Whole animal measurements of shear and adhesive forces in adult tree frogs: insights into underlying mechanisms of adhesion obtained from studying the effects of size and scale

This allometric study of adhesion in 15 Trinidadian tree frog species investigates how relationships between length, area and mass limit the ability of adult frog species of different sizes to adhere to inclined and overhanging surfaces. Our experiments show that hylid frogs possess an area-based wet adhesive system in which larger species are lighter than expected from isometry and adhere better than expected from their toe pad area. However, in spite of these adaptations, larger species adhere less well than smaller species. In addition to these adhesive forces, tree frogs also generate significant shear forces that scale with mass, suggesting that they are frictional forces. Toe pads detach by peeling and frogs have strategies to prevent peeling from taking place while they are adhering to surfaces, including orienting themselves head-up on slopes. The scaling of tree frog adhesion is also used to distinguish between different models for adhesion, including classic formulae for capillarity and Stefan adhesion. These classic equations grossly overestimate the adhesive forces that tree frogs produce. More promising are peeling models, designed to predict the pull-off forces of adhesive tape. However, more work is required before we can qualitatively and quantitatively describe the adhesive mechanism of tree frogs.     

Structural correlates of increased adhesive efficiency with adult size in the toe pads of hylid tree frogs

Tree frogs are able to climb smooth, vertical substrates using specialised toe pads which adhere via an area-based wet adhesive mechanism. Although the link between pads and arboreality in frogs is well-established, few studies have investigated the influence of morphology on adhesion. Trinidadian tree frogs from the genus Hyla are geometrically similar. There is a tendency towards comparatively reduced mass in larger species, but toe pad area increases as expected with isometry. As adhesion is area-dependent, forces are affected directly by the increase in mass relative to pad area, and there is a decrease in the ability of larger species to adhere to smooth rotation platforms. However, there is an increase in force per unit area that suggests larger species have more efficient toe pads. Toe pad structure is very similar though there are variations in the details of a number of features. Crucially, although differences in morphology appeared small they had demonstrable effects on adhesive efficiency of the pads. Epithelial cell area correlates positively with frog length and adhesive efficiency, related features of cell density and intercellular channel length correlate negatively. These findings are discussed in relation to the different forces involved in the tree frogs’ wet adhesive system.     

Competing tadpoles: Australian native frogs affect invasive cane toads (Rhinella marina) in natural waterbodies

The cane toad (Rhinella marina) is one of the most successful invasive species worldwide, and has caused significant negative impacts on Australian fauna. Experimental work in the laboratory and in mesocosms has shown that tadpoles of native frogs can affect survival, size at metamorphosis and duration of larval period of cane toad tadpoles. To test if these effects occur in nature, we conducted a field experiment using two temporary ponds where we set up enclosures with tadpoles of native green tree frogs (Litoria caerulea) and cane toads in treatments with a range of densities and combinations. The presence of green tree frog tadpoles significantly decreased the growth rate of toad tadpoles and increased the duration of their larval period in both ponds; in one pond, frog tadpoles also significantly reduced the body length and mass of metamorph toads. Toad tadpoles did not have any significant negative effects on green tree frog tadpoles, but there was strong intraspecific competition within the latter species: increased frog tadpole density resulted in increased larval period and reduced survival, growth rate and size at metamorphosis for frogs at one or both ponds. Our results are encouraging for the possibility of using native frogs as one component of an integrated approach to the biological control of cane toads.     

