Salamander Larvae Research Articles

Predator cannibalism can shift prey community composition toward dominance by small prey species.

Cannibalism among predators is a key intraspecific interaction affecting their density and foraging behavior, eventually modifying the strength of predation on heterospecific prey. Interestingly, previous studies showed that cannibalism among predators can increase or reduce predation on heterospecific prey; however, we know less about the factors that lead to these outcomes. Using a simple pond community consisting of Hynobius retardatus salamander larvae and their associated prey, I report empirical evidence that cannibalism among predators can increase predation on large heterospecific prey but reduce that on small heterospecific prey. In a field‐enclosure experiment in which I manipulated the occurrence of salamander cannibalism, I found that salamander cannibalism increased predation on frog tadpoles but reduced that on aquatic insects simultaneously. The contrasting effects are most likely to be explained by prey body size. In the study system, frog tadpoles were too large for non‐cannibal salamanders to consume, while aquatic insects were within the non‐cannibals’ consumable prey size range. However, when cannibalism occurred, a few individuals that succeeded in cannibalizing reached large enough size to consume frog tadpoles. Consequently, although cannibalism among salamanders reduced their density, salamander cannibalism increased predation on large prey frog tadpoles. Meanwhile, salamander cannibalism reduced predation on small prey aquatic insects probably because of a density reduction of non‐cannibals primarily consuming aquatic insects. Body size is often correlated with various ecological traits, for instance, diet width, consumption, and excretion rates, and is thus considered a good indicator of species’ effects on ecosystem function. All this considered, cannibalism among predators could eventually affect ecosystem function by shifting the size composition of the prey community.

Oviparity, viviparity or plasticity in reproductive mode of the olm Proteus anguinus: an epic misunderstanding caused by prey regurgitation?

Abstract Cave animals are biological models of fast evolutionary change induced by transition to extreme subterranean environments. But their concealed lifestyle makes it inherently difficult to study life-history changes. Therefore, currently very little is known on the reproduction of cave species, and even less is known on general patterns and potentially shared reproductive strategies. Theory predicts that the cave environment favours the production of a few well-developed offspring and live birth. For one of the most enigmatic cave animals, the olm (Proteus anguinus), it has been debated fiercely whether they reproduce by live birth (viviparity), egg-laying (oviparity) or facultatively. While successes in captive breeding after the 1950s report oviparity as the single parity mode, some historically older observations claimed viviparity. The controversial neo-Lamarckist Paul Kammerer even claimed to have induced changes in parity mode by altering environmental conditions. Here, we report on the feeding and regurgitation of fire salamander (Salamandra salamandra) larvae by olms. The salamander larvae showed clear teeth marks and other injuries on the head caused by the olm, yet one larva was still alive after regurgitation. We suggest that historical reports of olm viviparity could have been misled by regurgitated salamander larvae. Our data bring additional indications that at least some of Kammerer’s experiments were fraudulent.

A near-natural experiment on factors influencing larval drift in Salamandra salamandra

The larval stage of the European fire salamander (Salamandra salamandra) inhabits both lentic and lotic habitats. In the latter, they are constantly exposed to unidirectional water flow, which has been shown to cause downstream drift in a variety of taxa. In this study, a closed artificial creek, which allowed us to keep the water flow constant over time and, at the same time, to simulates with predefined water quantities and durations, was used to examine the individual movement patterns of marked larval fire salamanders exposed to unidirectional flow. Movements were tracked by marking the larvae with VIAlpha tags individually and by using downstream and upstream traps. Most individuals showed stationarity, while downstream drift dominated the overall movement pattern. Upstream movements were rare and occurred only on small distances of about 30 cm; downstream drift distances exceeded 10 m (until next downstream trap). The simulated flood events increased drift rates significantly, even several days after the flood simulation experiments. Drift probability increased with decreasing body size and decreasing nutritional status. Our results support the production hypothesis as an explanation for the movements of European fire salamander larvae within creeks.

