Article

Landscape resistance to movement of the poison frog, Oophaga pumilio, in the lowlands of northeastern Costa Rica

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Abstract

Conversion of forests to agricultural land or pastures is occurring at a rapid rate in many tropical regions. Amphibians may be particularly susceptible to changes in landscape composition and connectivity because of their physiological characteristics and complex life cycles. We experimentally assessed landscape resistance for the dart-poison frog Oophaga pumilio associated with two prevalent land-cover types, secondary forests and pastures, in the northeastern lowlands of Costa Rica. We measured recapture rates of individuals displaced into forests and into pastures, the effects of microclimate on the movement performance of individuals, and the influence of land-cover type and displacement distance on orientation ability of O. pumilio. Results showed a significant interaction between displacement distance and land-cover type indicating greater resistance to movement experienced by individuals displaced into pastures compared with frogs displaced into forests. Microclimatic conditions in pastures had a detrimental effect on the movement performance of O. pumilio and initial orientation was both distance and habitat dependent. Understanding the magnitude of resistance presented by different land-uses to amphibian dispersal is important for the development of successful conservation strategies in human-altered landscapes.

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... Tropical amphibians show extremely diverse reproductive and spatial behaviours, such as long-term territoriality and long-distance movements between fluctuating breeding sites. However, homing ability has rarely been studied in tropical species (but see Gonser & Woolbright 1995, Nowakowski et al. 2013, 2014a. Poison frogs (Dendrobatidae) are a group of small diurnal Neotropical frogs that show some of the most complex spatial behaviours among amphibians. ...
... Many poison frogs rely on homing as the water bodies for tadpole development are often situated outside their territory (e.g., Roithmair 1994, Ringler et al. 2009). Homing ability after experimental translo-cation has been studied only in the strawberry poison frog, Oophaga pumilio (McVey et al. 1981, Nowakowski et al. 2013 and Allobates femoralis (Pašukonis et al. , 2014a. Territorial A. femoralis males returned after translocations at a success rate of more than 80% for translocation distances of up to 200 m and 30% from 400 m . ...
... Furthermore, tracking experiments revealed that A. femoralis relies on being familiar with an area for homing, and barriers like rivers affect initial homeward orientation (Pašukonis et al. 2014b). Nowakowski et al. (2013) found that only 67% of translocated O. pumilio returned from 20 m (N = 30) and 57% from 30 m (N = 30), suggesting a smaller homing radius in this species. Contrary to most Allobates species, female O. pumilio deposit their tadpoles in phytothelms within or close to their established territories (Pröhl & Berke 2001). ...
... Thus, corridors should reduce problems stemming from small population size such as loss of genetic variability due to drift and inbreeding depression. Dispersal ability is dependent on functional connectivity of the surrounding landscape (Tischendorf and Fahrig, 2000;Ricketts, 2001;Vandermeer and Carvajal, 2001;Nowakowski et al., 2012) which is determined by structural connectedness in concert with the behavioral and physiological capacity for organisms to move between fragments. Functional isolation, the converse of functional connectivity, is often a result of harsh matrix habitat matrices that differ drastically from the habitat typically occupied by a given organism, through which organisms must pass to travel between fragments. ...
... Data were collected from the La Selva Biological Station and four forest fragments in the Sarapiqui region of northeastern Costa Rica. This is a fragmented landscape consisting of approximately 29% remnant forest (Nowakowski et al., 2012), 20% pasture, 20% regenerating forest (Sesnie et al., 2008), with much of the remainder as extensive commercial agriculture. Fragments were located using land cover maps and aerial photographs of the San Juan-La Selva corridor region (for description of the biological corridor, see Sesnie et al., 2008;Fagan et al., 2013) and were chosen based on their similarity of size (40-50 ha), high level of isolation from neighboring fragments (albeit representative of the corridor), and accessibility from La Selva (Fig. 1). ...
... Results from the dispersal challenge experiment suggested that M. caerulatus has a limited perceptual range, a trait that affects functional connectivity of its landscape (Lima and Zollner, 1996). The San Juan-La Selva BCN is composed of over 900 old growth (>30 year old, P2.5 ha) forest fragments imbedded in a matrix of primarily pasture (Fagan et al., 2013) the majority of which are separated by over 50 m (Nowakowski et al., 2012). Given M. caerulatus's limited dispersal abilities, this landscape-scale conservation may be of limited value for M. caerulatus and similar species, for example, lowland Neotropical birds (Laurance et al., 2004;Ibarra-Macias et al., 2011). ...
... Widespread forest loss is the primary threat to amphibian biodiversity in the region and likely interacts with other known causes of declines such as contamination and disease (Becker & Zamudio 2011, Gardner et al. 2007, Kerby et al. 2011, Vié et al. 2009, Whitfield et al. 2012. Amphibians may be particularly vulnerable to forest conversion because they are smallbodied, have limited vagility, and high susceptibility to desiccation, which can impede dispersal and reduce survival in habitats with little cover (Nowakowski et al. 2013, Rothermel & Luhring 2005. 1 Corresponding author. Email: anowa001@fiu.edu ...
... In north-eastern Costa Rica, the establishment of cattle pastures was the primary driver of deforestation during the previous three decades (Butterfield 1994). Pastures are characterized by extensive cover of grasses that inhibit the recruitment of woody plants, and by microclimates that are warmer and drier than in forest (Nowakowski et al. 2013, Slocum 2001. If pastures represent poor-quality habitat for amphibians, populations in pastures may act as sinks, may be dominated by subordinate individuals, and could experience greater fitness costs than individuals in nearby forest, such as increased parasite loads and reduced growth and survival (Hitchings & Beebee 1997, McKenzie 2007. ...
... There is still moderate cover of fragmented forest (c. 50% of the landscape), and nearest-neighbour distances between forest patches are typically ࣘ200 m (Nowakowski et al. 2013). While cattle pastures represent the dominant land use in the region, occupying approximately 20% of the land area, most pastures are of modest size and adjacent to forest. ...
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Conversion of natural habitats to anthropogenic land uses is a primary cause of amphibian declines in species-rich tropical regions. However, agricultural lands are frequently used by a subset of forest-associated species, and the habitat value of a given land use is likely modified by the presence and characteristics of remnant trees. Here we used mark–recapture methods to examine abundances and movement probability of the poison frog, Oophaga pumilio, at individual trees in forest-fragment edges and adjacent pastures in north-eastern Costa Rica. One hundred and forty-seven trees were surveyed at three replicate sites that each included a forest fragment and adjacent pasture. Trees were sampled at distances of ≤30 m into forest and ≤150 m into pastures for Oophaga pumilio, and local environmental characteristics were measured at each tree. We also measured indices of physical condition (size and endurance) of frogs captured in forest edges and in nearby pastures. Analyses of 167 marked individuals showed no difference in per-tree abundances or sex ratios between pasture and forest edges. We found significant interactions between habitat type and leaf-litter cover, tree dbh and number of logs, indicating greater influence of local variables on abundances in pastures. Movement among trees was infrequent and not predicted by sex, size, habitat type or environmental variables. While results of endurance tests did not differ for individuals from the two habitats, frogs captured in pastures were, on average, larger than frogs captured in forest edges. These data indicate that remnant trees are important habitat features for O. pumilio in pastures and corroborate research in other systems that suggests that large relictual trees should be retained to maximize the potential for altered landscapes to provide habitat for native species.
... In frogs and toads, homing behavior so far has mostly focused on nocturnal taxa from the temperate region (e.g., Bogert & Station 1947, Dole 1968, Jameson 1957, Twitty et al. 1964, Holenweg Peter et al. 2001. In recent years, there has been some research progress with regard to diurnal terrestrial anurans from the Neotropics, mainly in the intriguing group of poison frogs of the families Aromobatidae and Dendrobatidae (Nowakowski et al. 2013, Pichler et al. 2017. ...