Geckos as Springs: Mechanics Explain Across-Species Scaling of Adhesion

One of the central controversies regarding the evolution of adhesion concerns how adhesive force scales as animals change in size, either among or within species. A widely held view is that as animals become larger, the primary mechanism that enables them to climb is increasing pad area. However, prior studies show that much of the variation in maximum adhesive force remains unexplained, even when area is accounted for. We tested the hypothesis that maximum adhesive force among pad-bearing gecko species is not solely dictated by toepad area, but also depends on the ratio of toepad area to gecko adhesive system compliance in the loading direction, where compliance (C) is the change in extension (Δ) relative to a change in force (F) while loading a gecko’s adhesive system (C = dΔ/dF). Geckos are well-known for their ability to climb on a range of vertical and overhanging surfaces, and range in mass from several grams to over 300 grams, yet little is understood of the factors that enable adhesion to scale with body size. We examined the maximum adhesive force of six gecko species that vary in body size (~2–100 g). We also examined changes between juveniles and adults within a single species (Phelsuma grandis). We found that maximum adhesive force and toepad area increased with increasing gecko size, and that as gecko species become larger, their adhesive systems become significantly less compliant. Additionally, our hypothesis was supported, as the best predictor of maximum adhesive force was not toepad area or compliance alone, but the ratio of toepad area to compliance. We verified this result using a synthetic “model gecko” system comprised of synthetic adhesive pads attached to a glass substrate and a synthetic tendon (mechanical spring) of finite stiffness. Our data indicate that increases in toepad area as geckos become larger cannot fully account for increased adhesive abilities, and decreased compliance must be included to explain the scaling of adhesion in animals with dry adhesion systems.     

Canopy Closure,Competition, and the Endangered Dusky Gopher Frog

Abstract: A major challenge facing wildlife biologists is understanding why some species go extinct while others persist in the same habitat. To address this question, we investigated whether tree canopy closure over ponds affects growth and survival of rare and common tadpoles within ponds and mediates competitive interactions among species. We conducted 2 experiments to test whether canopy closure and competition may have contributed to the decline of the endangered dusky gopher frog (Rana sevosa), but allowed the persistence of the southern leopard frog (R. sphenocephala). We explored the response of both species to canopy closure in single-species and mixed- (1:1) species treatments of identical total tadpole density. An experiment using aquatic enclosures in temporary ponds showed that canopy closure reduced tadpole growth approximately 20% for both species. Survival of dusky gopher frog tadpoles was higher in mixed-species enclosures than in single-species enclosures. In a complementary experiment using artificial ponds, dusky gopher frogs had lower survival to metamorphosis, reduced size at metamorphosis, and produced a lower total biomass of metamorphosed juveniles in shaded ponds. Southern leopard frogs exhibited reduced body size at metamorphosis only when shaded. These studies suggest that pond canopy closure, not larval competition, may be contributing to the decline of the dusky gopher frog. The different responses to canopy closure suggest a potential mechanism for the loss of dusky gopher frogs and the persistence of southern leopard frogs. Removal of trees from historically open-canopy ponds may help facilitate the recovery of dusky gopher frogs and benefit similar species.     

Dual impacts of climate change: forest migration and turnover through life history

Tree species are predicted to track future climate by shifting their geographic distributions, but climate‐mediated migrations are not apparent in a recent continental‐scale analysis. To better understand the mechanisms of a possible migration lag, we analyzed relative recruitment patterns by comparing juvenile and adult tree abundances in climate space. One would expect relative recruitment to be higher in cold and dry climates as a result of tree migration with juveniles located further poleward than adults. Alternatively, relative recruitment could be higher in warm and wet climates as a result of higher tree population turnover with increased temperature and precipitation. Using the USDA Forest Service's Forest Inventory and Analysis data at regional scales, we jointly modeled juvenile and adult abundance distributions for 65 tree species in climate space of the eastern United States. We directly compared the optimal climate conditions for juveniles and adults, identified the climates where each species has high relative recruitment, and synthesized relative recruitment patterns across species. Results suggest that for 77% and 83% of the tree species, juveniles have higher optimal temperature and optimal precipitation, respectively, than adults. Across species, the relative recruitment pattern is dominated by relatively more abundant juveniles than adults in warm and wet climates. These different abundance‐climate responses through life history are consistent with faster population turnover and inconsistent with the geographic trend of large‐scale tree migration. Taken together, this juvenile–adult analysis suggests that tree species might respond to climate change by having faster turnover as dynamics accelerate with longer growing seasons and higher temperatures, before there is evidence of poleward migration at biogeographic scales.     

