toad toxins may be higher in planigales after 60 years (approximately 60 generations) of exposure to this toxic prey.     

Predator behaviour and morphology mediates the impact of an invasive species: cane toads and death adders in Australia

The arrival of an invasive species can have severe impacts on native species. The extent of the impact, as well as the speed at which native species may mount an adaptive response, depend upon the correlation between impact and the individual phenotypes of the native species. Strong correlation between phenotype and impact within the native species raises the possibility of rapid adaptive response to the invader. Here, we examine the impact of a dangerous newly arrived prey species (the highly toxic cane toad Bufo marinus ) on naïve predators (death adders Acanthophis praelongus ) in northern Australia. During laboratory trials and field radiotracking, toads killed 48% of the adders we studied. Long-term monitoring of the population also suggests a massive decline (>89%) in recent years concurrent with the arrival of toads. Variation in snake physiology (resistance to toad toxin) had little bearing on snake survival in the field. Snake behaviour (tendency to attack toads) and morphology (body size and head size), however, were strong predictors of snake survival. Smaller snakes with relatively small heads, and snakes that were unwilling to attack toads in the laboratory, had much higher survival rates in the field. These results show that toads have a massive impact on death adder populations, but that snake phenotypes strongly mediate this impact. Thus natural selection is operating on these adder populations and an adaptive response is a possibility. If these adders can rapidly shift toad-relevant morphological and behavioural traits (either through plastic or evolved means), they will ultimately face a lowered impact from this toxic invader.     

Increased juvenile predation is not associated with evolved differences in adult brain size in Trinidadian killifish (Rivulus hartii)

Vertebrates exhibit extensive variation in brain size. The long‐standing assumption is that this variation is driven by ecologically mediated selection. Recent work has shown that an increase in predator‐induced mortality is associated with evolved increases and decreases in brain size. Thus, the manner in which predators induce shifts in brain size remains unclear. Increased predation early in life is a key driver of many adult traits, including life‐history and behavioral traits. Such results foreshadow a connection between age‐specific mortality and selection on adult brain size. Trinidadian killifish, Rivulus hartii, are found in sites with and without guppies, Poecilia reticulata. The densities of Rivulus drop dramatically in sites with guppies because guppies prey upon juvenile Rivulus. Previous work has shown that guppy predation is associated with the evolution of adult life‐history traits in Rivulus. In this study, we compared second‐generation laboratory‐born Rivulus from sites with and without guppies for differences in brain size and associated trade‐offs between brain size and other components of fitness. Despite the large amount of existing research on the importance of early‐life events on the evolution of adult traits, and the role of predation on both behavior and brain size, we did not find an association between the presence of guppies and evolutionary shifts in Rivulus brain size. Such results argue that increased rates of juvenile mortality may not alter selection on adult brain size.     

The indestructible insect: Velvet ants from across the United States avoid predation by representatives from all major tetrapod clades

Velvet ants are a group of parasitic wasps that are well known for a suite of defensive adaptations including bright coloration and a formidable sting. While these adaptations are presumed to function in antipredator defense, observations between potential predators and this group are lacking. We conducted a series of experiments to determine the risk of velvet ants to a host of potential predators including amphibians, reptiles, birds, and small mammals. Velvet ants from across the United States were tested with predator's representative of the velvet ants native range. All interactions between lizards, free‐ranging birds, and a mole resulted in the velvet ants survival, and ultimate avoidance by the predator. Two shrews did injure a velvet ant, but this occurred only after multiple failed attacks. The only predator to successfully consume a velvet ant was a single American toad (Anaxyrus americanus). These results indicate that the suite of defenses possessed by velvet ants, including aposematic coloration, stridulations, a chemical alarm signal, a hard exoskeleton, and powerful sting are effective defenses against potential predators. Female velvet ants appear to be nearly impervious to predation by many species whose diet is heavily derived of invertebrate prey.     