... This behavior is suggested to be associated with the utilization of beneficial resources, such as food or shelter availability, or to be profitable in mate attraction. Resource use also explains homing behavior observed in some poison frog species (Nowakowski et al. 2013). An additional reason for pronounced homing abilities is that water bodies utilized for larval deposition are of-ten limited and specimens have to carry tadpoles over several hundred meters away from their home ranges (Pröhl & Hödl 1999, Ringler et al. 2009). ...
... An additional reason for pronounced homing abilities is that water bodies utilized for larval deposition are of-ten limited and specimens have to carry tadpoles over several hundred meters away from their home ranges (Pröhl & Hödl 1999, Ringler et al. 2009). As summarized in Table 1, of the 18 genera in the two poison frog families, homing after experimental translocation has been examined in three species of two genera only (McVey et al. 1981, Nowakowski et al. 2013, Pichler et al. 2017). All of them displayed a clear tendency to return, but return rates decreased with distance. ...
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Neotropical poison frogs (Aromobatidae, Dendrobatidae) are known for their complex behavior including site fidelity and home range maintenance. It has been shown in a few poison frog species that these amphibians are able to return to their home ranges after experimental translocation. In this study we asked if Ameerega trivittata can be allocated to the species performing homing behavior. In this taxon, males and females show home range behavior, while sexes were not distinguished in our study. Fieldwork was carried out in a wild population at Panguana (Peru), using replacement distances of 150 m, 600 m and 900 m. In total, 79 frogs were translocated. Most rapidly returned to their home ranges from all translocation distances, with a decrease of the homing success with longer distance. Among the poison frogs studied so far, it is remarkable that A. trivittata is the only one known to be able to return from 900 m (which perhaps is a remarkable homing distance for anurans in general), while maximum return distances in other species are less than 50% of this. Ameerega trivittata is one of the largest poison frogs (maximum snout–vent length 55 mm). However, long distance homing was not explained by the species’ body size. We rather expect that ‘good knowledge’ of the general area (in terms of integration of learned landmarks) that frogs live in is the reason for the ability of long distance homing in our focal taxon. © 2018 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Mannheim, Germany.
... Experimental studies showed that amphibians move more slowly on grassy land cover types, such as those mimicking pastures and other graminoid fields, than they do when exposed to less vertically structured types such as leaf litter or bare soil (Cline & Hunter, 2016;Nowakowski et al., 2013Nowakowski et al., , 2015Stevens et al., 2004). We found an analogous pattern in all stages of X. laevis (Figure 1; Figure 4A). ...
... Amphibians experience higher desiccation risk on bare land cover types than on other types characterized by higher structural complexity (Cayuela et al., 2020;Nowakowski et al., 2013;and Nowakowski et al., 2015) and this agrees well with our results in X. laevis ( Figure 4B). Structurally complex substrates such as grass or leaf litter retain water and reduce the animal's surface area exposed to evaporation to a greater degree than bare substrates such as asphalt or bare soil. ...
... In accordance with studies conducted on other amphibians, we found that in X. leavis resistance costs associated with dehydration conflict with those obtained by measuring physical resistance to locomotion ( Figure 4B; Supporting Information Appendix 8; Cayuela et al., 2020;Nowakowski et al., 2013Nowakowski et al., , 2015. Bare land cover types such as asphalt impose a higher dehydration risk but a lower mechanic resistance to locomotion when compared to structurally complex substrates such as grass, and vice versa ( Figure 4B). ...
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1. The description of functional connectivity is based on the quantification of landscape resistance, which represents species-specific movement costs across landscape features. Connectivity models use these costs to identify movement corridors at both individual and population levels and provide management recommendations for populations of conservation interest. Typically, resistance costs assigned to specific land cover types are assumed to be valid for all individuals of the population. Little attention has been paid to intraspecific variation in resistance costs due to age or dispersal syndrome, which may significantly affect model predictions. 2. We quantified resistance costs in an expanding invasive population of the African clawed frog Xenopus laevis in Western France. In this principally aquatic amphibian, juveniles, sub-adults and adults disperse overland. The enhancement of dispersal traits via spatial sorting has been also observed at the range periphery of the population. Resistance costs, and thus connectivity, might vary as a function of life stage and position within the invaded range. 3. We assessed multiple dimensions of functional connectivity. On various land cover types, we measured locomotion, as crossing speed, in different post-metamorphic age classes, and dehydration, sensitivity of locomotion to dehydration, and substrate preference in juveniles. We also tested the effect of the position in the invaded range (core vs. periphery) on individual performances. 4. In juveniles, general trends toward higher resistance costs on grass and lower resistance costs on bare soil and asphalt were observed, although not all experiments provided the same cost configurations. Resistance to locomotion varied between age classes, with adults and subadults facing lower costs than juveniles, particularly when crossing structurally complex land cover types like grass and leaf litter. The position in the range had a minor effect on landscape resistance, and only in the dehydration experiment, where water loss in juveniles was lower at the range periphery. 5. Depicting functional connectivity requires: i) assessing multiple dimensions of behavioural and physiological challenges faced by animals during movement; ii) considering factors, such as age and dispersal syndrome, that may affect movement at both individual and population level. Ignoring this complexity might generate unreliable connectivity models and provide unsupported management recommendations for conservation.
... Apparently, individuals of A. bombetes have a limited homing ability when compared to other poison frogs for which this behavior has been studied, except for O. pumilio, which seems more similar in body size and resources used for reproduction (i.e., phytotelmata in bromeliads). Moreover, our study differs from others with Dendrobatidae (McVey et al., 1981;Vail and Lahanas, 2010;Nowakowski et al., 2013;Pašukonis et al., 2013Pašukonis et al., , 2014aPašukonis et al., , 2014bPašukonis et al., , 2016Pašukonis et al., , 2018Liu et al., 2016;Pichler et al., 2017;Nothacker et al., 2018) in including a comparison of sex differences in homing ability with a large sample size. ...
... Most of the studies on homing in Dendrobatidae, including ours, have found an inverse relationship between homing ability and translocation distance (McVey et al., 1981;Nowakowski et al., 2013;Pašukonis et al., 2013;Pichler et al., 2017;Nothaker et al., 2018; but see Pašukonis et al., 2018 for A. trivittata). It is possible that homing ability may diminish with translocation distance because individuals are unable to recognize spatial cues if translocated a large distance away from their territory, and they do not have previous experience with the distant site (Dole, 1968;Ferguson, 1971;Sinsch, 1987Sinsch, , 2006. ...
... A comparison at interspecific level with poison frogs shows an apparent positive relationship between body size of species and the distance at which they exhibit homing ability. In A. bombetes (average SVL ¼ 19.2 mm), we found that the probability of homing was very low at 90 m; something similar has been reported for O. pumilio (SVL ¼ 17-22 mm), in which individuals tend to exhibit a strong decrease in homing ability after 20-50 m (McVey et al., 1981;Vail and Lahanas, 2010;Nowakowski et al., 2013). In larger poison frog species, individuals are able to home from farther distances. ...