Differential Infection of Two Sympatric, Cryptic Species of Appalachian Salamander (Genus Desmognathus) by the Trematode Metagonimoides oregonensis

In the southern Appalachian Mountains, U.S.A., the trematode Metagonimoides oregonensis, a parasite of raccoons and possibly mink, utilizes larvae of lungless salamanders as second intermediate hosts, most frequently using the salamander Desmognathus quadramaculatus. We tested whether there was a difference in parasite infection between this salamander and its sympatric, cryptic congener, Desmognathus folkertsi, in northern Georgia. Whereas larval D. quadramaculatus had a prevalence of 100% with intensities ranging from 18 to over 1,000, none of the D. folkertsi had visible metacercariae. These results indicate that M. oregonensis is more host-specific in salamander second intermediate hosts in the southern Appalachians than previously reported.

Complementary Occupancy of Semi-permanent Wetlands by Tiger Salamander (Ambystoma tigrinum) Larvae and Fishes as Indicated by Zooplankton Size and Color: How Respiratory Physiology Explains Community Ecology

Hydrology and dissolved oxygen (DO) availability drive wetland occupancy by zooplantivorous predators in the Prairie Pothole Region of the northeastern Great Plains, as follows. Permanent wetlands favor fishes, while the shallow waters of seasonal wetlands favor invertebrates and the larvae of the amphibian spring-breeding guild, including Tiger Salamanders (Ambystoma tigrinum). Semi-permanent wetlands fluctuate between these two extremities, holding water during wet years but drying during droughts, which means the aquatic vertebrate occupancy of these wetlands typically switches between fishes (wet periods) and amphibian larvae (droughts). Further, the shallow water of wetlands promotes hypoxic/anoxic conditions, creating “summerkills” and “winterkills,” primarily of fishes, which obligately breathe DO. Spring-breeding amphibian larvae avoid summerkills by air gulping—using their lungs to access atmospheric oxygen—and avoid winterkills by metamorphosing. Zooplankton, in turn, have several responses to these wetland conditions and their predators. In reaction to visually mediated, size-selective fish predation, small and semi-transparent zooplankton are selected for, and they undertake daily vertical migrations; the literature on this ecological interaction is vast. In response to intense invertebrate predation pressure, zooplankton become large. In response to wetland hypoxia, zooplankton upregulate hemoglobin (i.e., create blood), which makes them conspicuously red. Nocturnally active Tiger Salamander larvae use senses other than vision (likely lateral line mechano- and electroreceptors) to detect prey, permitting zooplankton to be large and red. The presence or absence of fishes or amphibians, combined with zooplankton morphology (small/large, semi-transparent/red), therefore create hypotheses regarding recent wetland conditions. This variability, while characterizing semi-permanent wetlands, is much more dramatic and dynamic than has previously been reported for palustrine basins. As such, by this and other criteria, I offer a synthesis built upon an understanding of respiratory physiology to explain the ecological communities observed in prairie wetlands.

Predator-avoidance of larval black-bellied salamanders (Desmognathus quadramaculatus) in response to cues from native and nonnative salmonids

Fish are significant predators of amphibian larvae in streams and larvae can detect these predators through both visual and olfactory cues. The ability to effectively recognize these cues may depend on the evolutionary history of predator and prey such that recently introduced predators may not be recognized as readily as those that have consistently coexisted with the prey species. As such, the relatively recent introduction of rainbow trout (Oncorhynchus mykiss) into Southern Appalachian headwater streams where the black-bellied salamander (Desmognathus quadramaculatus) and brook trout (Salvelinus fontinalis) naturally coexist has raised concern. The objective of this study was to determine whether black-bellied salamander larvae respond to cues from introduced rainbow trout. To evaluate this, salamander activity metrics (general activity and number of movements) were recorded before and after exposure to either native trout predator cue (brook), introduced trout predator cue (rainbow), or conditioned tap water (control). Larvae were collected from different stream reaches based on their cooccurrence with brook trout only, rainbow trout only, rainbow and brook trout, or no trout predators. Larvae that co-occur with trout reduced their activity when exposed to brook trout predator cue, but their response to rainbow trout predator cue depended on their previous co-occurrence. A follow-up test to determine the influence of alarm cue on predator response indicated that the alarm cue enhanced the response to the rainbow trout predator.