The impact of invasive cane toads on native wildlife in southern Australia

Commonly, invaders have different impacts in different places. The spread of cane toads (Rhinella marina: Bufonidae) has been devastating for native fauna in tropical Australia, but the toads' impact remains unstudied in temperate‐zone Australia. We surveyed habitat characteristics and fauna in campgrounds along the central eastern coast of Australia, in eight sites that have been colonized by cane toads and another eight that have not. The presence of cane toads was associated with lower faunal abundance and species richness, and a difference in species composition. Populations of three species of large lizards (land mullets Bellatorias major, eastern water dragons Intellagama lesueurii, and lace monitors Varanus varius) and a snake (red‐bellied blacksnake Pseudechis porphyriacus) were lower (by 84 to 100%) in areas with toads. The scarcity of scavenging lace monitors in toad‐invaded areas translated into a 52% decrease in rates of carrion removal (based on camera traps at bait stations) and an increase (by 61%) in numbers of brush turkeys (Alectura lathami). The invasion of cane toads through temperate‐zone Australia appears to have reduced populations of at least four anurophagous predators, facilitated other taxa, and decreased rates of scavenging. Our data identify a paradox: The impacts of cane toads are at least as devastating in southern Australia as in the tropics, yet we know far more about toad invasion in the sparsely populated wilderness areas of tropical Australia than in the densely populated southeastern seaboard.     

Size-dependent predation by snakes: selective foraging or differential prey vulnerability?

I staged replicate encounters between unrestrained lizards andsnakes in outdoor enclosures to examine size-dependent predationwithin the common garden skink (Lampropholis guichenoti). Yellow-facedwhip snakes (Demansia psammophis) forage widely for activeprey and most often consumed large skinks, whereas death adders(Acanthophis antarcticus) ambush active prey and most oftenconsumed small skinks. Small-eyed snakes (Rhinoplocephalusnigrescens) forage widely for inactive prey and consumed bothsmall and large skinks equally often. Differential predationmay reflect active choice by the predator, differential preyvulnerability, or both. To test for active choice, I presentedforaging snakes with an inert small lizard versus an inertlarge lizard. They did not actively select lizards of a particularbody size. To test for differential prey vulnerability, I quantifiedvariation between small and large lizards in behavior thatis important for determining the outcome of predator—prey interactions. Snakes did not differentiate between integumentarychemicals from small and large lizards. Large lizards tendto flee from approaching predators, thereby eliciting attackby the visually oriented whip snakes. Small lizards were moremobile than large lizards and therefore more likely to passby sedentary death adders. Additionally, small skinks were more effectively lured by this sit-and-wait species and less likelyto avoid its first capture attempt. In contrast, overnightretreat site selection (not body size) determined a lizard'schances of being detected by small-eyed snakes. Patterns ofsize-dependent predation by elapid snakes may arise not becauseof active choice but as a function of species-specific predatortactics and prey behavior.     

Ocean acidification increases the vulnerability of native oysters to predation by invasive snails

There is growing concern that global environmental change might exacerbate the ecological impacts of invasive species by increasing their per capita effects on native species. However, the mechanisms underlying such shifts in interaction strength are poorly understood. Here, we test whether ocean acidification, driven by elevated seawater pCO₂, increases the susceptibility of native Olympia oysters to predation by invasive snails. Oysters raised under elevated pCO₂ experienced a 20% increase in drilling predation. When presented alongside control oysters in a choice experiment, 48% more high-CO₂ oysters were consumed. The invasive snails were tolerant of elevated CO₂ with no change in feeding behaviour. Oysters raised under acidified conditions did not have thinner shells, but were 29–40% smaller than control oysters, and these smaller individuals were consumed at disproportionately greater rates. Reduction in prey size is a common response to environmental stress that may drive increasing per capita effects of stress-tolerant invasive predators.     

Effect of water depth on predation frequency by diving beetles on mosquito larvae prey

Diving behavior and its frequency may differ among species of mosquito larvae because of differences in predation pressure. The present study aimed to investigate the relationship between water depth and predation frequency on two mosquito species, Culex tritaeniorhynchus (wetland breeder) and Aedes albopictus (container breeder), by the diving beetle Eretes griseus. Culex tritaeniorhynchus spends more time at the surface than A. albopictus, which spends more time thrashing underwater. When intact mosquito larvae of both species were present, the diving beetles consumed almost all A. albopictus larvae (98.3%). After all the A. albopictus larvae had been consumed, the diving beetles began to prey on C. tritaeniorhynchus. In order to compare the effect of position on the predation preference of the diving beetles, equal numbers of both species were heat‐killed and allowed to settle on the bottom of the container. When all the dead mosquito larvae had sunk to the bottom of a plastic container, the diving beetles caught both mosquito species at random. These results indicate that mosquito larvae near the surface were eaten less frequently by diving beetles than those at the bottom. The low diving frequency of C. tritaeniorhynchus is regarded as a form of anti‐predatory behavior.     