Article
Homing is a behavior in which an animal returns to a specific place after they have moved or migrated to a distant place. In anurans, most of our knowledge about homing comes from studies in temperate-region species with nocturnal activity and reproduction associated with ponds. Recently, studies with poison frogs (Dendrobatidae) have increased our understanding about homing in tropical frogs with diurnal activity, and that do not breed in large ponds. The Rub´ı Poison Frog Andinobates bombetes offers a good opportunity to further increase the knowledge of behavioral ecology of homing in anurans because some natural history traits in this species differ from those exhibited in most poison frogs in which homing ability has been studied. For instance, A. bombetes have a smaller body size and use phytotelmata in bromeliads for tadpole development while others use terrestrial pools. To quantify the homing ability and the factors influencing it in A. bombetes, we performed translocation experiments of individuals at distances between 5 and 90 m outside their territory in a forest remnant located in the department of Quind´ıo, Central Andes of Colombia. In this study, we included a large sample size of females, which is important because homing studies with poison frogs has been almost exclusively studied in territorial males. Of 104 displaced individuals, 39 returned to their territory. The probability of homing in A. bombetes was negatively related to the translocation distance, but was unrelated to body size and sex. Apparently, this species has a limited homing ability when compared to most poison frogs studied so far except for O. pumilio, which seems more similar in body size and resources used for reproduction. Overall, homing ability appears to be widely shared in the family Dendrobatidae, Andinobates being the fourth genus of this family for which homing ability has been corroborated experimentally.
... Population connectivity is particularly important for species like amphibians that experience high turnover rates and exist as metapopulations or patchy populations (Smith and Green, 2005). Studies of amphibian movement at forest edges have found that forests have higher permeability than other habitat types (Vasconcelos and Calhoun, 2004;Rittenhouse and Semlitsch, 2006;Nowakowski et al., 2013; but see Graeter et al., 2008), which has been attributed to desiccation risk. Open canopy habitats tend to have higher temperatures and lower humidity, resulting in greater water loss (Rothermel and Semlitsch, 2002;Cosentino et al. 2011;Nowakowski et al. 2013). ...
... Studies of amphibian movement at forest edges have found that forests have higher permeability than other habitat types (Vasconcelos and Calhoun, 2004;Rittenhouse and Semlitsch, 2006;Nowakowski et al., 2013; but see Graeter et al., 2008), which has been attributed to desiccation risk. Open canopy habitats tend to have higher temperatures and lower humidity, resulting in greater water loss (Rothermel and Semlitsch, 2002;Cosentino et al. 2011;Nowakowski et al. 2013). Other studies of edge and habitat permeability have emphasized the importance of vegetation structure and ease of movement (e.g. ...
... Our study clearly demonstrates that microhabitats that reduce desiccation are important determinants for habitat choice in amphibians; this is consistent with other studies demonstrating a preference for amphibians to travel through habitats that minimize desiccation (e.g. Rothermel and Semlitsch, 2002;Cosentino et al., 2011;Nowakowski et al., 2013). In Experiment 1, individuals chose habitat with lower ground temperature and higher humidity (shade) and higher soil moisture. ...
... Compared to other taxa such as birds and mammals, amphibians and reptiles are generally more limited in dispersal capability (Hillman et al., 2014), and limited dispersal may limit their ability to colonize secondary forests. Dispersal is largely affected by geographic distance between patches (Brown and Kodric-Brown, 1977;Ficetola and De Bernardi, 2004), type of matrix between patches (Fahrig and Merriam, 1994;Gascon et al., 1999;Nowakowski et al., 2013), and species-specific behavior and physiology (Lees and Peres, 2009). Species that are highly mobile and resilient to matrix conditions will be more successful in colonizing isolated secondary forest patches. ...
... Additionally, it is unclear if amphibian and reptile populations in secondary forest patches are being maintained by internal recruitment, immigration from nearby mature forest, or a combination of the two processes. Although secondary forests do not provide suitable habitat to maintain populations of some species, they may still have other positive effects in comparison to matrix habitat such as increasing connectivity between older forest patches, providing less resistance to movement than matrix habitat, and acting as good corridors for dispersal (Nowakowski et al., 2013). ...
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Over the past century, humans have cleared the Earth's forests at an alarming rate and intensity. The majority of global forest cover is categorized as secondary forest, and it is becoming increasingly important to consider secondary forests in addition to old-growth forest in conservation planning for biota. We reviewed the literature to synthesize information on amphibian and reptile communities during secondary forest succession. We summarized literature on mechanisms of community change during forest succession and conducted a meta-analysis to estimate effect sizes for species richness and abundance in human-modified landscapes (agriculture, pasture, and plantation) and old-growth forests compared to regenerating secondary forests. Studies reported strong support for differences in species composition among human-modified landscapes, secondary forest, and old-growth forest as well as species-specific responses to successional forest change. Secondary forest generally had higher species richness and abundance than human-modified landscapes, but lower species richness and abundance than old-growth forests. This result was more pronounced in amphibians than reptiles, and effect size of abundance was more variable than richness among studies. Secondary forests have better conservation value than altered habitats, but they do not necessarily hold the same conservation value for species as old-growth forest.
... There is a growing understanding of the abilities of poison frogs to navigate in their natural environment. Oophaga pumilio use place cues (and not tadpole identity) to locate their tadpole deposition sites (Stynoski, 2009) and can accurately orient towards their territories after displacement (Nowakowski et al., 2013). Allobates femoralis has accurate homing abilities, navigating in a straight trajectory after displacement independent of egocentric path integration and route learning (Pašukonis et al., 2018(Pašukonis et al., , 2014a(Pašukonis et al., ,b, 2013(Pašukonis et al., , 2016. ...
... Together, these findings represent the first demonstration of a sketch map (topographic information) in an amphibian. Combined with the results of field experiments in O. pumilio and A. femoralis (Nowakowski et al., 2013;Pašukonis et al., 2018Pašukonis et al., , 2014aPašukonis et al., ,b, 2016Stynoski, 2009) and evidence of bearing maps (directional information) in other amphibians (Sinsch, 1990(Sinsch, , 2014, we can conclude that poison frogs are likely to have an integrated cognitive map that includes both bearing and sketch mapping systems. Our study provides the first conclusive evidence of an integrated cognitive map in an amphibian. ...
Article
A fundamental question in cognitive science is whether an animal can use a cognitive map. A cognitive map is a mental representation of the external world, and knowledge of one's place in this world, that can be used to determine efficient routes to any destination. Many birds and mammals are known to employ a cognitive map, but whether other vertebrates can create a cognitive map is less clear. Amphibians are capable of using beacons, gradients and landmarks when navigating, and many are proficient at homing. Yet only one prior study directly tested for a cognitive map in amphibians, with negative results. Poison frogs exhibit unusually complex social and spatial behaviors and are capable of long-distance homing after displacement, suggesting that they may be using complex spatial navigation strategies in nature. Here, we trained the poison frog Dendrobates auratus in a modified Morris water maze that was designed to suppress thigmotaxis to the maze wall, promoting exploration of the arena. In our moat maze, the poison frogs were able to use a configuration of visual cues to find the hidden platform. Moreover, we demonstrate that they chose direct paths to the goal from multiple random initial positions, a hallmark of a cognitive map. The performance of the frogs in the maze was qualitatively similar to that of rodents, suggesting that the potential to evolve a cognitive map is an evolutionarily conserved trait of vertebrates.
... Familiar landscape features within a novel environment can provide orientation cues that direct movement towards suitable resources and thus enhance fitness (Marable et al. 2012). Abiotic factors such as temperature (Attum et al. 2011) and landscape permeability (Nowakowski et al. 2013;Attum and Cutshall 2015) can further influence dispersal following translocation. ...
... "Landscape resistance" studies frequently report variability in dispersal rates through habitats that differ in structural attributes. For example, poison dart frogs are less willing to move through pasture than through woodland (Nowakowski et al. 2013), while the movement rate of Parnassius butterflies halved in dense woodland compared to more open meadows (Roland et al. 2000). Additionally, thermal variation between habitat types may have played a role in determining the cane toad's dispersal characteristics. ...
