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See detailOn the identification of paedomorphic and overwintering larval newts based on cloacal shape: review and guidelines
Denoël, Mathieu ULg

in Current Zoology (in press)

Paedomorphosis is an alternative process to metamorphosis in which adults retain larval traits at the adult stage. It is frequent in newts and salamanders, where larvae reach sexual maturity without ... [more ▼]

Paedomorphosis is an alternative process to metamorphosis in which adults retain larval traits at the adult stage. It is frequent in newts and salamanders, where larvae reach sexual maturity without losing their gills. However, in some populations, larvae overwinter in water, while remaining immature. These alternative ontogenetic processes are of particular interest in various research fields, but have different causes and consequences, as only paedomorphosis allows metamorphosis to be bypassed before maturity. It is thus relevant to efficiently identify paedomorphs versus overwintering larvae. In this context, the aim of this paper was threefold: firstly, to perform a meta-analysis of the identification procedures carried out in the literature; secondly, to determine the effectiveness of body size to make inferences about adulthood by surveying natural newt populations of Lissotriton helveticus and Ichthyosaura alpestris, and thirdly, to propose easy guidelines for an accurate distinction between large larvae and paedomorphs based on an external sexual trait, which is essential for reproduction — the cloaca. More than half of the studies in the literature do not mention the diagnostic criteria used for determining adulthood. The criteria mentioned were the presence of mature gonads (10%), eggs laid (4%), courtship behaviour (10%), and external morphological sexual traits (39%) including the cloaca (24%). Body-size thresholds should not be used as a proxy for paedomorphosis, because overwintering larvae can reach a larger size than paedomorphs within the same populations. In contrast, diagnosis based on cloacal external morphology is recommended, as it can be processed by the rapid visual assessment of all caught specimens, thus providing straightforward data at the individual level for both sexes. [less ▲]

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See detailHabitat selection and reproduction of newts in networks of fish and fishless aquatic patches
Winandy, Laurane ULg; Legrand, Pauline ULg; Denoël, Mathieu ULg

in Animal Behaviour (2017), 123

The spatial distribution of organisms in patchy environments can be determined by the relationship between habitat quality and animal behaviour. In species with complex life cycles, such as pond-breeding ... [more ▼]

The spatial distribution of organisms in patchy environments can be determined by the relationship between habitat quality and animal behaviour. In species with complex life cycles, such as pond-breeding amphibians, the selection of a suitable wetland is crucial. While the traditional view of amphibian ecology suggests strong site fidelity and low vagility, more recent research highlights mechanisms involving active site choice through avoidance behaviour and bet-hedging strategies in heterogeneous environments. The introduction of fish to the aquatic environment is one of the factors that may alter site selection and lead to local dispersal. In this context, we investigated the habitat choice of Alpine newts, Ichthyosaura alpestris, in networks of fish (Carassius auratus) and fishless aquatic patches. Using a laboratory design consisting of aquaria divided into two water tanks connected by a terrestrial platform, we assessed newt distribution and movement between patches. During the breeding period, we compared the reproductive success of individuals in two types of networks. We found that newts escaped fish by rapidly changing aquatic patches and then aggregating in safe aquatic patches that were free of fish. In the fish network, newts maintained reproduction, but the high local abundance resulted in decreased sexual activity and egg production and increased use of the terrestrial habitat. However, in the fishless network, newts moved between aquatic patches several times, exhibited more courtship behaviour and laid more eggs than they did in the fish networks. Our results showed both adaptive habitat switching due to environmental risks in the fish network and habitat supplementation (i.e. use of alternative resources) in the fishless network. Such studies on movement behaviour and habitat selection have conservation implications in showing that the persistence of native species in invaded networks depends on the rescue effect, with immigration to fish-free habitats potentially preventing local extinction. [less ▲]

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See detailPoissons, tritons et pédomorphes
Denoël, Mathieu ULg

Scientific conference (2016, November 25)

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See detailPhenotypic plasticity in a fossorial toad from a Pacific xeric forest (Ecuador)
Székely, Diana ULg; Szekely, Paul; Denoël, Mathieu ULg et al

Poster (2016, October 06)

For amphibians, optimal size at metamorphosis is determined by a trade-off between opportunities for growth and risks of mortality in aquatic and terrestrial habitats, and many species show a high degree ... [more ▼]