Adhesive Contact in Animal: Morphology, Mechanism and Bio-Inspired Application

Many animals possess adhesive pads on their feet,which are able to attach to various substrates while controlling adhesive forces during locomotion.This review article studies the morphology of adhesive devices in animals,and the physical mechanisms of wet adhesion and dry adhesion.The adhesive pads are either ‘smooth' or densely covered with special adhesive setae.Smooth pads adhere by wet adhesion,which is facilitated by fluid secreted from the pads,whereas hairy pads can adhere by dry adhesion or wet adhesion.Contact area,distance between pad and substrate,viscosity and surface tension of the liquid filling the gap between pad and substrate are the most important factors which determine the wet adhesion.Dry adhesion was found only in hairy pads,which occurs in geckos and spiders.It was demonstrated that van der Waals interaction is the dominant adhesive force in geckos' adhesion.The bio-inspired applications derived from adhesive pads are also reviewed.     

浙江丽水虎纹蛙形态特征的两性异形和食性

用数显游标卡尺测量了407只2001—2003年9月下旬至10月上旬浙江丽水罚没的死亡虎纹蛙的体长等10个形态指标,结果表明:雌性成体体长(SUL)大于雄性成体,幼体形态无显著两性差异;ANCOVA去除SUL差异的影响后,雌性成体的头长和后肢长大于雄性成体,前肢长、眼径和耳径则小于雄性成体。前肢两侧对称性的偏移度成体大于幼体,雌性大于雄性;后肢两侧对称性成幼体和两性无显著差异。10个形态指标主成分分析的前三个主成分共解释64·6%的变异:第一主成分中头宽、眼径和耳径,第二主成分中后肢长,第三主成分中眼间距和鼻间距分别有较高的正负载系数。用NikonSMZ-1000解剖镜鉴别277只个体胃内容物中的食物种类,发现其秋季食物以节肢动物为主;成幼体和两性食物生态位宽度为3·42~5·25,食物生态位重叠度较高为0·93~0·98。分析表明,虎纹蛙局部形态特征的两性差异微弱,而体长两性异形差异显著;雌体具有较大的体形与食性无关,而可能与生育力选择的作用有关。     

Enigmas of Pterorhodin,a Red Melanosomal Pigment of Tree Frogs

Melanosomes observed in dermal melanophores of adult leaf frogs contain a unique wine red pigment identified as pterorhodin, a pteridine dimer never before found in any vertebrate. This type of melanosome, almost twice as large as the typical eumelanin melanosome, contains a small electron dense core of eumelanin surrounded by a concentric fibrous mass of pterorhodin. Dermal melanophores of larval leaf frogs contain small eumelanin melanosomes that transform at metamorphosis through the gradual accumulation of pterorhodin on the eumelanin surface to form the compound melanosomes of adults. This process may be mediated by thyroxine. No explanation for the unique presence of pterorhodin in leaf frogs has yet surfaced. A variety of tree frog species from Australia and Papua New Guinea also possess pterorhodin and the large melanosome suggesting that tree frogs from the New World and those from Australia are closely related and may have been separated during continental drift. Several of the unsolved problems posed by the emergence of pterorhodin in a unique melanosome are discussed.     

Enigmas of pterorhodin,a red melanosomal pigment of tree frogs

Melanosomes observed in dermal melanophores of adult leaf frogs contain a unique wine red pigment identified as pterorhodin, a pteridine dimer never before found in any vertebrate. This type of melanosome, almost twice as large as the typical eumelanin melanosome, contains a small electron dense core of eumelanin surrounded by a concentric fibrous mass of pterorhodin. Dermal melanophores of larval leaf frogs contain small eumelanin melanosomes that transform at metamorphosis through the gradual accumulation of pterorhodin on the eumelanin surface to form the compound melanosomes of adults. This process may be mediated by thyroxine. No explanation for the unique presence of pterorhodin in leaf frogs has yet surfaced. A variety of tree frog species from Australia and Papua New Guinea also possess pterorhodin and the large melanosome suggesting that tree frogs from the New World and those from Australia are closely related and may have been separated during continental drift. Several of the unsolved problems posed by the emergence of pterorhodin in a unique melanosome are discussed.     