Article
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Biological invasions transport organisms to novel environments; but how does the translocation process influence movement patterns of the invader? Plausibly, the stress of encountering a novel environment, or of the transport process, might induce rapid dispersal from the release site—potentially enhancing (or reducing) invader success and spread. We investigated the effect of transportation and release to novel environments on dispersal-relevant traits of one of the world’s most notorious invaders, the cane toad (Rhinella marina). We collected toads in northern New South Wales from heath and woodland habitats, manipulated the level of transport stress and either returned toads to their exact collection point (residents) or reciprocally translocated them to a novel site. Both translocation and the level of transport stress drastically altered toad dispersal rates for at least 5 days post-release. Translocated toads (depending on their level of transport stress and release habitat) moved on average two to five times further per day (mean range 67–148 m) than did residents (mean range 22–34 m). Translocated toads also moved on more days, and moved further from their release point than did resident toads, but did not move in straighter lines. A higher level of transport stress (simulating long-distance translocation) had no significant effect on movements of resident toads but amplified the dispersal of translocated toads only when released into woodland habitat. These behavioural shifts induced by translocation and transportation may affect an invader’s ability to colonise novel sites, and need to be incorporated into plans for invader control.
... Trials were initiated by placing a frog at one end of the enclosure, and a standardized stimulus was applied to ensure continued movement across the length of the enclosure (e.g. Nowakowski et al. 2013). Longer travel times were assumed to indicate greater physical resistance of substrates to movement. ...
... We conclude that when possible, the use of empirically derived resistance surfaces will allow for clearer interpretation of processes underlying landscape connectivity compared to the use of expert opinion and model-fitting methods. This study and previous work suggest that pastures can represent inimical habitat and impede gene flow for some forest species (Felton et al. 2010;Nowakowski et al. 2013). Programmes that incentivize conversion of pastures to secondary forest and tree plantations should improve habitat connectivity by simultaneously increasing tree cover and decreasing extent of pastures on the landscape. ...
Article
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Conversion of forests to agriculture often fragments distributions of forest species and can disrupt gene flow. We examined effects of prevalent land uses on genetic connectivity of two amphibian species in northeastern Costa Rica. We incorporated data from field surveys and experiments to develop resistance surfaces that represent local mechanisms hypothesized to modify dispersal success of amphibians, such as habitat-specific predation and desiccation risk. Because time lags can exist between forest conversion and genetic responses, we evaluated landscape effects using land-cover data from different time periods. Populations of both species were structured at similar spatial scales but exhibited differing responses to landscape features. Litter frog population differentiation was significantly related to landscape resistances estimated from abundance and experiment data. Model support was highest for experiment-derived surfaces that represented responses to microclimate variation. Litter frog genetic variation was best explained by contemporary landscape configuration, indicating rapid population response to land-use change. Poison frog genetic structure was strongly associated with geographic isolation, which explained up to 45% of genetic variation, and long-standing barriers, such as rivers and mountains. However, there was also partial support for abundance and microclimate response derived resistances. Differences in species responses to landscape features may be explained by overriding effects of population size on patterns of differentiation for poison frogs, but not litter frogs. In addition, pastures are likely semi-permeable to poison frog gene flow because the species is known to use pastures when remnant vegetation is present, but litter frogs do not. Ongoing reforestation efforts will likely increase connectivity in the region by increasing tree cover and reducing area of pastures.This article is protected by copyright. All rights reserved.
... Males that occupy such territories have superior fighting abilities (Meuche et al. 2012); not as much is known about female territoriality. Nowakowski et al. (2013) conducted an experiment where the researchers caught frogs in the forest and released them onto a novel platform in either forest or pasture. Although this study found that frogs perceive greater risk in forest (as they jumped off the pasture platform much faster), they also found that some males chose to remain in the pasture, "potentially to avoid competition with frogs defending territories in the forest" (Nowakowski et al. 2013). ...
... Nowakowski et al. (2013) conducted an experiment where the researchers caught frogs in the forest and released them onto a novel platform in either forest or pasture. Although this study found that frogs perceive greater risk in forest (as they jumped off the pasture platform much faster), they also found that some males chose to remain in the pasture, "potentially to avoid competition with frogs defending territories in the forest" (Nowakowski et al. 2013). In La Selva, we may be witnessing a similar phenomenon. ...
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Tree growth is limited by phosphorus and nitrogen in the soil. The abundance of these nutrients in tropical forest floors is often spatially heterogeneous. pH is also spatially heterogeneous, and it influences the bioavailability of nutrients to plants and microorganisms. Pockets of high nutrient concentration and favorable pH in forest floors correlate with forest productivity and the abundance of certain species . Identifying why nutrients accumulate in certain areas will be useful for understanding patterns of plant productivity and community composition. Bat guano is rich in nitrogen and phosphorus and has a near-neutral pH. We investigated if bat guano deposited under hollow trees with bat roosts in them influenced soil pH and the concentration of nitrogen and phosphorus in the soil. We found the highest pH and concentrations of nitrate and phosphate directly under the bat roosts, with steep drop-offs in these values radially 1 m and 3 m from the hollow tree boles. The nitrate, phosphate, and pH concentrations at 1 m and 3m were comparable outside of hollow or control trees that lacked hollows. Thus, bat guano strongly influences soil properties, but the effects are highly localized to the hollow tree centers. Our findings revealed that bat guano contributes to spatial heterogeneity in nutrient concentrations in tropical lowland forest soils.
... However, behavioral avoidance of contaminated areas also has the potential to alter local amphibian abundance and community structure (Rohr and Crumrine 2005;Vonesh and Kraus 2009), effectively reducing available habitat area. Behavioral avoidance may also increase resistance to movement associated with contaminated agricultural areas ( Nowakowski et al. 2013). Finally, the possibility of a sexually dimorphic response to herbicide cues, as suggested by the results of this study, could result in sex-biased dispersal and habitat selection, which can also alter community dynamics and structure. ...
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Recent research has focused on the importance of behavior in mediating the effects of landscape change on amphibian populations and communities. Factors such as chemical contaminants may affect habitat selection and movement of amphibians in human-altered habitats and contribute to landscape-level patterns of distribution and abundance. The objective of this study was to determine if the Strawberry Poison Frog (Oophaga pumilio (Schmidt, 1857)) can use olfactory cues to detect and avoid the glyphosate-based herbicide Roundup™. Fifty frogs were captured in the field in Costa Rica and tested in experimental arenas where they were given a choice between a control and an herbicide treatment. Analysis of time spent in treatment areas revealed a significant interaction between sex and treatment. Analyses of choice at the start and end of the trials indicated that sex and cardinal direction were important factors influencing orientation behavior. These results suggest that males and females differed in their behavioral responses, and that male O. pumilio may use olfactory cues to detect and avoid areas treated with glyphosate-based herbicide. However, the sampled population was male-biased, which resulted in a lower sample size and lower power to detect an effect for females. Further work is needed to better understand amphibian behavioral responses to herbicides, as well as the role of sex and individual variation in modifying these responses.
... Functional connectivity varies among species, as it is influenced by factors such as vagility, 56 tolerance to stress, perception of risk and susceptibility to competition and predation. Accepting that connectivity depends on the perception of individuals and their responses to landscape 58 Nowakowski et al. 2013), fish (Turgeon et al. 2010, Shima et al. 2012) and insects (Berggren features are infrequently crossed because they are true barriers, or whether there is simply no motivation to move (e.g., individuals may have sufficient resources without needing to 81 cross these features). Translocations are also more logistically efficient as they allow researchers 82 to randomly or opportunistically place animals directly in landscape contexts of interest. ...