For amphibians, optimal size at metamorphosis is determined by a trade-off between opportunities for growth and risks of mortality in aquatic and terrestrial habitats, and many species show a high degree of plasticity in time and size at metamorphosis that allow them to adapt to unpredictable environments. We used as model a neotropical anuran species, the Pacific horned frog, Ceratophrys stolzmanni, that inhabits the Tumbesian dry forests of southwestern Ecuador, and lays its eggs in lentic habitats of variable size and unpredictable duration. We investigated (i) how tadpoles time their metamorphosis in order to escape a rapidly drying aquatic habitat, and (ii) the consequences of metamorphosis plasticity on the immediate and mid-term fitness of individuals. We conducted two experiments; in the first one we exposed 36 tadpoles to one of three water levels treatments: constant high, decreasing and constant low. Tadpoles that were raised in decreasing or low water level metamorphosed on average 13% and 10% faster than the ones from constant high water level, but at a lower body size and mass. Growth rates were among the highest recorded for tadpoles and individuals from the constant high water level treatment grew at a much faster rate than the others. In a second experiment, we sampled 72 freshly metamorphosed (Gosner stage 45) C. stolzmanni individuals of assorted sizes (SVL between 23.8 and 47.9 mm, body weight between 1.2 and 11.9 g). From this spectrum of sizes, we selected the 21 largest and 22 smallest individuals and evaluated the effects of body size at metamorphosis on trophic and locomotory performance parameters. We determined their growth rate and survival over the course of an activity season (i.e., two months). Our results show that bigger size at metamorphosis is correlated with better survival chances and performance. Larger individuals were more mobile, had bigger gape width and better survival rates (95% compared to 64% for small individuals). Growth rates were not correlated with initial size, and small individuals were capable of increasing their size at a higher rate. This indicates that, although size at metamorphosis has an immediate impact on fitness, smaller individuals are able to compensate with an increased growth rate. [less ▲]

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See detailWho are the winners in the race against desiccation – phenotypic plasticity in a fossorial toad
Székely, Diana ULg; Székely, Paul; Denoël, Mathieu ULg et al

Conference (2016, September 29)

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See detailUn morso di più: ecologia del cannibalismo in Salamandra salamandra
Melotto, Andrea; Manenti, Raoul; Ficetola, Francesco et al

Conference (2016, September 23)

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See detailRole of phenotypic plasticity and local adaptation in allowing cave exploitation: ecological and evolutionary insights from the fire salamander
Manenti, Raoul; Melotto, Andrea; Tagliaferro, L. et al

Conference (2016, August 31)

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See detailAmphibians breeding in refuge habitats have larvae with stronger antipredator responses
Manenti, Raoul; Melotto, Andrea; Denoël, Mathieu ULg et al

in Animal Behaviour (2016), 118

Antipredator responses are a key determinant of the successful persistence of prey, and behavioural modifications are a frequent antipredator strategy. However, conspecific populations often inhabit ... [more ▼]

Antipredator responses are a key determinant of the successful persistence of prey, and behavioural modifications are a frequent antipredator strategy. However, conspecific populations often inhabit heterogeneous environments. This can determine local adaptations, and might also induce variation in antipredator responses. Nevertheless, there is limited information on whether heterogeneity of predation risk among populations determines variation in antipredator response. Here we studied the fire salamander, Salamandra salamandra, a species that can breed in both surface streams and caves, habitats that are predator-rich and predator-free, respectively, and measured differences in antipredator responses across populations with different predation risk. We combined field surveys and laboratory experiments to understand the role of predation risk on the activity patterns of larvae, while measuring behavioural differences between populations. We reared larvae from different habitats in safe and risky conditions and tested their response to predator cues before and after rearing. In the field, predation risk was much higher in surface streams than in caves; larvae moved more in the absence of predators and when the light intensity was low. During laboratory experiments, larvae were less active if reared in risky conditions, but cave larvae showed a stronger response to risk than stream larvae. Therefore, larvae from sites without predators showed higher antipredator responses than those from risky habitats. This response fits the predictions of the risk allocation model, in which prey from habitats with a high background level of risk need to be active even when predators are present, to satisfy their energetic demands. Our findings show that antipredator behaviour may differ strongly between populations and stress the importance of integrating this variability in studies on predatory responses. [less ▲]