Epidermal galactose spurs chytrid virulence and predicts amphibian colonization

The chytrid fungal pathogens Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans cause the skin disease chytridiomycosis in amphibians, which is driving a substantial proportion of an entire vertebrate class to extinction. Mitigation of its impact is largely unsuccessful and requires a thorough understanding of the mechanisms underpinning the disease ecology. By identifying skin factors that mediate key events during the early interaction with B. salamandrivorans zoospores, we discovered a marker for host colonization. Amphibian skin associated beta-galactose mediated fungal chemotaxis and adhesion to the skin and initiated a virulent fungal response. Fungal colonization correlated with the skin glycosylation pattern, with cutaneous galactose content effectively predicting variation in host susceptibility to fungal colonization between amphibian species. Ontogenetic galactose patterns correlated with low level and asymptomatic infections in salamander larvae that were carried over through metamorphosis, resulting in juvenile mortality. Pronounced variation of galactose content within some, but not all species, may promote the selection for more colonization resistant host lineages, opening new avenues for disease mitigation.

Phenotypic Plasticity of Salamander Hatchlings in the Pre-Feeding Stage in Response to Future Prey.

Vulnerability of animals immediately after hatching may induce plasticity in early ontology that becomes important for subsequent survival and growth. Ezo salamanders (Hynobius retardatus) are amphibians inhabiting ponds in Hokkaido, Japan where ezo brown frogs (Rana pirica) spawn on occasion. The salamander larvae must achieve sufficient size in order to successfully capture frog tadpoles, and we examined whether the presence of tadpoles causes development of greater body and/or gape size in newly hatched salamander larvae, which will in turn result in advantageous future prey-predator interactions. To examine this hypothesis, we conducted three laboratory experiments to demonstrate the phenotypic plasticity of salamander hatchlings in response to the presence or absence of frog tadpoles and to screen the type of signals involved in the expression of the phenotypic plasticity. First, salamander hatchlings were reared alone or with tadpoles, and the growth and morphological traits of the hatchlings were compared. The results showed that hatchling larvae grew faster with a more developed gape in the presence of tadpoles. Next, to identify the type of signals inducing this plasticity, two separate experiments with manipulated chemical and visual signals from tadpoles were conducted. The findings showed that faster growth and a more developed gape were induced by chemical but not visual signals. This plasticity may be an adaptive strategy because it increases the likelihood of preying on tadpoles in future prey-predator interactions.

Salvage and translocation of endangered Santa Cruz long-toed salamander larvae

Salvage and translocation of endangered Santa Cruz long-toed salamander larvae

Investigating Acute and Subchronic Effects of Neonicotinoids on Northwestern Salamander Larvae

This research investigated the adverse effects of neonicotinoids on the Northwestern salamander (Ambystoma gracile; NWS) after acute and subchronic exposures during early aquatic life stages via whole organism (i.e., growth, development) and molecular (i.e., gene expression) level endpoints. In a 96-h exposure, NWS larvae were exposed to four imidacloprid concentrations (250, 750, 2250, 6750µg/L) and a water control treatment, and no effects on survival, body weight, snout-vent length (SVL), and total body length were observed. However, a significant 1.70- and 2.33-fold decrease in thyroid receptor β (TRβ) mRNA expression levels were detected in the larvae exposed to 750 and 2250µg/L imidacloprid, respectively, compared with the larvae in the water control. In subsequent subchronic experiments, NWS larvae were exposed for 35days to imidacloprid alone and an equal part mixture of neonicotinoids (imidacloprid, clothianidin, and thiamethoxam (ICT)) at three concentrations (10, 100 and 1000µg total neonicotinoids/L) and a water control. In these experiments, there were no effects on larval survival, body weight, SVL, and total body length. However, advanced development of larvae in the 100µg/L imidacloprid treatment was observed compared with the control after 35-day imidacloprid exposure, providing some evidence of disruption of the thyroid endocrine axis at an environmentally relevant concentration. Ultimately, there is a paucity of studies conducted examining the sensitivity of salamanders to pollutants; thus, this study reports novel findings that will contribute to understanding the sensitivity of a Caudate amphibian model to a common environmental pollutant.

