High Desiccation Risk Research Articles

Developmental plasticity to desiccation risk in tadpoles of a tropical inselberg specialist

Developmental plasticity evolves in heterogeneous environmental conditions as long as individuals can accurately perceive them. A paradigmatic example of developmental plasticity is the ability of amphibian larvae to alter growth and development in response to the risk of pond drying. Such responses are often found in amphibian species breeding in highly dynamic water bodies with high desiccation risk. The inselbergs of the Guianan Shield are rocky outcrops with extremely high and fluctuating temperatures and a marked seasonality in precipitation. During the rainy season, eroded depressions form precipitation-dependent pools with a high and variable risk of desiccation within the timeframe of a few days. The frog Leptodactylus lithonaetes specializes in breeding in this extreme environment, and its tadpoles are thus forced to cope with desiccation risk by adjusting their developmental trajectories and physiological performance. We experimentally assessed the effect of different levels of desiccation risk, under controlled temperature conditions, on developmental rate, growth, and temperature-dependent locomotor performance in tadpoles of Leptodactylus lithonaetes. We did not find an effect of desiccation risk on developmental rate, but under simulated drying conditions, tadpoles showed larger body size, greater body mass, and enhanced locomotor performance compared to constant (high or low) water levels. These results suggest that drying pools offer cues that trigger developmental and behavioral changes in these tadpoles, enabling them to enhance growth over a short time span without accelerating development. We discuss the potential compensatory mechanisms behind these responses and highlight the need for further investigations in species with semiterrestrial life histories in extreme environments.

Inability of yellow‐bellied toad to accelerate metamorphosis in desiccation conditions

AbstractMany amphibian species inhabit temporary aquatic habitats for reproduction to maximize larval growth under favorable conditions, but accelerate developmental rate to rapidly undergo metamorphosis under stress conditions when high desiccation risk exists. Desiccation affects different aspects of amphibian biology such as developmental rate, body size and mass, and growth rate. We studied the responses of yellow‐bellied toad (Bombina variegata) to different water levels (constant high, decreasing water level, and constant low water level) in the laboratory using individuals collected from natural ponds. To assess the effects of experimental pond drying, we investigated the effects on life‐history and morphological traits at metamorphosis as well as carry‐over effects on post‐metamorphic traits and locomotor performances. We found that B. variegata cannot accelerate developmental rate in response to pond drying. The metamorphs from decreasing and constant low water levels had similar size, mass, growth rate and body condition indices at metamorphosis, and all these traits were lower than in the constant high water level treatment. These changes in life‐history traits at metamorphosis did not affect tail shape although they had carry‐over effects on life‐history and morphological traits after metamorphosis. Post‐metamorphic individuals reared in desiccation treatments had similar but smaller lengths of femur and tibiofibula, but these changes did not have negative consequences on jumping performances. We show that responsiveness to pond drying of B. variegata is probably associated with maximum growth rate in favorable conditions and inability to increase growth rate as well as developmental rate in desiccation conditions. This resulted in prolonged developmental time to reach the minimum size and mass for metamorphosis.

Pool choice in a vertical landscape: Tadpole-rearing site flexibility in phytotelm-breeding frogs.

Many species of Neotropical frogs have evolved to deposit their tadpoles in small water bodies inside plant structures called phytotelmata. These pools are small enough to exclude large predators but have limited nutrients and high desiccation risk. Here, we explore phytotelm use by three common Neotropical species: Osteocephalus oophagus, an arboreal frog that periodically feeds eggs to its tadpoles; Dendrobates tinctorius, a tadpole‐transporting poison frog with cannibalistic tadpoles; and Allobates femoralis, a terrestrial tadpole‐transporting poison frog with omnivorous tadpoles. We found that D. tinctorius occupies pools across the chemical and vertical gradient, whereas A. femoralis and O. oophagus appear to have narrower deposition options that are restricted primarily by pool height, water capacity, alkalinity, and salinity. Dendrobates tinctorius tadpoles are particularly flexible and can survive in a wide range of chemical, physical, and biological conditions, whereas O. oophagus seems to prefer small, clear pools and A. femoralis occupies medium‐sized pools with abundant leaf litter and low salinity. Together, these results show the possible niche partitioning of phytotelmata among frogs and provide insight into stressors and resilience of phytotelm breeders.

