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.     

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.     

Post-metamorphic change in activity metabolism of anurans in relation to life history

Summary Newly-metamorphosed individuals of some species of frogs and toads differ from adults in behavior, ecology, and physiology. These differences may be related to broader patterns of the life histories of different species of frogs. In particular, the length of larval life and the size of a frog at metamorphosis appear to be significant factors in post-metamorphic ontogenetic change. These changes in performance are associated with rapid post-metamorphic increases in oxygen transport capacity. Bufo americanus (American toads) and Rana sylvatica (wood frogs) spend only 2–3 months as tadpoles and metamorphose at body masses of 0.25 g or less. Individuals of these species improve endurance and aerobic capacity rapidly during the predispersal period immediately following metamorphosis. Increases in hematocrit, hemoglobin concentration, and heart mass relative to body mass are associated with this improvement in organismal performance. Rana clamitans (green frogs) spend from 3 to 10 months as larvae and weigh 3 g at metamorphosis. Green frogs did not show immediate post-metamorphic increases in performance. Rana palustris (pickerel frogs) are intermediate to wood frogs and green frogs in length of larval life and in size at metamorphosis, and they are intermediate also in their post-metamorphic physiological changes.American toads and wood frogs appear to delay dispersal from their natal ponds while they undergo rapid post-metamorphic growth and development, whereas green frogs disperse as soon as they leave the water, even before they have fully absorbed their tails. The very small body sizes of newly metamorphosed toads and wood frogs appear to limit the scope of their behaviors. The brief larval periods of these species permit them to exploit transient aquatic habitats, but impose costs in the form of a period of post-metamorphic life in which their activities are restricted in time and space compared to those of adults.     

Microgeographic morphological variation across larval wood frog populations associated with environment despite gene flow

Gene flow has historically been thought to constrain local adaptation; yet, recent research suggests that populations can diverge despite exchanging genes. Here I use a common garden experiment to assess the combined effects of gene flow and natural selection on morphological variation of 16 wood frog (Rana sylvatica) populations, a species known to experience divergent selection pressures in open‐ and closed‐canopy ponds across relatively small geographic scales. Wood frog tadpoles from different ponds showed significant morphological variation associated with canopy type with a trade‐off between tail length and body depth consistent with previous research. In contrast, neutral genetic differentiation of nine microsatellite loci as measured by Jost's D was not associated with canopy type, indicating no pattern of isolation by environment. Genetic structure analyses indicated some substructure across the 16 ponds (K = 4); however, three out of four assigned clusters included both open‐ and closed‐canopy ponds. Together, these results suggest that morphological divergence among these wood frog populations is occurring despite gene flow and that selection within these environments is strong. Furthermore, morphological variation among ponds differed across two sampling periods during larval development, demonstrating the importance of evaluating phenotypic divergence over multiple time periods and at a time relevant to the processes being studied.     

Habitat selection by a threatened desert amphibian

Habitat degradation and fragmentation are major drivers of amphibian declines. The loss of environmental features that allow for movement between water sources may be particularly detrimental for amphibians in arid environments. Climate changes will increase the importance of microhabitats to amphibians. Enhancing areas to facilitate movement may be a necessary conservation strategy for many animal species that depend on wetlands, including federally threatened Chiricahua leopard frogs (Lithobates chiricahuensis). Habitat preferences of this frog species are not well understood. We sought to better understand fine‐scale habitat selection, to inform conservation of Chiricahua leopard frogs. We conducted our study on the Ladder Ranch, a privately owned working bison ranch in New Mexico, USA that supports a large proportion of the remaining Chiricahua leopard frogs in the state. We attached radio transmitters to 44 frogs during summer 2014. We located each frog daily for up to 8 weeks (median = 30 days). We assessed fine‐scale habitat selection by comparing characteristics at each frog location and a random location 5 m away using conditional logistic regression. Frogs preferred features that likely reduce desiccation, even after accounting for the presence of water. Frogs selected areas with more low‐lying cover, especially aquatic vegetation and woody debris, a tree overstory, and a mud substrate. We recommend managing potential movement corridors for Chiricahua leopard frogs by ensuring the presence of muddy creek bottoms, woody debris, riparian overstory, low‐lying ground cover, and pools. Microclimates created by these features seem especially valuable given warming temperatures and modified precipitation regimes, resulting in decreased surface water, soil moisture, and vegetation cover. Retaining or creating preferred habitat features and microclimates in areas between water sources may increase connectivity among isolated populations of Chiricahua leopard frogs and could improve persistence and recovery of other water‐obligate species in arid landscapes.     