Evaluating eDNA-based monitoring of fire salamander larvae under field conditions

Amphibians globally belong to the most threatened animal groups and monitoring their populations is of critical importance for their conservation. The fire salamander (Salamandra salamandra) is one of the European amphibian species which has been experiencing drastic regional population declines due to the spread of the invasive chytrid fungus Batrachochytrium salamandrivorans, making it a key species for monitoring efforts. Here, we evaluated how the sampling and analysis of eDNA can aid the monitoring of larval salamander populations in small streams under field conditions. Nine small streams with known adult and larval fire salamander populations were investigated in Tirol (Austria). Per steam a stretch of 30 m downstream from its source was divided into 10 m sections where salamander larvae were counted. Water samples were taken at the end of each section and filtered on site. The DNA extracted from these filters was tested by a new PCR assay developed for the detection of mitochondrial DNA of S. salamandra. This assay combines endpoint PCR with capillary electrophoresis, allowing to relatively quantify the amount of fire salamander eDNA present in the water samples. In two of the nine streams no eDNA of S. Salamandra could be detected. The outcomes of an analysis of how larval densities, discharge and volume of filtered water affected the detection of salamander eDNA will be presented. Finally, we will conclude on the practical implications of the current findings for eDNA-based monitoring of fire salamander populations.

Food level and light conditions affect the antipredator behavior in larvae of a stream-breeding amphibian

Understanding how long-term changes in environmental conditions influence the way that individuals cope with threats is essential in the context of behavioral adaptation to a rapidly changing world. However, little is known about the behavioral responses to predation risk for individuals that experienced different environmental conditions for extended periods of time, such as food levels and light conditions. In this experimental study, we tested whether previous long-term exposure to different food levels (low versus high) and light conditions (0-h light versus 8-h light) plays a significant role in shaping the antipredator response (i.e., the probability of emerging from the refuge and the distance moved) to stimuli from caged larval dragonflies, in larvae of the fire salamander (Salamandra salamandra). Specifically, we quantified behavioral differences in the response to predation risk in larval salamanders that were reared in the laboratory for 2 months under controlled food and light conditions. The results of this study showed that the interaction between food level and light conditions affected the antipredator behavior of the larvae. Fire salamander larvae maintained at low food levels and in 8-h light conditions emerged from the refuge with a higher probability (i.e., took more risk) than larvae maintained at high food levels and all other combinations of light conditions. Thus, our results highlight the complexity of antipredator responses, pointing attention to the fact that interactions among environmental factors are likely to determine the magnitude of antipredator response. Few studies have investigated the role of multiple environmental factors on the expression of predator-induced behavioral responses. Specifically, because no study has so far investigated the risk-taking behavior in individuals exposed to long-term, contrasting food levels, and light conditions, we investigated this in amphibian larvae. We showed that environmental conditions interactively determined antipredator behavior. This highlights the importance of considering long-term environmental conditions experienced by an organism and their interactions when experimentally studying behavioral variation to adequately understand its expression in natural conditions.

A case of color aberration in a fire salamander (Salamandra salamandra) larva

Color aberrations in salamanders are caused by defective chromatophores or by disrupted synthesis of the pigments, and have been previously reported in Europe. In this paper we report the first case of leucism in a fire salamander larva from a cave-dwelling population in Romania. The leucistic larva was larger and heavier compared to the other larvae from the same breeding habitat.

Significant reductions of host abundance weakly impact infection intensity of Batrachochytrium dendrobatidis.

Infectious diseases are considered major threats to biodiversity, however strategies to mitigate their impacts in the natural world are scarce and largely unsuccessful. Chytridiomycosis is responsible for the decline of hundreds of amphibian species worldwide, but an effective disease management strategy that could be applied across natural habitats is still lacking. In general amphibian larvae can be easily captured, offering opportunities to ascertain the impact of altering the abundance of hosts, considered to be a key parameter affecting the severity of the disease. Here, we report the results of two experiments to investigate how altering host abundance affects infection intensity in amphibian populations of a montane area of Central Spain suffering from lethal amphibian chytridiomycosis. Our laboratory-based experiment supported the conclusion that varying density had a significant effect on infection intensity when salamander larvae were housed at low densities. Our field experiment showed that reducing the abundance of salamander larvae in the field also had a significant, but weak, impact on infection the following year, but only when removals were extreme. While this suggests adjusting host abundance as a mitigation strategy to reduce infection intensity could be useful, our evidence suggests only heavy culling efforts will succeed, which may run contrary to objectives for conservation.