Better desiccated than eaten by fish: Distribution of anurans among habitats with different risks to offspring

Abstract Freshwater species with complex life cycles face a trade‐off between the risks of offspring mortality due to desiccation in temporary habitats and due to predators common in long‐duration habitats, especially fish. In real‐world conditions, intermediate‐gradient areas that are highly suitable for some ecological specialists are often limited. I examined the relative significance of drivers of the permanence–predation gradient in habitat selection by pond‐breeding anurans. Anuran oviposition was investigated at the community level in fish pond landscapes with only three types of habitat, permanent fish‐containing ponds and highly desiccation‐prone pools, either fishless or recently emptied of fish and with fish odour (fish cue). Altogether, 65 ponds/pools, interspersed in four clusters, were examined for the presence of egg masses. Bufo bufo was the only species preferring permanent ponds. Egg masses of Rana sp. (Rana arvalis/Rana temporaria) occurred in all fishless pools, and less frequently in the ponds. Bufotes viridis and long larval period species Pelobates fuscus and Hyla orientalis oviposited almost exclusively in fishless pools. Fish‐cue pools were avoided by all species. Anuran richness was higher in fishless pools than in permanent ponds. Species distribution between the two habitats was nested, with both common and rare species occurring in fishless pools. The results indicate the primacy of offspring predation risk over hydroperiod constraints in oviposition decision‐making by fish‐intolerant anurans. The absence of some species from ponds and pools with fish or fish cues shows that non‐consumptive interactions may better explain the scarcity of anuran larvae in waters dominated by fish than actual consumption. The strict avoidance of fish habitats despite their proximity to fishless patches indicates fine‐scale assessment of predation risk. However, rigid habitat selection against fish predation on offspring may prove maladaptive if habitats with high desiccation risk are the main alternative and are indiscriminately preferred. Maintenance of fishless wetlands with a hydroperiod sufficient to allow completion of metamorphosis should be a conservation priority for anuran diversity in areas where fishless habitats are limited.

Effect of predator cue on escape and oviposition behaviour of freshwater snail

Abstract When suitability of sites for parent is incompatible with that for their eggs, parent–offspring conflict occurs — the parent must choose between the optimal oviposition site for eggs and that suitable for itself. We examined effects of predator cue on parental habitat use and oviposition site in Physa acuta. We assessed desiccation risk in eggs and the relationship between water depth and predation risk. Predator cues induced the elevation of parental habitat away from the bottom but had no effect on the oviposition site. Oviposition site choice is not by-product of escape response. Eggs that were exposed to desiccation failed to hatch, indicating high desiccation risk. Eggs laid at deeper levels were at higher risk of stripping from oviposition substrates by crayfishes. Although the middle-water level would be suitable oviposition sites, the parents selected an oviposition site in the upper level. There are other benefits and costs of oviposition site selection.

Do biomass harvesting guidelines influence herpetofauna following harvests of logging residues for renewable energy?

Forests are a major supplier of renewable energy; however, gleaning logging residues for use as woody biomass feedstock could negatively alter habitat for species dependent on downed wood. Biomass Harvesting Guidelines (BHGs) recommend retaining a portion of woody biomass on the forest floor following harvest. Despite BHGs being developed to help ensure ecological sustainability, their contribution to biodiversity has not been evaluated experimentally at operational scales. We compared herpetofauanal evenness, diversity, and richness and abundance of Anaxyrus terrestris and Gastrophryne carolinensis among six treatments that varied in volume and spatial arrangement of woody biomass retained after clearcutting loblolly pine (Pinus taeda) plantations in North Carolina, USA (n = 4), 2011-2014 and Georgia (n = 4), USA 2011-2013. Treatments were: (1) biomass harvest with no BHGs, (2) 15% retention with biomass clustered, (3) 15% retention with biomass dispersed, (4) 30% retention with biomass clustered, (5) 30% retention with biomass dispersed, and (6) no biomass harvest. We captured individuals with drift fence arrays and compared evenness, diversity, and richness metrics among treatments with repeated-measure, linear mixed-effects models. We determined predictors of A. terrestris and G. carolinensis abundances using a priori candidate N-mixture models with woody biomass volume, vegetation structure, and groundcover composition as covariates. We had 206 captures of 25 reptile species and 8710 captures of 17 amphibian species during 53690 trap nights. Herpetofauna diversity, evenness, and richness were similar among treatments. A. terrestris abundance was negatively related to volume of retained woody biomass in treatment units in North Carolina in 2013. G. carolinensis abundance was positively related with volume of retained woody debris in treatment units in Georgia in 2012. Other relationships between A. terrestris and G. carolinensis abundances and habitat metrics were weak or absent. The lack of consistent community or population responses suggests the addition of a woody biomass harvest to a clearcut in pine plantations does not impact herpetofauna use of Coastal Plain loblolly plantations in the southeastern United States. We recommend additional research to examine relationships between woody biomass harvesting and rarer species or amphibians with high desiccation risk, particularly in other regions and harvesting systems.

