Introduced Goldfish Affect Amphibians through Inhibition of Sexual Behaviour in Risky Habitats: an Experimental Approach

The introduction of alien species is one of the major causes of current and global biodiversity loss. The introduction of fish can be a particular threat to native amphibian populations, which are declining worldwide. One way for amphibians to persist in such altered environments is to adopt anti-predator strategies especially at the behavioural level. However, although it has been shown that avoidance behaviour may decrease the probability of being detected by a potential predator, little is known on the consequences on sexual behaviour. In this study, we tested the hypothesis that adult Alpine newts (Ichthyosaura alpestris) use shelters more often and exhibit less sexual activity in the presence of goldfish (Carassius auratus) and that they reduce sexual activity more in risky micro-habitats than in safe environments. To this end, we assessed behavioural patterns of adult newts in a replicated laboratory design. Goldfish were present in direct contact with newts in half of the tanks. Consistently throughout the study period, significantly more newts used shelter in the presence of fish than in their absence. Newts also significantly decreased their sexual activity level overall, but specially outside the shelter when they were in direct contact with fish. These results show that fish presence can affect newts in complex ways, such as through inhibition of their reproduction. Our work highlights that integrating behaviour in conservation studies is essential to understanding the patterns of coexistence and exclusion between introduced fish and amphibians.     

Positive indirect effects of top-predators on the behaviour and survival of juvenile fishes

Top-predators can suppress mesopredator behaviour through risk effects. However, there is limited understanding of whether such behavioural suppression can dampen the lethal and sub-lethal effects of mesopredators on bottom level prey. Here, we document a field experiment that examines whether the presence of top-predator cues (visual and chemical stimuli from a coral trout) can cascade to indirectly influence the behaviour and survival of juvenile fish prey of different species (Pomacentrus amboinensis and P. chrysurus) and size (small = 1.18 cm SL versus large = 1.32 cm SL). Results showed that habitat patches exposed to top-predator cues received fewer visits and foraging attacks from mesopredators, leading to higher space use (~ 46%), feeding rate (~ 95%) and survival (~ 67%) from juvenile fish prey. Survival was always higher for individuals of P. amboinensis and of large-size, independent of the presence or absence of top-predator cues. Our data indicate that predation risk from the top-predator indirectly favoured the persistence and behaviour of juvenile fishes by promoting risk-averse behavioural responses in mesopredators. This study underscores the behavioural mechanisms by which risk effects can cascade through the food web and highlights the consequences that harvesting top-predators may have on the replenishment of bottom prey populations.     

Celestial orientation in the marbled newt (Triturus marmoratus)

Orientation toward breeding ponds plays an important role in the seasonal movements of amphibians. In this study, adult marbled newts were tested in a circular arena to determine sensory cues used to locate breeding ponds. Animals were collected from a temporary pond situated in northern Spain, taken to the experimental site 340 m distant, and tested for orientation under a variety of conditions (i.e., orientation under a clear night sky, orientation under an overcast night sky, and orientation under a clear night sky in the presence of an altered geomagnetic field). These investigations have demonstrated that the marbled newt is able to orient using celestial cues. Animals chose a compass course in the direction of their breeding pond only when celestial cues were available. Conversely, the ambient geomagnetic field does not seem to be relevant to orientation of marbled newts since they were unable to orient themselves using the ambient geomagnetic field in the absence of celestial cues. Electronic Publication     

Competitive and predatory interactions between invasive mosquitofish and native larval newts