The shape of things to come: linking developmental plasticity to post‐metamorphic morphology in anurans

Development consists of growth and differentiation, which can be partially decoupled and can be affected by environmental factors to different extents. In amphibians, variation in the larval environment influences development and causes changes in post‐metamorphic shape. We examined post‐metamorphic consequences, both morphological and locomotory, of alterations in growth and development. We reared tadpoles of two phylogenetically and ecologically distant frog species (the red‐eyed treefrog Agalychnis callidryas and the African clawed frog Xenopus laevis) under different temperatures with ad libitum food supply and under different food levels at a constant temperature. Low temperature and low food levels both resulted in similarly extended larval periods. However, low temperature yielded relatively long‐legged frogs with a lower degree of ossification than warm temperature, whereas low food yielded relatively short‐legged frogs with a higher degree of ossification than high food levels. Such allometric differences had no effect on locomotor performance of juveniles. Our results provide a basis for understanding the relationship between growth, differentiation and post‐metamorphic shape in anurans and help explain many of the discrepancies reported in previous studies.     

Past and Present Risk: Exposure to Predator Chemical Cues Before and after Metamorphosis Influences Juvenile Wood Frog Behavior

Animals are exposed to different predators over their lifespan. This raises the question of whether exposure to predation risk in an early life stage affects the response to predators in subsequent life stages. In this study, we used wood frogs (Rana sylvatica) to test whether exposure to cues indicating predation risk from dragonfly larvae during the wood frog larval stage affected post‐metamorphic activity level and avoidance of garter snake chemical cues. Dragonfly larvae prey upon wood frogs only during the larval stage, whereas garter snakes prey upon wood frogs during both the larval stage and the post‐metamorphic stage. Exposure to predation risk from dragonflies during the larval stage caused post‐metamorphic wood frog juveniles to have greater terrestrial activity than juvenile wood frogs that were not exposed to larval‐stage predation risk from dragonflies. However, exposure to predation risk as larvae did not affect juvenile wood frog responses to chemical cues from garter snakes. Wood frogs exposed as larvae to predation risk from dragonfly larvae avoided garter snake chemical cues to the same extent as wood frog larvae not exposed to predation risk from dragonfly larvae. Our results demonstrate that while some general behaviors exhibit carry‐over effects from earlier life stages, behavioral responses to predators may remain independent of conditions experienced in earlier life stages.     

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.     

The potential impact of simulated ground-water withdrawals on the oviposition,larval development,and metamorphosis of pond-breeding frogs

Wetland hydroperiod is a key factor for the reproductive success of pond-breeding amphibians. Ground-water withdrawals may cause intermittent ponds to dry prematurely, potentially affecting amphibian development. In three intermittent ponds, we monitored hydrology and tracked oviposition, larval development, and metamorphosis for three frog species that represented a range of breeding phenologies. The three species were the southern leopard frog (Lithobates sphenocephalus), spring peeper (Pseudacris crucifer), and Pine Barrens treefrog (Hyla andersonii). We simulated ground-water withdrawals by subtracting from 5 to 50 cm (in 5-cm increments) from the measured water-depth values at the ponds over a short-term (2-year) period and a long-term (10-year) period to estimate the potential impact of hydroperiod alterations on frog development. Short-term simulations indicated that 5 and 10 cm water-depth reductions would have resulted in little or no impact to hydroperiod or larval development and metamorphosis of any of the species. Noticeable impacts were estimated to occur for reductions ≥15 cm. Long-term simulations showed that impacts to the appearance of the first pre-metamorphs and metamorphs would have occurred at reductions ≥10 cm and impacts to initial egg deposition would have occurred at reductions ≥20 cm. For all simulations, successively greater reductions would have caused increasing impacts that varied by species and pond, with the 50-cm reductions shortening hydroperiods enough to practically eliminate the possibility of larval development and metamorphosis for all three species. Compared to the spring peeper and southern leopard frog, the estimated impacts of the simulations on the various life stages were the greatest for the Pine Barrens treefrog.     