Article
Translocation experiments, in which researchers displace animals and then monitor their movements to return home, are commonly used as tools to assess functional connectivity of fragmented landscapes. Such experiments are purported to have important advantages of being time efficient and of standardizing "motivation" to move across individuals. Yet, we lack tests of whether movement behavior of translocated birds reflects natural behavior of unmanipulated birds. We compared the routine movement behavior of a tropical hummingbird, the Green Hermit (Phaethornis guy), to that of experimentally translocated individuals. We tested for differences in site selection patterns during movement at two spatial scales (point and path levels). We also compared movement rates between treatments. Behaviors documented during translocation experiments reflected those observed during routine movements. At the point level, both translocated and non-translocated birds showed similar levels of preference for mature tropical forest. At the path level, step selection functions showed both translocated and non-translocated hummingbirds avoiding movement across non-forested matrix and selecting streams as movement corridors. Movement rates were generally higher during translocation experiments. However, the negative influence of forest cover on movement rates was proportionately similar in translocation and routine movement treatments. We report the first evidence showing that movement behavior of birds during translocation experiments is similar to their natural movement behavior. Therefore, translocation experiments may be reliable tools to address effects of landscape structure on animal movement. We observed consistent selection of landscape elements between translocated and non-translocated birds, indicating that both routine and translocation movement studies lead to similar conclusions regarding the effect of landscape structure and forest composition on functional connectivity. Our observation that hummingbirds avoid non-forest matrix and select riparian corridors also provides a potential mechanism for pollen limitation in fragmented tropical forest.
... Experimental translocations are becoming increasingly prevalent in landscape ecology, and they have been used to study functional connectivity for a wide variety of species including mammals (Bowman and Fahrig 2002;McDonald and St. Clair 2004;Smith et al. 2011;Bridgman et al. 2012;Lawes et al. 2013;Smith et al. 2013), temperate and tropical birds (Ibarra-Macias et al. 2011;Kennedy et al. 2011;Bridgman et al. 2012), reptiles (Butler et al. 2005;Brown et al. 2009), amphibians (Huste et al. 2006;Nowakowski et al. 2013), fish (Turgeon et al. 2010), and insects (Conradt et al. 2000;Haynes and Cronin 2006;Fletcher et al. 2013). Using this technique, researchers have assessed the importance of matrix type in facilitating animal movement (Aben et al. 2012;Castellon and Sieving 2006;Kennedy and Marra 2010;Tremblay and St. Clair 2011), reluctance to move through open areas (Desrochers et al. 2011;Smith et al. 2013), the utility of stepping stones to increase connectivity (Boscolo et al. 2008;Gillies and St. Clair 2010), selection of forest fragments while travelling (Hadley and Betts 2009;Gilles et al. 2011;Ibarra-Macias et al. 2011), and landscape isotropy (Bélisle and St. Clair 2001). ...
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Context Functional connectivity reflects the ease with which an organism can access different locations within its environment. Because functional connectivity can significantly influence dispersal, habitat selection, and ultimately the viability of populations, it is central to understanding and predicting biological responses to anthropogenic disturbance. Currently, no consensus exists on how to measure functional connectivity. Objectives and methods Species-centered approaches such as translocation experiments have recently been advocated because they enable strong inferences about functional connectivity. The use of these types of experiments is increasing rapidly, but to date there has been no synthesis of the wide range of methods available to minimize possible study design problems. Here, we review the recent literature on translocation experiments and highlight potential confounds that may lead to inappropriate conclusions from translocation studies. Results We report several approaches that can limit the degree to which these confounds affect inferences. We briefly describe paired and repeated-measures designs that use mixed models to address lack of spatial and temporal independence as means for coping with confounds. Conclusions Such approaches to the design and analyses of translocation experiments should facilitate high-quality measurements of landscape functional connectivity. We encourage investigators to continue functional connectivity research that capitalizes on the advantages of translocations while applying rigorous study designs.
... Although niche processes are the most important factor controlling anuran metacommunity structure, it is important to analyse spatial effects, at least in open regions. An interesting perspective is to compare these patterns, using the same protocol, with patterns observed in forested systems, in which anuran dispersal is less limited (Rothermel & Semlitsch 2002;Nowakowski et al. 2013) and could consequently reduce the importance of the neutral component of metacommunity structure. ...
Article
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One of the most important questions in ecology is the relative importance of local conditions (niche processes) and dispersal ability (neutral processes) in driving metacommunity structure. Although many studies have been conducted in recent years, there is still much debate. We evaluated the processes (niche and neutral) responsible for variation in anuran composition in 28 lentic water bodies in southeastern Brazil. Because anurans depend heavily on environmental conditions, we hypothesized that environmental variables (niche processes) are the most important drivers of community composition. Additionally, as anurans have limited dispersal abilities, and the study region presents harsh conditions (high forest fragmentation, low rainfall and long dry season), we expected a lower, but significant, spatial signature in metacommunity structure, due to neutral dynamics. We used a partial redundancy analysis with variation partitioning to evaluate the relative influence of environmental and spatial variables as drivers of metacommunity structure. Additionally, we used a recently developed spatial autocorrelation analysis to test if neutral dynamics can be attributed to the pure spatial component. This analysis is based on predictions that species abundances are independent but similarly spatially structured, with correlograms similar in shape. Therefore, under neutral dynamics there is no expectation of a correlation between the pairwise distance of spatial correlograms and the pairwise correlation of species abundances predicted by the pure spatial component. We found that the environmental component explained 21.5%, the spatial component 10.2%, and the shared component 6.4% of the metacommunity structure. We found no correlation between correlograms and correlation of abundances predicted by the pure spatial component (Mantel test = −0.109, P = 0.961). In our study, niche-based processes are the dominant process that explained community composition. However, neutral processes are important because spatial variation can be attributed to pure neutral dynamics rather than to missing spatially structured environmental factors.
... Desiccation resistance may influence how species use the matrix separating habitat patches, because relatively open vegetation types such as grassland may induce high rates of water loss that limit interpatch movements (Rothermel and Semlitsch 2002;Cosentino et al. 2011;Nowakowski et al. 2013;Lee-Yaw et al. 2015). When the matrix is relatively xeric, isolated patches may be unavailable for either initial colonization or demographic rescue by desiccationprone species. ...
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Context Although amphibian distributions are associated with environmental moisture at global and local scales, less is known about how desiccation tolerance influences landscape distributions of amphibians. Objectives We evaluated two hypotheses linking amphibian distributions in a fragmented tropical forest landscape to desiccation risk. The patch quality hypothesis predicts that desiccation-prone species are absent on small forest patches, which are generally warmer and drier than large patches. Alternatively, the matrix effects hypothesis suggests that desiccation-prone species are absent on isolated forest patches surrounded by open savanna because they will be unable to traverse the matrix in which patches occur. Methods We quantified interspecific variation in desiccation proneness using field-based desiccation trials, and tested for associations between desiccation proneness and distributions of amphibians in fragmented forest in northeastern Bolivia. Results Rates of evaporative water loss were negatively associated with an index of dispersal limitation, but unrelated to species’ area requirements. Conclusions By demonstrating that desiccation-prone species do not occur on isolated forest patches, we provide clear support for the matrix effects hypothesis. We suggest that desiccation proneness is a key trait that may determine amphibian responses to a range of global change drivers, including habitat loss and fragmentation, invasive species, and climate change.