Invasive fish have a high disruptive potential in aquatic ecosystems, in which amphibians may be highly impacted due to intense competition and/or predation on their eggs and larvae. Most studies have focused on the effect of large invasive fishes such as salmonids, whereas the effect of smaller fish on amphibians has been seldom investigated. We experimentally studied effects of the invasive Eastern mosquitofish (Gambusia holbrooki) on pygmy newts (Triturus pygmaeus), a species endemic to the Iberian Peninsula. We set up outdoor mesocosms in Doñana National Park with native aquatic flora and invertebrate fauna, and containing larval newts at two experimental densities. Density of larval newts was also crossed with presence or absence of mosquitofish, either free-swimming or caged, in order to distinguish consumptive and non-consumptive effects. Increased density of coexisting larval newts did not reduce their survival, but reduced their growth and development. Newt survival and size at metamorphosis were dramatically reduced in the presence of free-swimming mosquitofish, whether at low or high fish densities. Caged mosquitofish, however, had no effect on larval newts. In laboratory trials, mosquitofish preyed more efficiently on insect larvae than did larval pygmy newts, highlighting the high competitive potential of mosquitofish. This was confirmed by the depletion of zooplankton that free fish caused in the experimental outdoor mesocosms. Our study suggests that invasive mosquitofish exert a high negative impact on coexisting newt populations. Such effects can be explained by a combination of direct predation, injuries caused by predation attempts, and intense competitive exploitation of common food resources.     

Chemical defense of the eastern newt (Notophthalmus viridescens): variation in efficiency against different consumers and in different habitats

Amphibian secondary metabolites are well known chemically, but their ecological functions are poorly understood--even for well-studied species. For example, the eastern newt (Notophthalmus viridescens) is a well known secretor of tetrodotoxin (TTX), with this compound hypothesized to facilitate this salamander's coexistence with a variety of aquatic consumers across the eastern United States. However, this assumption of chemical defense is primarily based on observational data with low replication against only a few predator types. Therefore, we tested the hypothesis that N. viridescens is chemically defended against co-occurring fishes, invertebrates, and amphibian generalist predators and that this defense confers high survivorship when newts are transplanted into both fish-containing and fishless habitats. We found that adult eastern newts were unpalatable to predatory fishes (Micropterus salmoides, Lepomis macrochirus) and a crayfish (Procambarus clarkii), but were readily consumed by bullfrogs (Lithobates catesbeianus). The eggs and neonate larvae were also unpalatable to fish (L. macrochirus). Bioassay-guided fractionation confirmed that deterrence is chemical and that ecologically relevant concentrations of TTX would deter feeding. Despite predatory fishes rejecting eastern newts in laboratory assays, field experiments demonstrated that tethered newts suffered high rates of predation in fish-containing ponds. We suggest that this may be due to predation by amphibians (frogs) and reptiles (turtles) that co-occur with fishes rather than from fishes directly. Fishes suppress invertebrate consumers that prey on bullfrog larvae, leading to higher bullfrog densities in fish containing ponds and thus considerable consumption of newts due to bullfrog tolerance of newt chemical defenses. Amphibian chemical defenses, and consumer responses to them, may be more complex and indirect than previously appreciated.     

Habitat degradation disrupts neophobia in juvenile coral reef fish

Habitat degradation not only disrupts habitat‐forming species, but alters the sensory landscape within which most species must balance behavioural activities against predation risk. Rapidly developing a cautious behavioural phenotype, a condition known as neophobia, is advantageous when entering a novel risky habitat. Many aquatic organisms rely on damage‐released conspecific cues (i.e. alarm cues) as an indicator of impending danger and use them to assess general risk and develop neophobia. This study tested whether settlement‐stage damselfish associated with degraded coral reef habitats were able to use alarm cues as an indicator of risk and, in turn, develop a neophobic response at the end of their larval phase. Our results indicate that fish in live coral habitats that were exposed to alarm cues developed neophobia, and, in situ, were found to be more cautious, more closely associated with their coral shelters and survived four‐times better than non‐neophobic control fish. In contrast, fish that settled onto degraded coral habitats did not exhibit neophobia and consequently suffered much greater mortality on the reef, regardless of their history of exposure to alarm cues. Our results show that habitat degradation alters the efficacy of alarm cues with phenotypic and survival consequences for newly settled recruits.     