Amphibian species richness across environmental gradients

Large‐scale field patterns are a fundamental source of inferences on processes responsible for variation in species richness among habitats. We examined species richness of larval amphibian communities in 37 ponds over seven years on the Univ. of Michigan's E. S. George Reserve. Ordination of the community incidence matrix indicated a strong major axis of variation in species associations that was correlated with pond hydroperiod, surface area and forest canopy cover. Communities were significantly nested with those species found in ponds with high canopy cover, small area and short hydroperiod being nested subsets of those found in ponds with contrasting characteristics. Presence of fish had strong negative effects on species richness; relaxation of this effect also was apparent when fish were extirpated from ponds by drought. We employed a model selection analysis to identify the most appropriate statistical model for predicting the long‐term average species richness of these ponds from local abiotic and biotic (predator and competitor density) factors. A model including only the abiotic factors was overwhelmingly superior for the anurans; hierarchical partitioning indicated that area and canopy cover alone accounted for over 70% of the independent effects of predictor variables. The global model including both abiotic and biotic factors was the best supported model for the caudates, and correspondingly hierarchical partitioning suggested that area, hydroperiod, invertebrate predators and caudate biomass all accounted for 9–16% of the independent effects. Overall, biotic factors accounted for much less of the variation in species richness than abiotic factors. The patterns in larger, open‐canopy ponds provided little evidence of competitive effects on species richness, though there were patterns consistent with competitive effects in small, closed‐canopy ponds. The unusual temporal and spatial extent of these data enabled us to critically evaluate ideas regarding patterns in larval amphibian communities, and the effects of area, disturbance (hydroperiod) and productivity (canopy cover) on species richness of these communities. These results have important implications to the conservation of amphibian species richness in freshwater wetlands, which are among the most threatened ecosystems worldwide.     

Effects of transgenic American chestnut leaf litter on growth and survival of wood frog larvae

Biotechnology offers a new approach for the restoration of tree species affected by exotic pathogens; however, nontarget impacts of this novel strategy on other organisms have not been comprehensively assessed. We evaluated the effect of transgenic American chestnut (Castanea dentata) leaf litter on the growth and survival of larval wood frogs (Lithobates sylvaticus), a forest‐dwelling amphibian species widely sympatric with American chestnut, that forage almost entirely on periphyton and litter detritus that accumulate in temporary vernal pools in forests. We reared wood frog larvae on Castanea leaf litter (American chestnut genetically engineered for blight tolerance, nontransgenic American chestnut, Chinese chestnut [Castanea mollissima], and an American–Chinese chestnut hybrid) and litter from two non‐Castanea, nontransgenic “control” tree species, coupled with two levels of supplementary food. We observed no differences in growth or survival of wood frog larvae reared on transgenic versus nontransgenic American chestnut leaves. Without supplementary food, wood frog larvae provided leaves from American chestnut (both types) developed faster and grew larger than those exposed to other leaf litter treatments. Results of this study provide preliminary evidence that (1) American chestnut may have formerly been an important source of food for forest‐dwelling amphibians and (2) transgenic American chestnut litter generated as part of chestnut restoration efforts is unlikely to present direct novel risks to developing amphibian larvae in the forest environment.     

Amphibian phenotypic variation along a gradient in canopy cover: species differences and plasticity

The distributions of many freshwater organisms correlate with a gradient in canopy cover, ranging from sunny wetlands to closed woodland ponds. Little is known about mechanisms that exclude species from some sections of the gradient while allowing persistence in others. I addressed this question by manipulating shading in 740‐l outdoor mesocosms and measuring several ecologically‐relevant traits in three species of amphibian larva (Rana temporaria and Triturus alpestris, generalists occupying the entire gradient; and Hyla arborea, a specialist in open habitats). Shading caused delayed development, but had no effect on survival and increased the growth rate of R. temporaria. Body and tail color were darker in the shade. Plasticity in morphological shape, consisting of reduced gut width and increased tail size under shaded conditions, may reflect poor food availability and low dissolved oxygen. The canopy generalist R. temporaria increased activity in the shade, spent more time basking in shallow water, and maintained high larval performance. Unexpectedly, the specialist H. arborea was also highly plastic. These results describe extensive phenotypic plasticity induced by shade, and highlight traits that may influence performance along the canopy gradient.     