... Conversion of forested habitats to human land-uses is a primary cause of amphibian declines in tropical regions (Alford and Richards 1999;Vié et al. 2009;Robinson et al. 2013;Kurz et al. 2014). Amphibians may be susceptible to habitat alterations because of their sensitivity to microclimate changes, limited dispersal capacities, and high susceptibility to desiccation (Nowakowski et al. 2013;Robinson et al. 2013;Mendenhall et al. 2014). Previous studies at tropical latitudes have shown that human habitat disturbance generates changes in the structure and composition of amphibian ensembles, promotes the spread of generalists and alien species, and probably leads to local extinctions of species (Urbina-Cardona et al. 2006;Isaacs and Urbina-Cardona 2011;Cortés-Gómez et al. 2013). ...
... Studies on movement of amphibians through modified landscapes have pointed to the importance of vegetation structure and individual traits of species on ease of movement (Roznik and Johnson, 2009;Youngquist and Boone, 2014). Open canopy habitats, such as wooded grasslands, tend to have higher temperatures and lower humidity, resulting in greater desiccation risk (Cosentino, Schooley and Phillips, 2010;Tingley and Shine, 2011;Nowakowski et al., 2013). Therefore, dispersing amphibians may be more willing to use good-quality habitats, such as forested patches. ...
Article
Land use change has been identified as a major driver of amphibian decline around the world. Yet we generally lack an understanding of how conversion to exotic pastures affects freshwater communities. This study examined tadpole assemblages in areas converted to exotic pastures and native wooded grasslands in northern Pantanal wetland, Midwestern Brazil. We tested the differences in site occupancy probability and assemblage composition during a flood season. We registered thirteen tadpole species, but only five were detected at levels suitable for occupancy modelling. For most species, tadpole occupancy was higher at the beginning of the flood season. Only Scinax fuscomarginatus occupancy was related with vegetation cover. Occupancy probability for three species (Dendropsophus nanus, Physalaemus centralis, and Physalaemus cuvieri) was associated positively with species richness of fish. Multivariate analyses demonstrated that exotic pastures hosted a different tadpole assemblage than native areas. The assemblage composition gradient was associated with species richness of fish, vegetation cover and volume of herbaceous vegetation and leaf litter. These differences likely relate to specific traits of individual anuran species (dietary plasticity, reproductive mode, and habitat preference). The study showed that some generalist species were able to cope with replacement of native vegetation by exotic species. However, management practices have maintained many areas in the Pantanal at a stage of a near-pristine wetland ecosystem and replacement of native vegetation by exotic pastures should be done with caution.
... Maximum daytime temperatures (1 m from ground) in pasture are up to 10°C higher than in forest, though nighttime temperatures are comparable (Robinson et al., 2013). High risk of thermal stress coupled with few refuge sites (e.g., tree holes and leaf litter) in pasture are likely to constrain population sizes and limit dispersal success of reptiles and amphibians (Blaustein et al., 2010;Nowakowski et al., 2013b). Previous studies in similar tropical systems have also reported that pastures supported lower overall richness (Kanowski et al., 2006;Urbina-Cardona et al., 2006) and abundance (Toral et al., 2002;Kanowski et al., 2006;Herrera-Montes and Brokaw, 2010) of herpetofauna by comparison with forest. ...
... The station is a 1600-hectare reserve consisting of primarily old growth tropical wet forest in the Caribbean lowlands [36]. Much of the land surrounding La Selva has been deforested and converted to agriculture -primarily cattle pastures and plantations of banana, pineapple, and palm heart [36][37][38]. While there has been no significant usage of pesticides within the La Selva reserve, aerial drift from nearby agricultural plantations results in residues of several current use and legacy pesticides in La Selva air and soil [19,20,39] We constructed nine water baths each with a different temperature regime in a climate controlled laboratory at La Selva. ...
Article
Amphibian populations are declining globally, and multiple anthropogenic stressors, including contamination by pesticides and shifting climates are driving these declines. Climate change may increase average temperatures or increase temperature variability, either of which may affect susceptibility of non-target organisms to contaminants. We conducted 8-day ecotoxicological assays with red-eyed treefrog (Agalychnis callidryas) larvae to test for additive and interactive effects of exposure to the fungicide chlorothalonil, average temperature, and temperature variability on tadpole growth and survival. We collected egg masses from seasonal ponds at La Selva Biological Station in Costa Rica and exposed tadpoles to a series of chlorothalonil concentrations across a range of ecologically-relevant mean temperatures (23.4 - 27.3°C) and daily temperature fluctuations (1.1 - 9.9°C). We measured survival each day and measured tadpole growth at the end of each trial. Concentrations of chlorothalonil ≥60µg/L reduced survival, though survival was not affected by mean temperature or daily temperature range, and there were no synergistic interactions between chlorothalonil and temperature regime on survival. Chlorothalonil suppressed tadpole growth at relatively low concentrations (∼15µg/L). There were impacts of both average temperature and daily temperature range on tadpole growth, though there were no synergistic interactions between temperature regimes and chlorothalonil. Our study should inform efforts to manage ecosystems impacted by multiple large-scale anthropogenic stressors as well as methods for the design of ecologically-appropriate toxicology trials. This article is protected by copyright. All rights reserved.
... Individuals in directed mode are likely to display edge-mediated movement behavior and may be less willing to enter poor-quality habitat (DeMaynadier and Hunter, 1999;Stevens et al., 2006;Popescu and Hunter, 2011). This movement can be characterized using correlated random walk models with the inclusion of a bias parameter or advection toward important habitat features (Bartoń et al., 2009;Chapman et al., 2007;Crone and Schultz, 2008;Haddad, 1999); biased movement toward quality habitat has been documented in both temperate Rittenhouse and Semlitsch, 2006), and tropical amphibian species (Nowakowski et al., 2013). ...
... Bell and Donnelly (2006) also found evidence for a deterministic subset of species which are particularly vulnerable to loss in small fragments, and that this subset represents all major families and reproductive modes. Nowakowski et al. (2013) compared landscape type (closed-canopy forest or open pasture) on movement in Oophaga pumilio in northeastern Costa Rica and showed that pasture microhabitats negatively impacted movement in this species, suggesting that forest fragments nested within pastures may show limited connectivity. However, Robinson et al. (2013) showed that individual remnant trees within pasture habitats provide important habitat for Oophaga pumilio and may allow this species to disperse through pasture by moving among individual trees (i.e., island hopping). ...
Article
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Central America hosts a diverse, unique, and imperiled amphibian fauna, and for decades Central America been a major epicenter of research into amphibian decline and conservation. In this critical and quantitative review, we synthesize current knowledge regarding amphibian decline and conservation in the seven countries that constitute Central America. There are 495 currently recognized amphibian species known from the region, distributed among the three extant orders, 16 families, and 69 genera—though description of new species continues to occur at a rapid pace. Central America's amphibian fauna is unique: 251 species are restricted to the region, and amphibian diversity varies among the major biogeographic provinces and climatic zones found in Central America. We use data generated by the International Union for the Conservation of Nature (IUCN) to evaluate trends in extinction risk among Central American amphibians. As of 2014, there are 207 amphibian species considered threatened by the IUCN, and threat status varies according to taxonomic groupings, biogeographical association, elevation, and life history variables. Major threats to Central American amphibians include both conventional threats (habitat modification, habitat fragmentation, overharvesting, and invasive species) as well as emerging threats that operate on large spatial scales (pollution, emerging infectious diseases, UV-B radiation, and climate change). We conducted a quantitative literature review to document conservation research and to show trends in research activity. While the number of published studies on amphibian conservation increases each year, there are pronounced biogeographic biases in the distribution of published research, and most research is conducted by scientists at institutions outside of Central America with limited involvement of host-nation biologists in amphibian research. We synthesize empirical studies of conservation impacts to amphibians in Central America from habitat modification and fragmentation, overharvesting, invasive species, pollution, UV-B radiation, chytridiomycosis and other amphibian pathogens, climate change, and synergistic interactions among these threats. Much research in the past decade has focused on chytridiomycosis and the amphibian chytrid fungus (Batrachochytrium dendrobatidis), with far fewer studies on habitat modification, other amphibian pathogens, or climate change impacts to amphibians. We describe ongoing conservation actions for amphibians in the region, including monitoring, protected areas, captive assurance programs, protection of relict populations, reintroductions, and development of in-country capacity for research and conservation programs. We conclude with a list of priorities in research and conservation action for amphibians in the region.