Use of a Magnetic Compass for Nocturnal Homing Orientation in the Palmate Newt, Lissotriton helveticus

Previous studies have shown that migrating palmate newts (Lissotriton helveticus) can rely on acoustic cues for orientation to breeding ponds. Nonetheless, although acoustic cues are reliable over relatively short distances, they are unlikely to account for the long‐distance homing demonstrated in several other species of newts. Most individuals of L. helveticus migrate only a few hundred meters (Diego‐Rasilla, F. J. & Luengo, R. M. 2007: Acoustic orientation in the palmate newt, Lissotriton helveticus. Behav. Ecol. Sociobiol. 61, 1329—1335), raising the possibility that this species may only utilize short‐distance cues (Joly, P. & Miaud, C. 1993: How does a newt find its pond? The role of chemical cues in migrating newts (Triturus alpestris). Ethol. Ecol. Evol. 5, 447—455; Russell, A. P., Bauer, A. M. & Johnson, M. K. 2005: Migration of amphibians and reptiles: an overview of patterns and orientation mechanisms in relation to life history strategies. In: Migration of Organisms (Elewa, M. T., ed). Springer‐Verlag, Berlin Heidelberg, pp. 151—203; Sinsch, U. 2006: Orientation and navigation in Amphibia. Mar. Freshw. Behav. Phy. 39, 65—71). Therefore, experiments were carried out to investigate the use of the geomagnetic field in the nocturnal homing orientation of L. helveticus. Tests were carried out at night in an outdoor circular arena, under total overcast sky that prevented access to celestial compass cues. Individual newts were tested in one of four symmetrical alignments of an earth‐strength magnetic field. We studied the orientation behaviour of newts from two breeding ponds located 9.05 km west‐southwest and 19 km east‐northeast of the testing site. The distribution of magnetic bearings from both groups of newts exhibited significant orientation in the homeward direction. These findings indicate that palmate newts are capable of long‐distance homing and are able to orient in the homeward direction at night using the magnetic compass as the sole source of directional (i.e., compass) information.     

Expression of sexual ornaments in a polymorphic species: phenotypic variation in response to environmental risk

Secondary sexual traits may evolve under the antagonistic context of sexual and natural selection. In some polymorphic species, these traits are only expressed during the breeding period and are differently expressed in alternative phenotypes. However, it is unknown whether such phenotypes exhibit phenotypic plasticity of seasonal ornamentations in response to environmental pressures such as in the presence of fish (predation risk). This is an important question to understand the evolution of polyphenisms. We used facultative paedomorphosis in newts as a model system because it involves the coexistence of paedomorphs that retain gills in the adult stage with metamorphs that have undergone metamorphosis, but also because newts exhibit seasonal sexual traits. Our aim was therefore to determine the influence of fish on the development of seasonal ornamentation in the two phenotypes of the palmate newt (Lissotriton helveticus). During the entire newt breeding period, we assessed the importance of phenotype and fish presence with an information‐theoretic approach. Our results showed that paedomorphs presented much less developed ornamentation than metamorphs and those ornamentations varied over time. Fish inhibited the development of sexual traits but differently between phenotypes: in contrast to metamorphs, paedomorphs lack the phenotypic plasticity of sexual traits to environmental risk. This study points out that internal and external parameters act in complex ways in the expression of seasonal sexual ornamentations and that similar environmental pressure can induce a contrasted evolution in alternative phenotypes.     

Influence of shelters and food resources on smoltification of juveniles of the Atlantic salmon <Emphasis Type="Italic">Salmo salar</Emphasis>

Influence of feeding conditions and of the presence of a various number of shelters in basins on development of differentiation of juveniles of Salmo salar at the age 1+ and formation of smolts were studied under experimental conditions. The experiments had been carried out on groups of ten fish. The influence of investigated factors turned out to be significant. Under normal feeding four times a day, the quantity of formed smolts depends on the number of shelters: the more shelters that are available, the fewer smolts appear in groups. The presence of one shelter is a strong stimulant enhancing aggressive activity towards conspecific individuals, resulting in destruction of some fish in the group. Under feeding once a day, i.e., under food shortage, more fish perished, and the number of smolts decreased as the fish did not accumulate a sufficient energy potential for the morphophysiological transformation. One of the potential mechanisms of development of differentiation of fish juveniles into parrs and future smolts is discussed, based on domination of some fish possessing the individual territory and exclusion of subdominant specimens into open water as a result of social interaction.     