Leaf litter input mediates tadpole performance across forest canopy treatments

Understanding the mechanisms limiting the distributions of organisms is necessary for predicting changes in community composition along habitat gradients. In many areas of the USA, land originally cleared for agriculture has been undergoing a process of reforestation, creating a gradient of canopy cover. For small temporary wetlands, this gradient can alter abiotic conditions and influence the resource base of wetland food webs by affecting litter inputs. As distributions of amphibians and many other temporary wetland taxa correlate with canopy cover, we experimentally manipulated shade levels and litter types in pond mesocosms to explore mechanisms limiting species performance in wetlands with canopy cover. Most differences between ponds were mediated by litter type rather than direct effects of shading. Although all three amphibian species tested are open-canopy specialists, spring peepers were the only species to show decreased survival in shaded ponds. Pond litter type generally had strong effects on growth and development rates, with tadpoles of two species in grass litter ponds growing to twice the size of, and metamorphosing 7 days earlier than, those in leaf litter ponds. Contrary to our initial hypothesis, shade level and litter type showed very few significant interactions. Our results indicate that the effects of shading cannot be considered in isolation of vegetation changes in pond basins when evaluating the effects of forest succession on temporary pond communities.     

Microgeographical variation in thermal preference by an amphibian

Ectotherms use behaviour to buffer effects of temperature on growth, development and survival. While behavioural thermoregulation is widely reported, localized adaptation of thermal preference is poorly documented. Larval amphibians live in wetlands ranging from entirely open to heavily shaded by vegetation. We hypothesized that populations undergo localized selection leading to countergradient patterns of thermal preference behaviour. Specifically, we predicted that wood frog (Rana sylvatica) larvae from closed canopy ponds would be more strongly temperature selective and would prefer higher temperatures than conspecifics from populations found in open canopy ponds. In a study of six breeding ponds in north‐eastern Connecticut, USA, these predictions were upheld. The countergradient, microgeographical variation in thermal preference documented here implies that wood frog populations may have diverged rapidly in the face of contrasting selection pressures. Rapid, behaviourally mediated responses to changing thermal environments have important implications for understanding population responses to climate change.     

Reciprocal subsidies in ponds: does leaf input increase frog biomass export?

Reciprocal subsidies occur when ecosystems are paired, both importing and exporting resources to each other. The input of subsidies increases reciprocal subsidy export, but it is unclear how this changes with other important factors, such as ambient resources. We provide a conceptual framework for reciprocal subsidies and empirical data testing this framework using a pond–forest system in Missouri, USA. Our experiment used in situ pond mesocosms and three species of anurans: wood frogs, American toads, and southern leopard frogs. We predicted that increases in ambient resources (primary productivity) and detrital subsidy input (deciduous tree leaves) into pond mesocosms would increase reciprocal export (frog biomass) to the surrounding terrestrial ecosystem. In contrast, we found that increases in primary productivity consistently decreased frog biomass, except with leaf litter inputs. With leaf inputs, primary productivity did not affect the export of frogs, indicating that leaf detritus and associated microbial communities may be more important than algae for frog production. We found that subsidy inputs tended to increase reciprocal exports, and thus partial concordance with our conceptual framework.     

The growth–mortality tradeoff: evidence from anuran larvae and consequences for species distributions

A tradeoff affecting the ability to grow under high versus low resource levels has been commonly hypothesized to influence species distributions across resource gradients in a wide variety of taxa. This influence is dependent on individual growth being proportional to traits that affect demographic processes such as mortality. However, data on how individual growth scales with demographic performance are rare. We conducted a mesocosm experiment, and re-analyzed data from a similarly designed field experiment, to examine the relationship between growth and mortality in two tadpole species that segregate across a resource gradient. Overall, environmental conditions leading to faster growth also lead to lower mortality rates. However, species differed in this relationship. Leopard frogs achieved faster growth than wood frogs, but their absolute mortality was greater and increased steeply as growth decreased. Conversely, absolute mortality of wood frogs was lower and less strongly dependent on growth. These interspecific differences suggest a second tradeoff, that between maximizing growth rates or minimizing mortality, with potentially important demographic consequences. Leopard frogs grow faster than wood frogs in productive ponds, but are excluded from unproductive ponds dominated by wood frogs due to accelerating mortality rates with declining realized growth. A review of the literature suggests that in diverse taxa, including plants, microcrustaceans and drosophilids, patterns in mortality are consistent with this tradeoff indicating that the mechanism we demonstrate could be a link between individual performance and demographic rates influencing species distributions in other systems.     