Microgeographic divergence of functional responses among salamanders under antagonistic selection from apex predators.

A predator's functional response determines predator-prey interactions by describing the relationship between the number of prey available and the number eaten. Its shape and parameters fundamentally govern the dynamic equilibrium of predator-prey interactions and their joint abundances. Yet, estimates of these key parameters generally assume stasis in space and time and ignore the potential for local adaptation to alter feeding responses and the stability of trophic dynamics. Here, we evaluate if functional responses diverge among populations of spotted salamander (Ambystoma maculatum) larvae that face antagonistic selection on feeding strategies based on their own risk of predation. Common garden experiments revealed that spotted salamander from ponds with varying predation risks differed in their functional responses, suggesting an evolutionary response. Applying mechanistic equations, we discovered that the combined changes in attack rates, handling times and shape of the functional response enhanced feeding rate in environments with high densities of gape-limited predators. We suggest how these parameter changes could alter community equilibria and other emergent properties of food webs. Community ecologists might often need to consider how local evolution at fine scales alters key relationships in ways that alter local diversity patterns, food web dynamics, resource gradients and community responses to disturbance.

Macrogeographic variation of a pond predator's top‐down effects in a common garden environment

AbstractGeographic variation in species behavior and life history has been well documented in biology. Species with wide geographic distributions (i.e., across a continent) but small home ranges (i.e., <1 km2) likely experience wide variability in abiotic environments across the entirety of their range, possibly exhibiting strong local adaptation. Understanding variation across a large geographic scale is especially important when considering species that have strong ecological importance, such as keystone species. Yet, few studies have compared the potential cascading ecological effects of a predator with a keystone role in at least part of its range. To understand how keystone ability in pond food webs can vary across a large geographic range, we conducted an artificial pond experiment with a known keystone predator in at least part of its range, the marbled salamander (Ambystoma opacum). To do so, we collected size‐matched salamander larvae from three geographically distant populations (>650 km apart) in Ohio, Mississippi, and North Carolina and placed them in mesocosms with a suite of spring breeding amphibian prey species. We observed differential survival of some prey species leading to differences in spring‐breeding amphibian diversity among the three predator populations, indicating that keystone predation may vary at a geographic scale. Prey diversity was lowest with predators from northern (Ohio) populations of salamanders. Further understanding of large‐scale variability in ecologically important predators and the potential effects of translocating wide‐ranging ambystomatid species is needed to direct future conservation efforts and preserve biodiversity.

Do Existing Constructed Ponds on Pelee Island, Ontario Match the Habitat Requirements of Endangered Ambystoma Larvae?

Global loss of wetlands has significantly reduced the habitat available for amphibians. Various organizations now regularly construct wetlands to provide areas for amphibian reproduction and larval development. To support wetland taxa, including federally-endangered salamanders, numerous ponds have been constructed in Southern Ontario. We examine natural and constructed ponds to address three questions: 1) What environmental variables govern the presence of salamander larvae in ponds?, 2) What environmental variables predict relative abundance of salamander larvae?, and 3) Do constructed ponds match the habitat needs for salamander larvae as observed in natural ponds? Presence of larvae was associated with high canopy cover and crayfish burrow presence, whereas catch-per-unit-effort increased with the amount of leaf litter in the substrate and presence of submergent vegetation. Constructed ponds had less canopy cover, less leaf litter in the substrate, warmer water, and fewer contained submergent vegetation. Larvae were caught in only 33% of constructed ponds, and catch-per-unit-effort was ~4-10x lower than in natural ponds. Constructed ponds on Pelee Island therefore require additional restoration support or naturalization before they are of substantial conservation value to salamanders. Protecting natural breeding sites remains critical for amphibian conservation, as created ponds may not adequately alleviate the loss of this habitat.