Alternative intrapopulation life‐history strategies and their trade‐offs in an African annual fish

In ephemeral habitats, the same genotypes cope with unpredictable environmental conditions, favouring the evolution of developmental plasticity and alternative life-history strategies (ALHS). We tested the existence of intrapopulation ALHS in an annual killifish, Nothobranchius furzeri, inhabiting temporary pools. The pools are either primary (persisting throughout the whole rainy season) or secondary (refilled after desiccation of the initial pool), representing alternative niches. The unpredictable conditions led to the evolution of reproductive bet-hedging with asynchronous embryonic development. We used a common garden experiment to test whether the duration of embryonic period is associated with post-embryonic life-history traits. Fish with rapid embryonic development (secondary pool strategy, high risk of desiccation) produced phenotypes with more rapid life-history traits than fish with slow embryonic development (primary pool strategy). The fast fish were smaller at hatching but had larger yolk sac reserves. Their post-hatching growth was more rapid, and they matured earlier. Further, fast fish grew to a smaller body size and died earlier than slow fish. No differences in fecundity, propensity to mate or physiological ageing were found, demonstrating a combination of plastic responses and constraints. Such developmentally related within-population plasticity in life history is exceptional among vertebrates.

Discontinuous Gas Exchange, Water Loss, and Metabolism inProtaetia cretica(Cetoniinae, Scarabaeidae)

Insects are at high risk of desiccation because of their small size, high surface-area-to-volume ratio, and air-filled tracheal system that ramifies throughout their bodies to transport O(2) and CO(2) to and from respiring cells. Although the tracheal system offers a high-conductance pathway for the movement of respiratory gases, it has the unintended consequence of allowing respiratory transpiration to the atmosphere. When resting, many species exchange respiratory gases discontinuously, and an early hypothesis for the origin of these discontinuous gas exchange cycles (DGCs) is that they serve to reduce respiratory water loss. In this study, we test this "hygric" hypothesis by comparing rates of CO(2) exchange and water loss among flower beetles Protaetia cretica (Cetoniinae, Scarabaeidae) breathing either continuously or discontinuously. We show that, consistent with the expectations of the hygric hypothesis, rates of total water loss are higher during continuous gas exchange than during discontinuous gas exchange and that the ratio of respiratory water loss to CO(2) exchange is lower during discontinuous gas exchange. This conclusion is in agreement with other studies of beetles and cockroaches that also support the hygric hypothesis. However, this result does not exclude other adaptive hypotheses supported by work on ants and moth pupae. This ambiguity may arise because there are multiple independent evolutionary origins of DGCs and no single adaptive function underlying their genesis. Alternatively, the observed reduction in water loss during DGCs may be a side effect of a nonadaptive gas exchange pattern that is elicited during periods of inactivity.

Variable reproductive strategies of an African savanna frog, Phrynomantis microps (Amphibia, Anura, Microhylidae)

Abstract:West African savannas are habitats with unpredictable rainfall. Species with varying life-history traits may be more successful in these environments than species with fixed traits. We studied the reproduction strategies of the microhylid frog Phrynomantis microps in different savanna types, a humid savanna in Ivory Coast and a drier one in Benin. We recorded 5437 clutches in eight ponds in the humid savanna during five consecutive rainy seasons. A further 694 clutches were investigated in 10 ponds in Benin in one rainy season. For each clutch, we recorded egg numbers, deposition time, location within the pond and rainfall. Precipitation was important in triggering reproduction. However, the amount of rainfall needed differed in relation to rainy season length and total annual rainfall. Especially in years and regions with a late rainy season a threshold of minimum precipitation was needed to initiate spawning, indicating a trade-off between the need to reproduce and the survival probabilities of offspring in ponds with a high desiccation risk. Egg numbers per clutch further differed between pond sizes, breeding season length, as well as to time within the rainy season. Potential explanations for these differences, in particular desiccation and predation risks are discussed, but need further experimental support.