Behavioural Correlations May Cause Partial Support for the Risk Allocation Hypothesis in Damselfly Larvae

Prey animals are often confronted with situations that differ in predation risk. According to the risk allocation hypothesis, prey animals should adaptively allocate antipredator behaviour in accordance with the magnitude and frequency of those risk situations. According to the first prediction prey animals should increase foraging in the safe situations and decrease foraging in the dangerous situations as these situations become relatively more dangerous. The second prediction is that with increased time spent in the dangerous situations, progressively more foraging effort is shown in both the dangerous and safe situations, especially in the safer ones. Prey animals may, however, show maladaptive behaviour due to behavioural correlations across risk situations. Here we test for the first time both predictions generated by the risk allocation hypothesis while considering behavioural correlations. We reared larvae of the damselfly Ischnura elegans, from the egg stage, under five rearing risk conditions: (i) in isolation, (ii) in the presence of conspecific larvae, (iii) in the presence of one fish, (iv) in the presence of two fish, and (v) in the presence of two fish for 50% of the time. For each rearing risk condition, we scored their behaviour in the absence and in the presence of fish. In accordance with the first prediction, in the absence of a predator, larvae reared under increasing risk conditions increased their level of foraging. In accordance with the second prediction, in the absence of a predator, larvae that were more frequently exposed to fish during rearing, increased foraging. However, opposite to the predictions from the risk allocation hypothesis, foraging increased both with increasing rearing risk, and with increased predator exposure frequency. The observed positive behavioural correlation of foraging activity across test situations with and without fish, may generate the combination of adaptive patterns in the absence of fish and the maladaptive patterns in the presence of fish. Former studies of the risk allocation hypothesis also found, at best, mixed support, and we hypothesize that behavioural correlations across risk situations, if present, will likely cause partial deviations from model predictions.     

Contestable shelters provoke aggression among 0+ perch, <Emphasis Type="BoldItalic">Perca fluviatilis</Emphasis>

Synopsis We examined behavioural interactions and feeding within triads of young-of-the-year (YOY) Eurasian perch, Perca fluviatilis, in aquaria with and without a shelter. For the first time we showed that competition for shelters, but not for food, provokes aggressiveness and triggers establishment of social hierarchy among young perch. No aggressiveness occurred during feeding bouts, when food was a limited resource. We expect the observed interactions to occur in natural heterogeneous habitats providing limited number of refuges and high local density of fish. They may ultimately lead to previously anticipated interference competition among juvenile perch.     

The Use of Conspecific Chemical Cues for Cannibal Avoidance in California Newts (Taricha torosa)

Adult California newts, Taricha torosa (Caudata: Salamandridae), prey on both conspecific egg masses and larvae. We used both laboratory and field experiments to determine if newt larvae use conspecific chemical cues to avoid adult intraspecific predators. Larvae showed significant hiding responses when exposed to adult cues in both the field and the laboratory. Larvae did not exhibit significant hiding responses to chemical cues from invertebrate predators.     

Field verification of the use of chemical alarm cues in a coral reef fish

Chemical alarm cues function as early indicators of a predation threat and influence the outcome of predator–prey interactions in the favour of the prey animal. The tropical goby, Asterropteryx semipunctatus, responded with a stereotypical alarm response, including reduced movement and feeding, following exposure to water that contained chemical cues from injured conspecifics under natural field conditions. Gobies did not exhibit an alarm response when challenged with extracts from damaged fish from a different taxonomic family. The behavioural response in the field was similar to that observed in laboratory experiments. This study verifies the use of chemical alarm cues in a marine fish in their natural environment.     

Hunger‐dependent and sex‐specific antipredator behaviour of larvae of a size‐dimorphic mosquito

1. Modification of behaviours in the presence of predators or predation cues is widespread among animals. The costs of a behavioural change in the presence of predators or predation cues depend on fitness effects of lost feeding opportunities and, especially when organisms are sexually dimorphic in size or timing of maturation, these costs are expected to differ between the sexes. 2. Larval Aedes triseriatus (Say) (Diptera: Culicidae) were used to test the hypothesis that behavioural responses of the sexes to predation cues have been selected differently due to different energy demands. 3. Even in the absence of water‐borne predation cues, hungry females (the larger sex) spent more time browsing than did males, indicating a difference in energy needs. 4. In the presence of predation cues, well‐fed larvae of both sexes reduced their activity more than did hungry larvae, and males shifted away from high‐risk behaviours to a greater degree than did females, providing the first evidence of sex‐specific antipredator behaviour in foraging mosquito larvae. 5. Because sexual size dimorphism is common across taxa, and energetic demands are probably correlated with size dimorphism, this research demonstrates the importance of investigating sex‐specific behaviour and behavioural responses to enemies, and cautions against generalising results between sexes.     