The role of pollutant accumulation in determining the use of stormwater ponds by amphibians

Urbanization often results in the creation of habitats such as stormwater management ponds. Although stormwater ponds are designed to retain runoff and associated pollutants, they are frequently colonized by wildlife including pond-breeding amphibians. Understanding of the ecological function of these created habitats is limited. This study investigated the role of pollutants in shaping use of stormwater ponds by amphibians. A survey of 68 stormwater ponds in Baltimore County, Maryland, and statistical modeling found wood frogs (Rana [= Lithobates] sylvatica) were more likely to breed in ponds with longer hydroperiods and Cl^? concentrations below approximately 250 mg/L. American toad (Bufo [= Anaxyrus] americanus) use of ponds was primarily influenced by hydroperiod; toads were more likely to use longer hydroperiod ponds. To confirm use was a result of toxicity and differential sensitivity among species, wood frog and American toad embryos and larvae were exposed to sediment from six stormwater ponds spanning the range of pollutant conditions documented in the field. Survival of wood frogs through metamorphosis was related to metal and salt levels of pond sediments, but survival of American toads was not. In agreement with the field study, no wood frog larvae survived to metamorphosis when Cl^? levels were above 260 mg/L. The results suggest that pollutants that accumulate in stormwater ponds, specifically road deicing salts, are acting as local filters capable of creating unique assemblages of anuran larvae in urban areas.     

Anthropogenic changes to leaf litter input affect the fitness of a larval amphibian

相似文献   

Synergistic effects of multiple mechanisms drive priority effects within a tadpole assemblage

Mounting evidence suggests that the history of species arrival to a locality can have important effects on species performance but the mechanism(s) through which priority effects are produced is not always clear. Differences in the developmental time of frog tadpoles provide an opportunity to examine mechanisms through which priority effects may influence fitness components of a late arriving taxon. Specifically, tadpoles of the southern leopard frog (Rana) can often require more than a year to complete metamorphosis so they overwinter in a pond and compete with newly deposited tadpoles in the spring. We conducted an experiment in artificial ponds to evaluate mechanisms through which overwintering Rana tadpoles influence fitness components of southern toad (Bufo) tadpoles deposited into ponds during the spring. We found that overwintered Rana reduced Bufo performance while newly hatched Rana that enter a pond simultaneously with Bufo did not. The production of this priority effect was primarily the result of Rana depleting algal resources in a pond during the winter prior to Bufo arrival. The performance of Bufo did not correspond with variation in the abundance of algae present in a pond during the spring and we found evidence to indicate that, in the absence of resource exploitation during the winter, overwintered Rana do not compete strongly with Bufo during the spring when both species co‐occur. When Rana deplete algal resources during the winter, however, interactions between Rana and Bufo during the spring became much more important as both the development rate and survival of Bufo was reduced to a greater extent than what would have been predicted by resource exploitation alone. Our results demonstrate that priority effects can result from early colonists depleting resource availability prior to the arrival of other species which can intensify behavioral/physical interactions between species when they co‐occur.     

Competition and the distribution of spring peeper larvae

Studies of tadpole distributions have shown that despite overlapping affinities for semipermanent and permanent ponds, distributions of the spring peeper (Pseudacris crucifer) and the green frog (Rana clamitans) tend to be nonoverlapping. Because spring peepers are believed to be poor competitors, I hypothesized that competition from green frog larvae limits the distribution of spring peeper larvae. I stocked field enclosures with a constant density of spring peeper larvae, and one of four densities of green frog larvae (a target-neighbor design). Increased green frog density had a small effect on metamorphic size and no effects on survivorship, larval period or growth rates of spring peepers. In contrast to these small interspecific effects, green frogs had a large effect on their own performance. Intraspecific competition resulted in a 50% decline in growth rate and an 11% decline in metamorphic size. These results suggest that the species are segregated in resource use, or that compared with green frogs, spring peepers are better able to cope with depressed resource densities. In either case, this field experiment provides no evidence that interspecific competition from green frogs limits distributions of spring peepers. Other factors such as predation and breeding site choice by adults may contribute to the absence of spring peeper larvae from many semipermanent and permanent ponds.