Spawning site selection by feral cane toads (Bufo marinus) at an invasion front in tropical Australia

Abstract Spawning sites are a critical and often scarce resource for aquatic‐breeding amphibians, including invasive species such as the cane toad (Bufo marinus). If toads select spawning sites based on habitat characteristics, we can potentially manipulate those characteristics to either enhance or reduce their suitability as breeding sites. We surveyed 25 spawning sites used by cane toads, and 25 adjacent unused sites, in an area of tropical Australia recently invaded by these feral anurans. Water chemistry (pH, conductivity, salinity, turbidity) was virtually identical between the two sets of waterbodies, but habitat characteristics were very different. Toads selectively oviposited in shallow pools with gradual rather than steep slopes, and with open (unvegetated) gradually sloping muddy banks. They avoided flowing water, and pools with steep surrounds. In these respects, cane toads broadly resemble previously studied toad species in other parts of the world, as well as conspecifics within their natural range in South America.     

Post‐release predation on hatchery‐reared Japanese flounder Paralichthys olivaceus in the coast of Fukushima,Japan

To determine the predators of 100 mm total length hatchery‐reared juvenile Japanese flounder Paralichthys olivaceus, fishes and crabs were collected using gillnets and a small trawl net off the coast of Fukushima Prefecture, Japan. Predation on juvenile P. olivaceus by older conspecifics, the snailfish Liparis tanakai, ocellate spot skate Okamejei kenojei and the swimming crab Ovalipes punctatus, was detected based on analogical observation and molecular techniques. These predators are nocturnal feeders except for P. olivaceus. Liparis tanakai with body sizes large enough to consume juveniles only appeared in winter, whereas the large O. punctatus was abundant in early summer and in late autumn. Such seasonal variation in predator abundance indicates that the release season can be optimized for reducing predation mortality.     

Effects of density and predation risk on leaf litter processing by Phylloicus sp.

The allochthonous detritus that accumulates in the substrate of streams is used by aquatic invertebrate shredders for shelter and food. Shredders are considered rare in tropical systems, and little information is available about the role of density effects and predation risk (associated with the perception of predators by prey) in relationship to the resources used by these organisms. The aim of this study was to examine experimentally the effects of increased predation risk and of the density of Phylloicus sp. (i.e. of two types of biological relationships) on the processing of the leaf litter of Nectandra megapotamica (Spreng.) Mez. Phylloicus sp. can use leaf litter for case building and as a food resource. The density effect was measured using four treatments that differed only in the number of individuals (one, two, three or four). A second experiment with five treatments was performed to test the risk of non‐lethal predation on detritus consumption (shelter and food) by Phylloicus sp. (T1: Caddisfly; T2: Mayfly; T3: Astyanax sp./fish; T4: Damselflies; T5: Stonefly). A single Phylloicus and one other organism (a potential predator blocked with 0.5 mm fine mesh) were placed in each tank (0.002 m³ volume). We observed a negative effect of density on per capita litter consumption (experiment 1). The low density of Phylloicus may be a natural factor that decreases intraspecific competition. In the presence of fish, Phylloicus showed the lowest amount of litter processing observed in the experiment, indicating top‐down control (experiment 2). In treatments that involved the presence of invertebrates (non‐predatory and predatory), Phylloicus showed the highest amount and an intermediate amount of leaf litter processing, respectively (experiment 2). This observation also suggests that the predation effect is more probable for specific predator–prey pairs. Population density and predation risk in Phylloicus may be important factors controlling leaf litter processing.     

Abiotic and biotic influences on the dispersal behavior of metamorph cane toads (Bufo marinus) in tropical Australia

A mechanistic understanding of factors influencing the dispersal behavior of metamorph cane toads (Bufo marinus) has direct conservation relevance in Australia. These invasive anurans are toxic to native predators, and if we can predict their distribution across the landscape, we can also predict (and perhaps, manage) the scale of their impact. We propose that the major drivers of metamorph distribution are the risk of dehydration (restricting the young toads to moist substrates near pond margins) and biotic advantages to dispersal away from the pond (especially, less risk of cannibalism). To test this model, we investigated the influence of abiotic and biotic cues on the behavior of individual toads in the laboratory. Substrate moisture levels strongly influenced metamorph activity levels and habitat selection: dry substrates induced most metamorphs to remain near water. The only biotic cue to influence metamorph dispersal was proximity of a larger (cannibalistic) conspecific; a cannibal's presence at the pond margin caused most metamorphs to spend less time there, and as a consequence, to dehydrate more rapidly. Our results suggest that the spatial and temporal distribution of metamorph cane toads reflects a trade-off between competing risks: the danger of desiccation tends to keep young toads close to the pond margin in dry conditions, whereas the danger of cannibalism stimulates dispersal.     