... coloration, advertisement and mating calls) and strong genetic divergence have been driven quite rapidly in this group (1000-10,000 years) (Summers et al., 1997;Wang & Shaffer, 2008); comparative evidence suggests that on average, the achievement of complete secondary sympatry in the tropics takes on the order of millions of years (Weir & Price, 2011). This argument is likely to be particularly relevant in the case of Oophaga poison frogs, given the limited dispersal capacity of amphibians (Pyron & Wiens, 2013) and the lower levels of vagility when compared with other taxa (a mark-recapture study in O. pumilio showed that 70% of the recaptured individuals were found < 20 m from the marking site) (Nowakowski et al., 2013). Thus, it is likely that speciation with gene flow has played a key role in the diversification of these two Oophaga clades. ...
Article
Aim: Despite the incredible diversity of lowland tropical rain forests, we still have limited understanding of the drivers of speciation in these ecoregions. Here, we investigated the relative contribution of geographical and environmental factors to the diversification of a Neotropical genus of poison frogs (Oophaga). Location: Central and South America, including regions from southern Nicaragua to northern Ecuador. Methods: We generated gene genealogies (12S, 16S, COI, CytB and tRNA-val, SIAH1, H3 and Rag1) and used species phylogenetic methods (MDC and *beast) to generate a robust phylogeny of Oophaga frogs. Then, we combined the resulting phylogenetic hypothesis with detailed geographical data and environmental niche modelling (ENM) to test the role of geographical isolation, climatic niche divergence and altitudinal gradients. Results: Gene genealogies were discordant and did not show exclusive genealogical patterns; however, species tree resolved the phylogenetic relationship among Oophaga species with strong node support (> 0.9 ML/BPP). Geographical ranges showed little overlap between distantly related species. However, within the South American and Central American clades, sister taxa showed substantially overlapping ranges. Analyses of ecological disparity (DTT) indicated a departure from a neutral (Brownian) model of evolution, and age-range correlations, predicted niche occupancy profiles, and Seeva analyses showed that different species tend to evolve under different potential climatic niches. Main conclusions: Oophaga frogs originated in Central America and reached South America after the closure of the Panama Isthmus. The South- and Central-American clades of this genus have convergently evolved to similar patterns of geographical distribution and niche occupancy. Within clades, sister taxa showed parapatric distributions replacing each other along elevational gradients as predicted by the models of divergence along continuous ecological gradients. Accordingly, we found strong shifts in climatic niches throughout the history of these two clades. However, the largest niche shifts seem to post-date the final elevation of the Talamanca and northern Andes. Overall, our data suggest that speciation along climatic gradients on a structured landscape has been a major evolutionary force behind the diversification of Oophaga poison frogs.
... Finally, human-transformed habitats may also affect parents' orientation capacity by attenuating their familiarity with sensory cues. For example in Oophaga pumilio, orientation depends both on the distance and the habitat type (forests or pastures) (Nowakowski et al. 2013). Thus, given that males often select tadpole deposition sites outside of their territories or core areas (Ringler et al. 2013;Pašukonis et al. 2019), parents' ability to find good rearing sites in the first place, or to return to selected phytotelmata in the case of tadpole feeding species, could be impaired. ...
Article
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The current and cascading effects of global change challenges the interactions both between animal individuals (i.e. social and sexual behaviour) and the environment they inhabit. Amphibians are an ecologically diverse class with a wide range of social and sexual behaviours, making them a compelling model to understand the potential adaptations of animals faced with the effects of human-induced rapid environmental changes (HIREC). Poison frogs (Dendrobatoidea) are a particularly interesting system, as they display diverse social behaviours that are shaped by conspecific and environmental interactions, thus offering a tractable system to investigate how closely related species may respond to the impacts of HIREC. Here, we discuss the potential impacts of global change on poison frog behaviour, and the future challenges this group may face in response to such change. We pay special attention to parental care and territoriality, which are emblematic of this clade, and consider how different species may flexibly respond and adapt to increasingly frequent and diverse anthropogenic stress. More specifically, we hypothesise that some parents may increase care (i.e. clutch attendance and distance travelled for tadpole transport) in HIREC scenarios and that species with more generalist oviposition and tadpole deposition behaviours may fare more positively than their less flexible counterparts; we predict that the latter may either face increased competition for resources limited by HIREC or will be forced to adapt and expand their natural preferences. Likewise, we hypothesise that human-driven habitat alteration will disrupt the acoustic and visual communication systems due to increased noise pollution and/or changes in the surrounding light environment. We highlight the need for more empirical research combining behavioural ecology and conservation to better predict species’ vulnerability to global change and efficiently focus conservation efforts.
... Deforestation may also affect the effective distances between current climates and their future analogs through the creation of migration barriers. The idea that the movement or dispersal of forest organisms will be impeded by deforestation is consistent with the findings of previous studies which have shown that individuals of many different tropical animal groups including birds (Willis, 1974;Laurance et al., 2004;Lees & Peres, 2009), mammals (Laurance & Laurance, 1999;de Lima & Gascon, 1999), frogs (de Lima & Gascon, 1999;Nowakowski et al., 2012), and insects (Hill, 1995;Larsen et al., 2005;Larsen, 2012), all actively avoid forest edges. In the case of forest plants, deforestation can create unsuitable habitats which can only be crossed through seed dispersal but this dispersal may be hindered if animal dispersers are unable or unwilling to cross deforested areas (McConkey et al., 2012). ...
Article
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Species migrations in response to climate change have already been observed in many taxonomic groups worldwide. However, it remains uncertain if species will be able to keep pace with future climate change. Keeping pace will be especially challenging for tropical lowland rainforests due to their high velocities of climate change combined with high rates of deforestation, which may eliminate potential climate analogs and/or increase the effective distances between analogs by blocking species movements. Here, we calculate the distances between current and future climate analogs under various climate change and deforestation scenarios. Under even the most sanguine of climate change models (IPSL_CM4, A1b emissions scenario), we find that the median distance between areas in the Amazon rainforest and their closest future (2050) climate analog as predicted based on just temperature changes alone is nearly 300 km. If we include precipitation, the median distance increases by over 50% to >475 km. Since deforestation is generally concentrated in the hottest and driest portions of the Amazon, we predict that the habitat loss will have little direct impact on distances between climate analogs. If, however, deforested areas also act as a barrier to species movements, nearly 30% or 55% of the Amazon will effectively have no climate analogs anywhere in tropical South America under projections of reduced or Business-As-Usual deforestation, respectively. These ‘disappearing climates’ will be concentrated primarily in the southeastern Amazon. Consequently, we predict that several Amazonian ecoregions will have no areas with future climate analogs, greatly increasing the vulnerability of any populations or species specialized on these conditions. These results highlight the importance of including multiple climatic factors and human land-use in predicting the effects of climate change, as well as the daunting challenges that Amazonian diversity faces in the near future.
... Body size determines which microhabitats and what spatial and temporal scales are relevant for thermoregulation and highly mobile animals will be able to sample larger spatial extents than more sedentary species. When navigating heterogenous landscapes, perceptual range of an organism will limit ability to detect available microhabitats, increasing search times, and thereby modify relative costs of thermoregulation [137][138][139]. However, few comprehensive examinations of the energetic costs of thermoregulation in humanaltered landscapes exist, and quantifying these costs remains necessary for predicting the consequences for populations in changing thermal landscapes. ...