There is no place like home: Larval habitat type and size affect risk‐taking behaviour in fire salamander larvae (Salamandra salamandra)

AbstractIndividual life histories are strongly influenced by early environmental conditions and experiences. They shape morphology as well as behaviour and can promote adaptive divergence and phenotypic plasticity with regard to different habitat types. The fire salamander (Salamandra salamandra) in the Kottenforst forest in Bonn, Germany, exhibits two genetically distinct ecotypes occurring in two larval habitats, either ponds or streams. In this study, we investigated whether both ecotypes differ in risk‐taking behaviour, measured as the behavioural response during a shelter‐emergence test and a shelter‐seeking test, and whether larval habitat type and size impact these behaviours. Our results revealed an influence of size as well as habitat type. Larger larvae of both habitats appear to be more risk‐prone, as they spent more time outside the starting shelter in the shelter‐emergence test. Irrespective of size, pond larvae sought shelter more often in the shelter‐seeking test and are thus considered to be less risk‐prone. These results indicate that larvae conform to a given niche by adjusting their behaviour. Future studies are needed to disentangle the role of genetic adaptation or phenotypic plasticity and to investigate long‐term consequences of the larval habitat for the adult phenotype. Thereby, efforts should be made to create a concise set of multiple tests assessing behavioural patterns.

Do Salamanders Limit the Abundance of Groundwater Invertebrates in Subterranean Habitats?

Several species of surface salamanders exploit underground environments; in Europe, one of the most common is the fire salamander (Salamandra salamandra). In this study, we investigated if fire salamander larvae occurring in groundwater habitats can affect the abundance of some cave-adapted species. We analyzed the data of abundance of three target taxa (genera Niphargus (Amphipoda; Niphargidae), Monolistra (Isopoda; Sphaeromatidae) and Dendrocoelum (Tricladida; Dedrocoelidae)) collected in 386 surveys performed on 117 sites (pools and distinct subterranean stream sectors), within 17 natural and 24 artificial subterranean habitats, between 2012 and 2019. Generalized linear mixed models were used to assess the relationship between target taxa abundance, fire salamander larvae occurrence, and environmental features. The presence of salamander larvae negatively affected the abundance of all the target taxa. Monolistra abundance was positively related with the distance from the cave entrance of the sites and by their surface. Our study revealed that surface salamanders may have a negative effect on the abundance of cave-adapted animals, and highlited the importance of further investigations on the diet and on the top-down effects of salamanders on the subterranean communities.

Seasonal variation in the strength of interference competition among headwater stream predators

Abstract Vertebrate communities in headwater streams are assumed to be regulated through competitive and predatory interactions. Although documented predation is rare, studies regularly report competitive dominance by fish that, as larger competitors reliant on aquatic habitat, exclude semi‐aquatic salamanders to marginal stream habitat. However, it is unclear whether fish interact with stream‐breeding salamanders through indirect effects such as competition for resources (e.g. food or cover) or fear (i.e. threat of predation) nor is it known whether these interactions are consistent through time. This study used a novel caging approach to determine if competitive outcomes between a headwater fish and salamanders were regulated primarily through resource depletion (exploitative competition) or behavioural avoidance (interference competition). We paired banded sculpin (Cottus carolinae) and larval red salamanders (Pseudotriton ruber) of similar body size in independent flow through mesocosms with intra‐ and inter‐specific pairs allowed to interact physically or non‐physically. The experiment was repeated in the autumn and in the spring when stream salamander larvae begin to transform into terrestrial juveniles. Banded sculpin negatively influenced growth of red salamanders regardless of whether they were allowed to physically interact, suggesting interference competition and behavioural avoidance. This asymmetrical effect was strongest in the spring when salamanders underwent metamorphosis at higher rates in the presence of fish. However, in the autumn, the effects were more balanced between the two species with salamanders impacting fish through exploitative competition. By studying the temporal relationships between two competitors and using a caging method novel to competition studies, we established that the outcomes of competition are dependent on season and may vary in type relative to the timing of life‐history events. For this community, these results suggest that outcomes of competition are highly dependent on season and could indicate a biotic mechanism maintaining headwater salamander distributions through source–sink dynamics. Our results also suggest that, in this species interaction, it may be unwarranted to assume that the outcomes of competition at one time represent the complex relationships regulating community interactions.