Threat of predation alters aggressive interactions among spotted salamander (Ambystoma maculatum) larvae

Intraspecific aggression represents a major source of mortality for many animals and is often experienced alongside the threat of predation. The presence of predators can strongly influence ecological systems both directly by consuming prey and indirectly by altering prey behavior or habitat use. As such, the threat of attack by higher level predators may strongly influence agonistic interactions among conspecifics via nonconsumptive (e.g., behaviorally mediated) predator effects. We sought to investigate these interactions experimentally using larval salamanders (Ambystoma maculatum) as prey and dragonfly nymphs (Anax junius) as predators. Specifically, we quantified salamander behavioral responses to perceived predation risk (PPR) from dragonfly nymphs and determined the degree to which PPR influenced intraspecific aggression (i.e., intraspecific biting and cannibalism) among prey. This included examining the effects of predator exposure on the magnitude of intraspecific biting (i.e., extent of tail damage) and the resulting change in performance (i.e., burst swim speed). Salamander larvae responded to PPR by reducing activity and feeding, but did not increase refuge use. Predator exposure did not significantly influence overall survival; however, the pattern of survival differed among treatments. Larvae exposed to PPR experienced less tail damage from conspecifics, and maximum burst swim speed declined as tail damage became more extensive. Thus, escape ability was more strongly compromised by intraspecific aggression occurring in the absence of predation risk. We conclude that multitrophic indirect effects may importantly modulate intraspecific aggression and should be considered when evaluating the effects of intraspecific competition.     

Why ratio dependence is (still) a bad model of predation

The history of the idea that predation rates are functions of the ratio of prey density to predator density, known as ratio dependence, is reviewed and updated. When the term was introduced in 1989, it was already known that higher predator abundance often reduced an individual predator's average intake rate of prey. However, the idea that this effect was a universally applicable inverse proportionality was new. That idea was widely criticized in many articles in the early 1990s, and many of these criticisms have never been addressed. Nevertheless, ratio dependence seems to be gaining in popularity and is the subject of a recent monograph by the originators. This article revisits the most important objections to this theory, and assesses to what extent they have been answered by the theory's proponents. In this process, several new objections are raised. The counterarguments begin with the lack of a plausible, generally applicable mechanism that could produce ratio dependence. They include the fact that ratio dependence is a special case of predator‐density effects, which, in turn, are only one of many non‐prey species effects that influence the consumption rate of a particular prey. The proclaimed simplicity advantage of ratio dependence is at best small and is outweighed by its disadvantages; it predicts biologically implausible phenomena, and cannot easily be extended to describe multi‐species systems, trait‐mediated interactions, coevolution, and a number of other important ecological phenomena. Any potential small simplicity advantage disappears with corrections to remove unrealistic low‐density dynamics caused by ratio dependence. The frequent occurrence of strong predator dependence does not make ratio dependence a better ‘default’ model of predation than prey dependence, and empirical studies of the full range of non‐prey species effects on the consumption rates of predators are needed.     

Protistan predation interferes with bacterial long‐term adaptation to substrate restriction by selecting for defence morphotypes

Bacteria that are introduced into aquatic habitats face a low substrate environment interspersed with rare productive ‘hotspots’, as well as high protistan grazing. Whereas the former condition should select for growth performance, the latter should favour traits that reduce predation mortality, such as the formation of large cell aggregates. However, protected morphotypes often convey a growth disadvantage, and bacteria thus face a trade‐off between investing in growth or defence traits. We set up an evolutionary experiment with the freshwater isolate Sphingobium sp. strain Z007 that conditionally increases aggregate formation in supernatants from a predator–prey coculture. We hypothesized that low substrate levels would favour growth performance and reduce the aggregated subpopulation, but that the concomitant presence of a flagellate predator might conserve the defence trait. After 26 (1‐week) growth cycles either with (P+) or without (P?) predators, bacteria had evolved into strikingly different phenotypes. Strains from P? had low numbers of aggregates and increased growth yield, both at the original rich growth conditions and on various single carbon sources. By contrast, isolates from the P+ treatment formed elevated proportions of defence morphotypes, but exhibited lower growth yield and metabolic versatility. Moreover, the evolved strains from both treatments had lost phenotypic plasticity of aggregate formation. In summary, the (transient) residence of bacteria at oligotrophic conditions may promote a facultative oligotrophic life style, which is advantageous for survival in aquatic habitats. However, the investment in defence against predation mortality may constrain microbial adaptation to the abiotic environment.     