Diet Composition and Overlap between Recently Metamorphosed Rana areolata and Rana sphenocephala: Implications for a Frog of Conservation Concern

Interspecific competition for resources is predicted to be high in dense populations of closely related species and should lead either to species partitioning resources along one or more niche axes, or exclusion of the competitively inferior species. Between 19 June and 19 July 2003, we collected 71 recently metamorphosed Rana areolata (Crawfish Frogs) and 69 recently metamorphosed R. sphenocephala (Southern Leopard Frogs) from a single pond in northeastern Oklahoma and compared their morphology and diet. We found that recently metamorphosed R. areolata and R. sphenocephala are morphologically similar. Further, diets of both species were similar: hemipterans predominated, prey items were similarly sized, and dietary niche breadths overlapped, but R. areolata had significantly lower volumes of prey in their stomachs. Because of the high risk of desiccation, especially in Great Plains populations, newly metamorphosed Rana are not expected to disperse far from their natal ponds. During this first season, Rana also experience rapid growth. Dietary restrictions directly influence growth rate, which in turn are known to have major consequences during later life stages, ultimately affecting fitness. Rana areolata is a species of conservation concern across its range. Competitive interactions with other species of Rana have been proposed to be contributing to declines in R. areolata. Our results indicate that competitive interactions with R. sphenocephala have the potential to negatively affect prey consumption, and ultimately fitness, in R. areolata.

The reproduction of the Apennine yellow-bellied toad (Bombina pachypus) in central Italy

AbstractAmphibians are declining worldwide and many species are threatened for unknown reasons. In fact, information on ecology of several species are not available due to the lack of studies. The Apennine yellow-bellied toad (Bombina pachypus) is an Italian endemic species in progressive decline in many areas, often for unclear reasons. A two-year study of 116 temporary ponds in a grazing area of the Majella National Park (central Italy) from 2001 to 2002 revealed that: (a) Apennine yellow-bellied toads reproduced in small ponds characterized by high desiccation risk; (b) breeding activity occurred for a prolonged period (at least from May to the beginning of August), during which females spawned clutches of very few eggs in several, successive events; (c) the reproductive success was very low especially because of high egg mortality; and (d) the main cause of mortality was the desiccation of ponds. Consequently, the characteristics of breeding areas (i.e., small, ephemeral ponds) are the most important feature influencing the reproduction. The safeguard of temporary ponds is crucial for the conservation of this amphibian and could preserve also the other species using these pools.

Evaluation of Rhizobium inoculant formulations for alfalfa yield and N fixation

Because of its small seed size, alfalfa (Medicago sativa L.) typically is seeded at a shallow depth, putting Rhizobium inoculated onto the seed coat at a high risk of desiccation. Granular inoculants may provide a superior delivery formulation for Rhizobium because the inoculant can be placed deeper in the soil than the seed, where it is protected from desiccation. Sinorhizobium meliloti cv. Beaver delivered as (1) pre-inoculated alfalfa seed from the inoculant manufacturer, (2) commercial peat-based, self-sticking inoculant applied on-site, and (3) granular inoculant placed with the seed or (4) banded below and to the side of the seed was evaluated against uninoculated alfalfa controls at three field sites in Saskatchewan. Overall, alfalfa inoculated with the granular formulation placed below and to the side of the alfalfa seed was among the highest biomass producer in the establishment year, although it did not exhibit superior nodulation or biological N fixation compared with the other treatments. Any advantage conferred by the granular inoculant in the establishment year did not persist through the first and second production years. Under the conditions of this study, the delivery formulation had no long-term affect on alfalfa productivity, nodulation and biological N fixation. Furthermore, none of the inoculant treatments were consistently superior to the uninoculated controls. Key words: Alfalfa, granular inoculant, peat inoculant, pre-inoculated seed, Medicago sativa L., Sinorhizobium meliloti

Evolutionary significance of oral morphology in the carnivorous tadpoles of tiger frogs, genus Hoplobatrachus (Ranidae)

We describe the larval stages of three species of the Asian-African tiger frogs Hoplobatrachus chinensis, H. occipitalis and H. tigerinus. The tadpoles of all three species are very similar, with peculiar oral features: (1) double rows of needle-like labial teeth, (2) strong emarginations on the large jaw sheaths and (3) keratinized spurs on the buccal floor. Characters 1 and 2 (and perhaps 3) are probably related to the carnivorous habits of these tadpoles. A molecular phylogeny based on 2430 base pairs of two nuclear and four mitochondrial genes corroborated monophyly of Asian and African Hoplobatrachus, and identified Euphlyctis as their sister group. Tadpoles of the latter genus lack buccal spurs and double labial tooth rows but share large jaw sheaths, the upper with a medial projection. Therefore, the common ancestor of Euphlyctis and Hoplobatrachus probably was also characterized by this state, and may have been facultatively carnivorous. Further carnivorous specializations in Hoplobatrachus could explain why tiger frogs have been so successful in populating arid environments where ponds are at high risk of desiccation. Larval morphology may prove to be the key innovation which enabled them to disperse, in the Late Cenozoic, into their current very wide distribution area in Asia and Africa. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 81, 171–181.