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See detailHigh gene flow between alternative morphs and the evolutionary persistence of facultative paedomorphosis
Oromi Farrús, Neus ULg; Michaux, Johan ULg; Denoël, Mathieu ULg

in Scientific Reports (2016), 6

Paedomorphosis and metamorphosis are two major developmental processes that characterize the evolution of complex life cycles in many lineages. Whereas these processes were fixed in some taxa, they ... [more ▼]

Paedomorphosis and metamorphosis are two major developmental processes that characterize the evolution of complex life cycles in many lineages. Whereas these processes were fixed in some taxa, they remained facultative in others, with alternative phenotypes expressed in the same populations. From a genetic perspective, it is still unknown whether such phenotypes form a single population or whether they show some patterns of isolation in syntopy. This has deep implications for understanding the evolution of the phenotypes, i.e. towards their persistence or their fixation and speciation. Newts and salamanders are excellent models to test this hypothesis because they exhibit both developmental processes in their populations: the aquatic paedomorphs retain gills, whereas the metamorphs are able to colonize land. Using microsatellite data of coexisting paedomorphic and metamorphic palmate newts (Lissotriton helveticus), we found that they formed a panmictic population, which evidences sexual compatibility between the two phenotypes. The high gene flow could be understood as an adaptation to unstable habitats in which phenotypic plasticity is favored over the fixation of developmental alternatives. This makes then possible the persistence of a polyphenism: only metamorphosis could be maintained in case of occasional drying whereas paedomorphosis could offer specific advantages in organisms remaining in water. [less ▲]

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See detailTemporal habitat shift of a polymorphic newt species under predation risk
Winandy, Laurane ULg; Colin, Mélanie; Denoël, Mathieu ULg

in Behavioral Ecology (2016), 27(4), 1025-1032

The temporal partitioning hypothesis suggests that the evolution of different diel activity rhythms in animals might facilitate the coexistence between prey and predators. However, the temporal shift of ... [more ▼]

The temporal partitioning hypothesis suggests that the evolution of different diel activity rhythms in animals might facilitate the coexistence between prey and predators. However, the temporal shift of habitat use induced by predation has rarely been observed. The study of such a mechanism is particularly relevant for introduced species because it might explain how native species can persist or decline in response to the presence of alien species. The introduction of fish into ponds inhabited by amphibians has severe consequences for their occurrence and abundance. Fish particularly affect an alternative newt phenotype, the paedomorph, which does not undergo metamorphosis and maintains larval traits such as gills at the adult stage. In a laboratory design, we assessed the diel patterns of habitat use in the 2 distinct morphological phenotypes of palmate newt (Lissotriton helveticus) in the presence or absence of goldfish (Carassius auratus). Both newt phenotypes avoided a risky habitat more in the presence than in the absence of fish. This habitat shift was more pronounced during the daytime (i.e., when the risk could be considered higher for the newts) than during nighttime. However, in contrast to metamorphs, paedomorphs showed less adaptive changes according to temporal risk and remained in their shelter for most of the time. Temporal and habitat partitioning at the diel scale between native and alien species might promote their coexistence, but diel change can also imply a cost in the overall reduction of the time allocated to essential activities, showing that species interactions remain complex. [less ▲]

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See detailCollective vortex behaviors: diversity, proximate, and ultimate causes of circular animal group movements
Delcourt, Johann ULg; Bode, W.F. Nikolaï; Denoël, Mathieu ULg

in Quarterly Review of Biology (2016), 91(1), 1-24

Ant mill, caterpillar circle, bat doughnut, amphibian vortex, duck swirl, and fish torus are different names for rotating circular animal formations, where individuals turn around a common center. These ... [more ▼]

Ant mill, caterpillar circle, bat doughnut, amphibian vortex, duck swirl, and fish torus are different names for rotating circular animal formations, where individuals turn around a common center. These “collective vortex behaviors” occur at different group sizes from pairs to several million individuals and have been reported in a large number of organisms, from bacteria to vertebrates, including humans. However, to date, no comprehensive review and synthesis of the literature on vortex behaviors has been conducted. Here, we review the state of the art of the proximate and ultimate causes of vortex behaviors. The ubiquity of this behavioral phenomenon could suggest common causes or fundamental underlying principles across contexts. However, we find that a variety of proximate mechanisms give rise to vortex behaviors. We highlight the potential benefits of collective vortex behaviors to individuals involved in them. For example, in some species, vortices increase feeding efficiency and could give protection against predators. It has also been argued that vortices could improve collective decision making and information transfer. We highlight gaps in our understanding of these ubiquitous behavioral phenomena and discuss future directions for research in vortex studies. [less ▲]