Insular shifts in body size of rice frogs in the Zhoushan Archipelago, China

1. Differences in body size between mainland and island populations have been reported for reptiles, birds and mammals. Despite widespread recognition of insular shifts in body size in these taxa, there have been no reports of such body size shifts in amphibians. 2. We provide the first evidence of an insular shift in body size for an amphibian species, the rice frog Rana limnocharis. We found significant increases in body size of rice frogs on most sampled islands in the Zhoushan archipelago when compared with neighbouring mainland China. 3. Large body size in rice frogs on islands was significantly related to increased population density, in both breeding and non-breeding seasons. Increases in rice frog density were significantly related to higher resource availability on islands. Increased resource availability on islands has led to higher carrying capacities, which has subsequently facilitated higher densities and individual growth rates, resulting in larger body size in rice frogs. We also suggest that large body size has evolved on islands, as larger individuals are competitively superior under conditions of harsh intraspecific competition at high densities. 4. Increases in body size in rice frogs were not related to several factors that have been implicated previously in insular shifts in body size in other taxa. We found no significant relationships between body size of rice frogs and prey size, number of larger or smaller frog species, island area or distance of islands from the mainland. 5. Our findings contribute to the formation of a broad, repeatable ecological generality for insular shifts in body size across a range of terrestrial vertebrate taxa, and provide support for recent theoretical work concerning the importance of resource availability for insular shifts in body size.     

Helminth infracommunities of the frogs Rana catesbeiana and Rana clamitans from Turkey Marsh, Michigan

One hundred twenty-seven bullfrogs, Rana catesbeiana, and 120 green frogs, Rana clamitans, collected in July and August 1987 from Turkey Marsh, Michigan, were examined for helminths. Of the 16 helminth species found, Falcaustra catesbeianae had the highest prevalence and mean intensity in bullfrogs. In green frogs, Megalodiscus temperatus had the highest prevalence and Haematoloechus parviplexus had the highest mean intensity. Taxonomically, 1,030 (30.5%) trematodes and 2,348 (69.5%) nematodes occurred in bullfrogs; 2,874 (96.4%) trematodes, 2 (0.1%) cestodes, and 105 (3.5%) nematodes were found in green frogs. The larger and more aquatic of the 2 hosts, R. catesbeiana, had the highest mean number of helminth species, helminth intensity, diversity, and evenness. Adult frogs of both species had a significantly higher mean number of helminth species than did juveniles. Significant correlations existed between the number of helminth species and frog length. Although the helminth communities of Turkey Marsh frogs are isolationist in character, they are more diverse than other helminth communities studied in amphibians.     

Effects of terrestrial buffer zones on amphibians on golf courses

A major cause of amphibian declines worldwide is habitat destruction or alteration. Public green spaces, such as golf courses and parks, could serve as safe havens to curb the effects of habitat loss if managed in ways to bolster local amphibian communities. We reared larval Blanchard's cricket frogs (Acris blanchardi) and green frogs (Rana clamitans) in golf course ponds with and without 1 m terrestrial buffer zones, and released marked cricket frog metamorphs at the golf course ponds they were reared in. Larval survival of both species was affected by the presence of a buffer zone, with increased survival for cricket frogs and decreased survival for green frogs when reared in ponds with buffer zones. No marked cricket frog juveniles were recovered at any golf course pond in the following year, suggesting that most animals died or migrated. In a separate study, we released cricket frogs in a terrestrial pen and allowed them to choose between mown and unmown grass. Cricket frogs had a greater probability of using unmown versus mown grass. Our results suggest that incorporating buffer zones around ponds can offer suitable habitat for some amphibian species and can improve the quality of the aquatic environment for some sensitive local amphibians.     

Specificity of cell adhesion: differences between normal and hybrid sea urchin cells.

The adhesive specificity of embryonic sea urchin cells from two species, and the two hybrid crosses between these species was examined by a cell-aggregate collection assay. Cells of normal Lytechinus or Tripneustes embryos were found to adhere to homospecific cell aggregates at a much higher rate than they would adhere to heterospecific aggregates. Hybrid cells adhered to collecting aggregates at an intermediate rate. The observed pattern of hybrid cell adhesion suggested that paternal gene products are capable of modifying cell surface adhesive sites as early as the mesenchyme blastula stage.     