The behavioural response of adult Petromyzon marinus to damage‐released alarm and predator cues

Using semi‐natural enclosures, this study investigated (1) whether adult sea lamprey Petromyzon marinus show avoidance of damage‐released conspecific cues, damage‐released heterospecific cues and predator cues and (2) whether this is a general response to injured heterospecific fishes or a specific response to injured P. marinus. Ten replicate groups of 10 adult P. marinus, separated by sex, were exposed to one of the following nine stimuli: deionized water (control), extracts prepared from adult P. marinus, decayed adult P. marinus (conspecific stimuli), sympatric white sucker Catostomus commersonii, Amazon sailfin catfish Pterygoplichthys pardalis (heterospecific stimuli), 2‐phenylethylamine (PEA HCl) solution, northern water snake Nerodia sipedon washing, human saliva (predator cues) and an adult P. marinus extract and human saliva combination (a damage‐released conspecific cue and a predator cue). Adult P. marinus showed a significant avoidance response to the adult P. marinus extract as well as to C. commersonii, human saliva, PEA and the adult P. marinus extract and human saliva combination. For mobile P. marinus, the N. sipedon washing induced behaviour consistent with predator inspection. Exposure to the P. pardalis extract did not induce a significant avoidance response during the stimulus release period. Mobile adult female P. marinus showed a stronger avoidance behaviour than mobile adult male P. marinus in response to the adult P. marinus extract and the adult P. marinus extract and human saliva combination. The findings support the continued investigation of natural damage‐released alarm cue and predator‐based repellents for the behavioural manipulation of P. marinus populations in the Laurentian Great Lakes.     

Effects of prey abundance,distribution, visual contrast and morphology on selection by a pelagic piscivore

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One cost of being gold: selective predation and implications for the maintenance of the Midas cichlid colour polymorphism (Perciformes: Cichlidae)

In the colour‐polymorphic Midas cichlid fish species complex (Amphilophus citrinellus spp.), gold morphs occur at much lower frequencies (< 10%) than dark individuals. This might be surprising because gold coloration is dominant and coded for by a single Mendelian locus. Furthermore, gold individuals are considered to be competitively advantaged over dark ones because they grow faster and win aggressive encounters more often compared to dark individuals of equal size. However, one might expect a cost of being gold in terms of natural selection as a result of predation. We tested whether the Jaguar cichlid (Parachromis managuensis), a major fish predator of Midas cichlids, preys differentially on colour variants of goldfish (Carassius auratus auratus), which were used as a proxy for Midas cichlids because of their similarity in colour. Size‐matched pairs of prey fish (gold and dark) were offered to the predator and the time until the fish were attacked was recorded. The gold morph was attacked first more often (approximately 70%) but not faster than the dark morph. This suggests that the predator perceives the gold individual first, and/or that the predator exhibits a preference or higher motivation to attack the gold prey fish. The increased risk of predation of gold prey fish suggests for the Midas cichlid system that being gold may carry significant costs in terms of natural selection as a result of its major piscivorous predator. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 350–358.     

Shift in predation regime mediates diversification of foraging behaviour in a dragonfly genus

1. Behavioural adaptations to avoid and evade predators are common. Many studies have investigated population divergence in response to changes in predation regime within species, but studies exploring interspecific patterns are scant. Studies on interspecific divergence can infer common outcomes from evolutionary processes and highlight the role of environmental constraints in shaping species traits. 2. Species of the dragonfly genus Leucorrhinia underwent well‐studied shifts from habitats being dominated by predatory fish (fish lakes) to habitat being dominated by predatory invertebrates (dragonfly lakes). This change in top predators resulted in a set of adaptive trait modifications in response to the different hunting styles of both predator types: whereas predatory fish actively search and pursue prey, invertebrate predator follow a sit‐and‐wait strategy, not pursuing prey. 3. Here it is shown that the habitat shift‐related change in selection regime on larval Leucorrhinia caused species in dragonfly lakes to evolve increased larval foraging and activity, and results suggest that they lost the ability to recognise predatory fish. 4. The results of the present study highlight the impact of predators on behavioural trait diversification with habitat‐specific predation regimes selecting for distinct behavioural expression.