Trait‐mediated effects of predation across life‐history stages in container mosquitoes

1. It was determined if the predatory midge Corethrella appendiculata Grabham imposes a fitness cost in a native mosquito, Ochlerotatus triseriatus Say, and an invasive mosquito, Aedes albopictus Skuse. The hypothesis that decreased activity of immature prey in the presence of predator cues is associated with life history costs through all life cycle stages was tested. 2. In experiment 1, individual larvae of O. triseriatus or A. albopictus were raised in the presence or absence of predation cues at two resource levels. Prey were video recorded to detect behavioural responses and to measure development time, size at emergence, and adult longevity. In experiment 2, prey populations were reared in similar environments and the frequency of predator cue additions was varied. 3. Only O. triseriatus reduced its activity in the presence of predation cues. Predation cues were associated with longer immature development times and shorter adult life spans in O. triseriatus, whereas in A. albopictus, the cues were associated with a larger size of emerging adults. 4. In the present study, it was found that behavioural modifications during the larval stage can affect mosquitoes through multiple stages of their complex life cycle. The species‐specific behavioural differences are probably attributable to the longer evolutionary history O. triseriatus has with predators, relative to the invasive A. albopictus.     

Sensory cues of a top‐predator indirectly control a reef fish mesopredator

Behavioural trophic cascades highlight the importance of indirect/risk effects in the maintenance of healthy trophic‐level links in complex ecosystems. However, there is limited understanding on how the loss of indirect top–down control can cascade through the food‐web to modify lower level predator–prey interactions. Using a reef fish food‐web, our study examines behavioural interactions among predators to assess how fear elicited by top‐predator cues (visual and chemical stimuli) can alter mesopredator behaviour and modify their interaction with resource prey. Under experimental conditions, the presence of any cue (visual, chemical, or both) from the top‐predator (coral trout Plectropomus leopardus) strongly restricted the distance swum, area explored and foraging activity of the mesopredator (dottyback Pseudochromis fuscus), while indirectly triggering a behavioural release of the resource prey (recruits of the damselfish Pomacentrus chrysurus). Interestingly, the presence of a large non‐predator species (thicklip wrasse Hemigymnus melapterus) also mediated the impact of the mesopredator on prey, as it provoked mesopredators to engage in an ‘inspection’ behaviour, while significantly reducing their feeding activity. Our study describes for the first time a three‐level behavioural cascade of coral reef fish and stresses the importance of indirect interactions in marine food‐webs.     

Some Consequences of Size Variability in Juvenile Prickly Sculpin, Cottus asper

Variation in size among fishes can have important ecological consequences. The origin and persistence of variation in size among a cohort of juvenile prickly sculpin, Cottus asper, was explored experimentally by manipulating the size variability in juvenile fish and the presence of conspecific adult fishes in a factorial design. I found that adult fish significantly suppressed the growth and survivorship of juveniles, while the variance treatment alone had no effect on growth or survivorship. The presence of adults was also associated with a decrease in size variability in the high variance treatment. An analysis of juvenile growth patterns revealed no evidence for size dependent growth or temporal correlations in growth (`growth autocorrelation'), and are consistent with a lack of amplification of size variance through time. Juvenile C. asper appear to have been feeding on a relatively homogeneous resource and utilizing those resources similarly. Thus, patterns of individual growth and the presence of adult conspecifics may both serve to dampen size differences in this coastal fish species.     

