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The significance of spatial memory for water finding in a tadpole-transporting frog.

ABSTRACT: The ability to associate environmental cues with valuable resources strongly increases the chances of finding them again, and thus memory often guides animal movement. For example, many temperate region amphibians show strong breeding site fidelity and will return to the same areas even after the ponds have been destroyed. In contrast, many tropical amphibians depend on exploitation of small, scattered and fluctuating resources such as ephemeral pools for reproduction. It remains unknown whether tropical amphibians rely on spatial memory for effective exploitation of their reproductive resources. Poison frogs (Dendrobatidae) routinely shuttle their tadpoles from terrestrial clutches to dispersed aquatic deposition sites. We investigated the role of spatial memory for relocating previously discovered deposition sites in an experimental population of the brilliant-thighed poison frog, Allobates femoralis, a species with predominantly male tadpole transport. We temporarily removed an array of artificial pools that served as the principal tadpole deposition resource for the population. In parallel, we set up an array of sham sites and sites containing conspecific tadpole odour cues. We then quantified the movement patterns and site preferences of tadpole-transporting males by intensive sampling of the area and tracking individual frogs. We found that tadpole-carrier movements were concentrated around the exact locations of removed pools and most individuals visited several removed pool sites. In addition, we found that tadpole-transporting frogs were attracted to novel sites that contained high concentrations of conspecific olfactory tadpole cues. Our results suggest that A. femoralis males rely heavily on spatial memory for efficient exploitation of multiple, widely dispersed deposition sites once they are discovered. Additionally, olfactory cues may facilitate the initial discovery of the new sites.

SUBMITTER: Pasukonis A

PROVIDER: S-EPMC5321284 | biostudies-literature | 2016 Jun

REPOSITORIES: biostudies-literature

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The significance of spatial memory for water finding in a tadpole-transporting frog.

Pašukonis Andrius A Trenkwalder Katharina K Ringler Max M Ringler Eva E Mangione Rosanna R Steininger Jolanda J Warrington Ian I Hödl Walter W

Animal behaviour 20160601

The ability to associate environmental cues with valuable resources strongly increases the chances of finding them again, and thus memory often guides animal movement. For example, many temperate region amphibians show strong breeding site fidelity and will return to the same areas even after the ponds have been destroyed. In contrast, many tropical amphibians depend on exploitation of small, scattered and fluctuating resources such as ephemeral pools for reproduction. It remains unknown whether ...[more]

PMID: 28239185

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Project description:Animals relying on uncertain, ephemeral and patchy resources have to regularly update their information about profitable sites. For many tropical amphibians, widespread, scattered breeding pools constitute such fluctuating resources. Among tropical amphibians, poison frogs (Dendrobatidae) exhibit some of the most complex spatial and parental behaviors-including territoriality and tadpole transport from terrestrial clutches to ephemeral aquatic deposition sites. Recent studies have revealed that poison frogs rely on spatial memory to successfully navigate through their environment. This raises the question of when and how these frogs gain information about the area and suitable reproductive resources. To investigate the spatial patterns of pool use and to reveal potential explorative behavior, we used telemetry to follow males of the territorial dendrobatid frog Allobates femoralis during tadpole transport and subsequent homing. To elicit exploration, we reduced resource availability experimentally by simulating desiccated deposition sites. We found that tadpole transport is strongly directed towards known deposition sites and that frogs take similar direct paths when returning to their home territory. Frogs move faster during tadpole transport than when homing after the deposition, which probably reflects different risks and costs during these two movement phases. We found no evidence for exploration, neither during transport nor homing, and independent of the availability of deposition sites. We suggest that prospecting during tadpole transport is too risky for the transported offspring as well as for the transporting male. Relying on spatial memory of multiple previously discovered pools appears to be the predominant and successful strategy for the exploitation of reproductive resources in A. femoralis. Our study provides for the first time a detailed description of poison frog movement patterns during tadpole transport and corroborates recent findings on the significance of spatial memory in poison frogs. When these frogs explore and discover new reproductive resources remains unknown.

Project description:UnlabelledRanaviruses (Iridoviridae) are posing an increasing threat to amphibian populations, with anuran tadpoles being particularly susceptible to these viral infections. Moreover, amphibians are the most basal phylogenetic class of vertebrates known to possess both type I and type III interferon (IFN)-mediated immunity. Moreover, little is known regarding the respective roles of the IFN mediators in amphibian antiviral defenses. Accordingly, we transcriptionally and functionally compared the amphibian Xenopus laevis type I (IFN) and III (IFN-λ) IFNs in the context of infections by the ranavirus frog virus 3 (FV3). X. laevis IFN and IFN-λ displayed distinct tissue expression profiles. In contrast to our previous findings that X. laevis tadpoles exhibit delayed and modest type I IFN responses to FV3 infections compared to the responses of adults, here we report that tadpoles mount timely and robust type III IFN gene responses. Recombinant forms of these cytokines (recombinant X. laevis IFN [rXlIFN] and rXlIFN-λ) elicited antiviral gene expression in the kidney-derived A6 cell line as well as in tadpole leukocytes and tissues. However, rXlIFN-λ was less effective than rXlIFN in preventing FV3 replication in A6 cells and tadpoles and inferior at promoting tadpole survival. Intriguingly, FV3 impaired A6 cell and tadpole kidney type III IFN receptor gene expression. Furthermore, in A6 cultures rXlIFN-λ conferred equal or greater protection than rXlIFN against recombinant viruses deficient for the putative immune evasion genes, the viral caspase activation and recruitment domain (vCARD) or a truncated vIF-2α gene. Thus, in contrast to previous assumptions, tadpoles possess intact antiviral defenses reliant on type III IFNs, which are overcome by FV3 pathogens.ImportanceAnuran tadpoles, including those of Xenopus laevis, are particularly susceptible to infection by ranavirus such as FV3. We investigated the respective roles of X. laevis type I and type III interferons (IFN and IFN-λ, respectively) during FV3 infections. Notably, tadpoles mounted timely and more robust IFN-λ gene expression responses to FV3 than adults, contrasting with the poorer tadpole type I IFN responses. However, a recombinant X. laevis IFN-λ (rXlIFN-λ) conferred less protection to tadpoles and the A6 cell line than rXlIFN, which may be explained by the FV3 impairment of IFN-λ receptor gene expression. The importance of IFN-λ in tadpole anti-FV3 defenses is underlined by the critical involvement of two putative immune evasion genes in FV3 resistance to IFN- and IFN-λ-mediated responses. These findings challenge the view that tadpoles have defective antiviral immunity and suggest, rather, that their antiviral responses are predominated by IFN-λ responses, which are overcome by FV3.

Dataset Information

The significance of spatial memory for water finding in a tadpole-transporting frog.

Publications

The significance of spatial memory for water finding in a tadpole-transporting frog.

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