Habitat-mediated impact of alien mink predation on common frog densities in the outer archipelago of the Baltic Sea

Alien predators have been recognised as one possible cause for amphibian declines around the world, but little is known of habitat-mediated predation impacts especially on adult amphibians. We studied common frog Rana temporaria under American mink Mustela vison predation in the outer archipelago of the Baltic Sea, south-western Finland. Using egg batches as an index of breeding frog female numbers we compared frog numbers and densities between a large, long-term mink-removal area and a comparable control area. Frog numbers in the removal area were at least 2.7-fold higher than those in the control area. In the presence of mink, frog densities increased with the amount of vegetation cover on the islands, indicating that mink predation affected frog densities especially on less-vegetated islands. An opposite trend appeared to be true for frogs in the mink-removal area, where other predators like snakes could induce a decline of frog densities on more vegetated islands. Shrub or grass vegetation seems to provide frogs shelter against alien mink predation. Our result highlights the importance of landscape-level habitat management as a conservation tool for amphibian populations.     

Condensation onto the skin as a means for water gain by tree frogs in tropical Australia

Green tree frogs, Litoria caerulea, in the wet-dry tropics of northern Australia remain active during the dry season with apparently no available water and temperatures that approach their lower critical temperature. We hypothesized that this surprising activity might be because frogs that are cooled during nighttime activity gain water from condensation by returning to a warm, humid tree hollow. We measured the mass gained when a cool frog moved into either a natural or an artificial hollow. In both hollows, water condensed on cool L. caerulea, resulting in water gains of up to 0.93% of body mass. We estimated that the water gained was more than the water that would be lost to evaporation during activity. The use of condensation as a means for water gain may be a significant source of water uptake for species like L. caerulea that occur in areas where free water is unavailable over extended periods.     

Predicting population trends from size distributions: a direct test in a tropical tree community

ABSTRACT Forest ecologists often evaluate how well the species composition of saplings in the understory matches that of the canopy: absence of juveniles suggests that a tree species is suffering population decline. Here we offer a theoretical and empirical test of this assertion using data from a 50-ha census plot in Panama. Theory indicates that higher rates of population change, lambda, lead to more steeply declining size distributions (more juveniles relative to adults). But other parameters also affect the size distribution: lower growth rate of juveniles and lower survival at any size pro duce more steeply declining size distributions as well. Empirical evaluation of 216 tree populations showed that juvenile growth was the strongest predictor of size distribution, in the direction predicted by theory. Size distribution did correlate with population growth, but weakly and only in understory species, not canopy seecies. Size distribution did not correlate with the growth rate of larger individuals nor with survival. Results suggest that static in formation on the size distribution is not a good predictor of future population trends, while demographic information is. Fast-growing species will have fewer juveniles in the understory than slow growing species, even when population growth is equal.     

Small frogs get their worms first: the role of nonodonate arthropods in the recruitment of Haematoloechus coloradensis and Haematoloechus complexus in newly metamorphosed northern leopard frogs, Rana pipiens, and woodhouse's toads, Bufo woodhousii