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See detailProvenance of Ichthyosaura alpestris (Caudata: Salamandridae) introductions to France and New Zealand assessed by mitochondrial DNA analysis
Arntzen, Jan W.; King, Tania M.; Denoël, Mathieu ULg et al

in The Herpetological Journal (2016), 26(1), 49-56

The last century has seen an unparalleled movement of species around the planet as a direct result of human activity, which has been a major contributor to the biodiversity crisis. Amphibians represent a ... [more ▼]

The last century has seen an unparalleled movement of species around the planet as a direct result of human activity, which has been a major contributor to the biodiversity crisis. Amphibians represent a particularly vulnerable group, exacerbated by the devastating effects of chytrid fungi. We report the malicious translocation and establishment of the alpine newt (Ichthyosaura alpestris) to its virtual antipode in North Island of New Zealand. We use network analysis of mitochondrial DNA haplotypes to identify the original source population as I. a. apuana from Tuscany, Italy. Additionally, a population in southern France, presumed to be introduced, is identified as I. a. alpestris from western Europe. However, the presence of two differentiated haplotypes suggests a mixed origin. This type of analysis is made possible by the recent availability of a phylogenetic analysis of the species throughout its natural range. We discuss the particulars of both introductions. [less ▲]

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See detailNewt life after fish introduction: extirpation of paedomorphosis in a mountain fish lake and newt use of satellite pools
Denoël, Mathieu ULg; Scime, Patrick; Zambelli, Nicola

in Current Zoology (2016), 62(1), 61-69

Fish introduction is one of the main causes of amphibian decline worldwide. It affects particularly rare aquatic phenotypes such as paedomorphs, which retain gills during the adult stage. In this context ... [more ▼]

Fish introduction is one of the main causes of amphibian decline worldwide. It affects particularly rare aquatic phenotypes such as paedomorphs, which retain gills during the adult stage. In this context, we determined whether small wetlands, such as pools surrounding fished and fishless lakes, could sustain paedomorphic and metamorphic newts. To this end, we surveyed lakes known historically to sustain Alpine newts (Ichthyosaura alpestris) as well as 35 nearby pools. On the basis of the published records, the only known population exhibiting paedomorphosis in the Swiss Alps was found to be extirpated by salmonid introductions. However, the metamorphs persisted in peripheral pools, paedomorphosis was discovered at a new locality, and overwintering larvae were still present in one of the lakes. These results show the importance of conserving varied aquatic habitats such as pools in mountainous environments where the main resources can become unsuitable for amphibians because of fish introductions. Pools may also function as reservoirs in maintaining newt populations until programs to remove fish from lakes can be carried out. It is not known if paedomorphs could reappear after fish removal. However, the combined resilience of amphibians after fish removal and the genetic basis for paedomorphosis highlighted in other taxa by previous studies suggest that there is the potential to maintain this intraspecific case of diversity even after its disappearance. [less ▲]

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See detailThe importance of phenotypic diversity in conservation: Resilience of palmate newt morphotypes after fish removal in Larzac ponds (France)
Denoël, Mathieu ULg; Winandy, Laurane ULg

in Biological Conservation (2015), 192

Resilience of organisms after threat removal is an essential feature to justify conservation efforts. Amphibians are particularly threatened with a worldwide decline, showing a low resistance to invaders ... [more ▼]