Context-Dependent Plastic Response during Egg-Laying in a Widespread Newt Species

Previous research on predator-induced phenotypic plasticity mostly focused on responses in morphology, developmental time and/or behaviour during early life stages, but the potential significance of anticipatory parental responses has been investigated less often. In this study I examined behavioural and maternal responses of gravid female smooth newts, Lissotriton vulgaris, in the presence of chemical cues originating from invertebrate predators, Acilius sulcatus water beetles and Aeshna cyanea dragonfly larvae. More specifically, I tested the extent of oviposition preference, plasticity in egg-wrapping behaviour and plasticity in egg size when females had the possibility to lay eggs at oviposition sites with and without predator cues during overnight trials. I found that individuals did not avoid laying eggs in the environment with predator cues; however, individuals that deposited eggs into both environments adjusted the size of the laid eggs to the perceived environment. Females deposited larger eggs earlier in the season but egg size decreased with time in the absence of predator cues, whereas individuals laid eggs of average size throughout the investigated reproductive period when such cues were present. Also, egg size was found to be positively related to hatching success. Individuals did not adjust their wrapping behaviour to the presence of predator cues, but females differed in the extent of egg-wrapping between ponds. Females’ body mass and tail depth were also different between ponds, whereas their body size was positively associated with egg size. According to these results, female smooth newts have the potential to exhibit activational plasticity and invest differently into eggs depending on temporal and environmental factors. Such an anticipatory response may contribute to the success of this caudate species under a wide range of predator regimes at its natural breeding habitats.     

Patterns of coexistence between two mesocarnivores in northern Patagonia in the presence of invasive hares and anthropogenic disturbance

We analysed coexistence patterns between two mesocarnivores, Geoffroy's cat (Leopardus geoffroyi: Felidae) and culpeo fox (Pseudalopex culpaeus: Canidae), in northern Patagonia, Argentina. We examined spatial distribution influenced by land cover, anthropogenic disturbance and invasive hare presence, and analysed temporal activity patterns and dietary composition. If competitive exclusion accounts for carnivore coexistence in this system, we predicted segregation would occur in one or more of these aspects as a mechanism for coexistence. We performed camera trapping in Nahuel Huapi National Park, from February to May 2012 and January to April 2013. Using camera detections, we analysed spatial patterns with co‐occupancy modelling and temporal patterns by fitting kernel density estimates and measuring overlap. We performed a dietary meta‐analysis using available literature and performed a discriminant function analysis of diet categories between species. We observed high spatial and temporal overlap between Geoffroy's cats and culpeo foxes. We found no evidence of segregation in relation to land cover occupancy, anthropogenic disturbance, invasive hare occurrence or activity patterns. Though both species consumed predominantly small and medium mammals, Geoffroy's cats consumed more birds, reptiles and amphibians, and culpeo foxes consumed more large mammals, carrion and plant material; coexistence between these two carnivores in this Patagonian protected area appears to be facilitated by diet segregation.     

A newt does not change its spots: using pattern mapping for the identification of individuals in large populations of newt species

The correct identification of individuals is a requirement of capture-mark-recapture (CMR) methods, and it is commonly achieved by applying artificial marks or by mutilation of study-animals. An alternative, non-invasive method to identify individuals is to utilize the patterns of their natural body markings. However, the use of pattern mapping is not yet widespread, mainly because it is considered time consuming, particularly in large populations and/or long-term CMR studies. Here we explore the use of pattern mapping for the identification of adult individuals in the alpine (Ichthyosaura alpestris) and smooth (Lissotriton vulgaris) newts (Amphibia, Salamandridae), using the freely available, open-source software Wild-ID. Our photographic datasets comprised nearly 4000 captured animals’ images, taken during a 3-year period. The spot patterns of individual newts of both species did not change through time, and were sufficiently varied to allow their individual identification, even in the larger datasets. The pattern-recognition algorithm of Wild-ID was highly successful in identifying individual newts in both species. Our findings indicate that pattern mapping can be successfully employed for the identification of individuals in large populations of a broad range of animals that exhibit natural markings. The significance of pattern-mapping is accentuated in CMR studies that aim in obtaining long-term information on the demography and population dynamics of species of conservation interest, such as many amphibians facing population declines.