Studies on the life cycles and epizootiology of North American frog lung flukes indicate that most species utilize odonates as second intermediate hosts; adult frogs become infected by ingesting odonate intermediate hosts. Newly metamorphosed frogs are rarely infected with these parasites, predominantly because they are gape-limited predators that cannot feed on large intermediate hosts such as dragonflies. We examined the role of the frog diet and potential intermediate hosts in the recruitment of the frog lung fluke, Haematoloechus coloradensis, to metamorphosed northern leopard frogs (Rana pipiens), Woodhouse's toads (Bufo woodhousii), and bullfrogs (Rana catesbeiana) from western Nebraska. Because of the uncertain validity of H. coloradensis as a distinct species from Haematoloechus complexus, morphological characters of both species were reevaluated and the life cycles of both species were completed in the laboratory. The morphological data on H. coloradensis and H. coimplexus indicate that they differ in their oral sucker to pharynx ratio, uterine loop distribution, and placement of vitelline follicles. However, in terms of their life cycles, both species are quite similar in their use of physid snails as first intermediate hosts, a wide range of nonodonate and odonate arthropods as second intermediate hosts, and leopard frogs and toads as definitive hosts. These results indicate that H. coloradensis and H. complexus are generalists at the second intermediate host level and might be able to infect newly metamorphosed leopard frogs and toads by using small nonodonate arthropods more commonly than other frog lung fluke species. Comparisons of population structure of adult flukes in newly metamorphosed leopard frogs indicate that the generalist nature of H. coloradensis metacercariae enables it to colonize young of the year leopard frogs more commonly than other Haematoloechus spp. that only use odonates as second intermediate hosts. In this respect, the generalist nature of H. coloradensis and H. complexus at the second intermediate host level is an avenue for the colonization of young of year frogs.     

Size-dependent colouration balances conspicuous aposematism and camouflage

Colour is an important component of many different defensive strategies, but signal efficacy and detectability will also depend on the size of the coloured structures, and how pattern size interacts with the background. Consequently, size-dependent changes in colouration are common among many different species as juveniles and adults frequently use colour for different purposes in different environmental contexts. A widespread strategy in many species is switching from crypsis to conspicuous aposematic signalling as increasing body size can reduce the efficacy of camouflage, while other antipredator defences may strengthen. Curiously, despite being chemically defended, the gold-striped frog (Lithodytes lineatus, Leptodactylidae) appears to do the opposite, with bright yellow stripes found in smaller individuals, whereas larger frogs exhibit dull brown stripes. Here, we investigated whether size-dependent differences in colour support distinct defensive strategies. We first used visual modelling of potential predators to assess how colour contrast varied among frogs of different sizes. We found that contrast peaked in mid-sized individuals while the largest individuals had the least contrasting patterns. We then used two detection experiments with human participants to evaluate how colour and body size affected overall detectability. These experiments revealed that larger body sizes were easier to detect, but that the colours of smaller frogs were more detectable than those of larger frogs. Taken together our data support the hypothesis that the primary defensive strategy changes from conspicuous aposematism to camouflage with increasing size, implying size-dependent differences in the efficacy of defensive colouration. We discuss our data in relation to theories of size-dependent aposematism and evaluate the evidence for and against a possible size-dependent mimicry complex with sympatric poison frogs (Dendrobatidae).     

Thermal Buffering of Microhabitats is a Critical Factor Mediating Warming Vulnerability of Frogs in the Philippine Biodiversity Hotspot

Species may circumvent the impacts of climate warming if the habitats they use reduce ambient temperature. In this study, we identified which frog species from a tropical montane rain forest in the Philippines may be vulnerable to climate warming. To do so, we selected five anuran species that utilize four breeding habitats and identified the sensitivity and exposure of tadpoles and direct‐developer eggs to heat by measuring their critical thermal maximums (CT_max) and the habitat‐specific temperatures they experience. Our study species included two direct‐developer frogs—one species that lays its eggs on exposed leaves, and another that lays its eggs in ferns—and three species that produce aquatic free‐swimming tadpoles—two stream breeders, and one phytotelm (tree hole) breeder. We compared thermal tolerances derived from microclimates of breeding habitats with tolerances derived from macroclimate (i.e., non‐buffered air temperature taken from the rain forest canopy). We also examined whether differences in CT_max existed across life‐history stages (egg, metamorph/young‐of‐year, and adult) for the two direct‐developer frog species. Habitats buffered ambient temperature and expanded thermal tolerances of all frog species. We found that direct‐developers, however, are more vulnerable to increased temperatures than aquatic breeders—indicated by their high sensitivity to temperature, and exposure to high temperatures. Direct‐developer eggs were more sensitive to warming than both metamorph and adult life‐history stages. Thermally buffered microhabitats may represent the only protection against current and impending climate warming. Our data highlight the importance of considering sensitivity and exposure in unison when deciphering warming vulnerability of frogs.