Resilience of organisms after threat removal is an essential feature to justify conservation efforts. Amphibians are particularly threatened with a worldwide decline, showing a low resistance to invaders such as fish. Previous research has shown that they could recover after fish extirpation due to metamorphosed colonizers. However, not all amphibian phenotypes are able to persist to fish introduction and disperse. In many species of newts and salamanders, paedomorphs retain gills in the adult stage, which makes them fully aquatic. A proposed way to conserve this phenotype would be to remove introduced fish from their habitats. However, because paedomorphosis is usually not expressed in the presence of fish, it is unknown whether fish removal could allow the resilience of paedomorphs. This would be possible only if progenies of metamorphosed individuals could become paedomorphic in restored habitats. Through a quantitative survey in three types of ponds, including control ponds without fish, ponds in which fish were extirpated, and fish ponds, we determined abundances of paedomorphic and metamorphic palmate newts (Lissotriton helveticus). The results show that paedomorphosis resilience is possible and even highly frequent, as paedomorphs were found in 80% of ponds where fish disappeared. Abundances were similar between these ponds and control ponds whereas fish ponds had almost no newts, indicating a very low resistance to invaders. This shows that conserving common phenotypes can help to preserve endangered phenotypes, as paedomorphs were produced through the reproduction of metamorphs. There is thus hope of maintaining intraspecific biodiversity though conservation action involving threat removal. [less ▲]

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See detailThe aggressive personality of an introduced fish affects foraging behavior in a polymorphic newt
Winandy, Laurane ULg; Denoël, Mathieu ULg

in Behavioral Ecology (2015), 26(6), 1528-1536

The study of personality has aroused much interest and has provided insight into the understanding of animal behavior. Nevertheless, the study of the ecological consequences of personality is a newer ... [more ▼]

The study of personality has aroused much interest and has provided insight into the understanding of animal behavior. Nevertheless, the study of the ecological consequences of personality is a newer field that could shed light on cases of alien species introductions. The goldfish (Carassius auratus) is frequently introduced worldwide and affects the abundance of newts, having an especially negative impact on an alternative phenotype, the paedomorph, which maintains larval traits at the adult stage, unlike the other phenotype, the metamorph, which has undergone metamorphosis. We experimentally assessed the impact of goldfish on the foraging behavior of both phenotypes of palmate newts (Lissotriton helveticus). More particularly, we assessed fish personality by analyzing the foraging activity and the aggressiveness toward newts, and newt personality by analyzing individual difference in boldness. In the presence of fish, fewer newts foraged than in their absence, and paedomorphs were more affected than metamorphs. We found strong personality differences in fish and fewer newts foraged in the presence of a more aggressive fish. Newts differed in boldness, but fish aggressiveness remains a key factor to explain newt behavior. Studying behavioral interactions between native and alien species helps to understand the mechanisms of coexistence and exclusion and why different phenotypes might be affected differently by the same threat. To a great extent, not only the presence of fish alters the foraging opportunities of newts but also the personality of the invader; integrating personality patterns of invaders is therefore a key to understanding the ecological consequences of alien species introduction. [less ▲]

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See detailAmphibians forgo aquatic life in response to alien fish introduction
Winandy, Laurane ULg; Darnet, Elodie; Denoël, Mathieu ULg

in Animal Behaviour (2015), 109

Species with complex life cycles are good models to understand trade-offs between life in hostile and favourable habitats. Newts remain in breeding wetlands for a long period and are strongly affected by ... [more ▼]

Species with complex life cycles are good models to understand trade-offs between life in hostile and favourable habitats. Newts remain in breeding wetlands for a long period and are strongly affected by fish introduction; however, mechanisms of the exclusion observed in the field are still not well known. In particular, whether newts skip breeding and leave water for land in response to fish introduction and how aquatic shelter may influence their choice remain open questions. To investigate these questions, we experimentally studied the use of aquatic and terrestrial habitats during the breeding season of palmate newts, Lissotriton helveticus, in the presence and absence of goldfish, Carassius auratus. We determined the consequences of habitat choice on newt fitness by assessing sexual activity and number of eggs. There was a strong, significant avoidance of the aquatic environment in the presence of fish, particularly when no aquatic shelter was available. This escape from the water had an impact on reproduction: newts decreased their sexual activity and laid fewer eggs. The availability of shelters favoured coexistence but did not prevent a large proportion of the newts from leaving water and skipping reproduction. This study shows how the presence of fish and the absence of aquatic shelters can lead to newts forgoing aquatic life, thus improving our understanding of the mechanisms behind the coexistence and exclusion patterns found in the wild. More broadly, these data contribute to explaining aquatic versus terrestrial life in favourable and unfavourable environments. [less ▲]

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