Article
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Climate change and habitat modification both alter thermal environments and species distributions. However, these drivers of global change are rarely studied together, even though many species are experiencing climate change and habitat modification simultaneously. Here we review existing literature and propose avenues for merging the largely disparate lines of climate and landscape ecological research using temperature exposure and species’ thermal sensitivity as a shared framework. The integration of research on climate and landscape change is in the early stages and lags behind research focused solely on the ecological effects of climate change. Recent studies highlight important mismatches between the resolution of widely used climate datasets and ecological processes, which can be addressed through detailed mapping of thermal landscapes and the microclimates within them. Furthermore, the thermal niches of species, evolved under past climates, can predict the responses of species to changing microclimates associated with habitat modification; this suggests that microclimates and thermal niches may together act as a common filter, reassembling communities in response to both climate and landscape change. There is a need to further integrate microclimate and thermal niche data into landscape ecological research to advance our basic understanding of the combined effects of landscape and climate change and to provide actionable data for climate adaptation strategies that largely focus on activities at landscape scales.
... Anurans exhibit multiple types of parental care strategies and are distributed across diverse habitats, including some that feature harsh environmental conditions where many other animals are absent (Wells 2007;Vitt and Caldwell 2014). Homing in anurans has been studied for decades in temperate region species (McAtee 1921;Jameson 1957;Dole 1968;Grubb 1975;Sinsch 1987Sinsch , 2014 and recently in poison frogs of the family Dendrobatidae (McVey et al. 1981;Nowakowski et al. 2013;Pašukonis et al. 2013Pašukonis et al. , 2016Pašukonis et al. , 2018Pašukonis et al. , 2019Pichler et al. 2017;Nothacker et al. 2018;Arcila-Pérez et al. 2020). These studies, however, have examined homing mechanisms and patterns without robustly investigating how homing behavior interacts with parental care (but see McVey et al. 1981;Navarro-Salcedo et al. 2021). ...
Article
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Parental care directly affects the fitness of individuals because it increases the probability of offspring survival. Therefore, it is expected that parents be particularly motivated to return (i.e., exhibit homing behavior) and resume care if they are moved away from offspring by disturbances. Yet, despite several studies on the behavioral ecology of homing in vertebrates, aspects underlying the relationship between movement and offspring care in anurans remain largely unknown. We tested the relative importance of parental care as a driver of homing in Ikakogi tayrona, the only glassfrog with demonstrated prolonged maternal care. We carried out translocation experiments in 58 calling males, 23 gravid females, and 19 females caring for eggs. Contrary to expectations, females did not exhibit homing despite the risk of increased offspring mortality. On the other hand, males exhibit homing (they returned from translocation distances up to 320 m), possibly to recover a specific territory that is important for attracting mates. Taken together, our work documents a paradoxical result that may lead to future research testing specific hypothesis about the causes of sex differences in homing and the associated cognitive process. Significance statement Studying the relationship between parental care and homing behavior provides a better understanding of how diverse ecological and evolutionary factors influence movement patterns in animals. However, such relationship has been almost untested in anurans, even though their homing behavior and diversity of parental care strategies have separately received great attention from behavioral ecologists. In this study, we found sex differences in homing for the glassfrog Ikakogi tayrona. Males are highly motivated to return to a specific territory, possibly to recover a particular place from which they increase mating opportunities. Interestingly, females caring for eggs did not exhibit homing, even if that behavioral decision results in higher mortality rates of offspring in their clutches, as demonstrated in this and other glassfrogs. This work is one of the few studies on homing in anurans that includes a large sample size of females and accounts for both gravid females and females already caring for offspring. Altogether, this study broadens our understanding of how ecological and evolutionary factors can influence homing behavior in vertebrates.
... During the contest stage ( Figure 2 Step 5), we simultaneously released the original (the removed male) and the new occupant (the newly established male) to their point of capture, staging a contest between the two males. Because O. pumilio have good spatial memory and homing behavior (Mcvey et al., 1981;Nowakowski et al., 2013), both males likely recognized the release location as their territory. We observed both escalated physical combat and non-escalated contest resolution between the two individuals we released on several occasions. ...
Article
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in aggression level, suggesting a potential dominance hierarchy between these di- vergent phenotypes. In a contact zone between red and blue-color morphs, we first removed territorial males from their calling sites, and examined whether certain color morph(s) were better at establishing in these now-vacant territories. We then staged a territorial contest by simultaneously releasing the original and the new occupant to their point of capture. Surprisingly, we found no significant effect of color on ac- quiring territories or winning staged contests. However, the original occupants won against the new occupant in 84% of the staged contests, revealing a strong prior resi- dence effect. This suggests that asymmetries that stem from prior residency over- ride coloration in predicting contest outcomes of male–male territorial contests in wild O. pumilio. Thus, contradicting our hypothesis, male–male territorial competition alone seems unlikely to exert selection on coloration in this contact zone. K
... With habitat fragmentation, areas used for breeding and to obtain other resources are disconnected, causing increased mortality due to desiccation and predation mainly (BECKER et al. 2007;BECKER et al. 2010). As the species do not respond similarly to matrix presence (NOWAKOWSKI et al. 2013;LEE-YAW et al. 2015) there may be a difference in the composition of amphibian communities in accordance with the surrounding landscape (MANENTI 2013;D'ANUNCIAÇÃO et al. 2013). In addition, many amphibians are cryptic and difficult to detect causing not only the underestimation of specie presence, but also misleading conclusions about the spatial "Ecology in the Anthropocene" gy p 16-19 August 2016 -São Carlos -SP -P II International Symposium of Ecology g g distribution of species and associations with forest fragment attributes of landscape (MOILANEN 2002;MAZEROLLE et al. 2005). ...
Conference Paper
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Fragmentation process and habitat loss, are recognized as one of the main threats to biodiversity, leading to the formation of different types of matrix surrounding forest fragments. Because of their life history characteristics, amphibians are particularly sensitive to habitat changes. The aim of this study was to understand how the different types of matrix affects the amphibians occupancy. We created a buffer of 500 m surrounding each forest fragment and we determined the proportion of each land use type and water bodies. For Rhinella ornata the percentage of water bodies influence positively. For Proceratophrys boiei the reservoir influences in a negative way, and for Haddadus binotatus the null model was the most plausible. The influence of matrix's type is species-specific and probably dependent on the type of reproductive mode exhibited by each species. It is clear that conservation and management measures must consider the species present in the region and not the group as a whole.
... However, few previous studies have investigated the relationship between landscape heterogeneity and the body condition of anurans. Agricultural landscapes with higher edge density might have a greater food availability and provide more refuge habitats for anurans (Nowakowski et al. 2013;Molina et al. 2014). It has also been hypothesized that anuran species might benefit from smaller field edge habitats, which could facilitate movement through the landscape and decrease energy consumption (Collins and Fahrig 2017). ...
Article
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Amphibians play a key role in structuring biological assemblages of agricultural landscapes, but they are threatened by global agricultural intensification. Landscape structure is an important variable influencing biodiversity in agricultural landscapes. However, in the Yangtze River Delta, where a ‘farmland-orchard-fishpond’ agricultural pattern is common, the effects of landscape construction on anuran populations are unclear. In this study, we examined the effects of agricultural landscape parameters on the abundance and body condition of the rice frog (Fejervarya multistriata), which is a dominant anuran species in farmland in China. Employing a visual encounter method, we surveyed rice frog abundance for three years across 20 agricultural landscapes. We also calculated the body condition index (BCI) of 188 male frog individuals from these agricultural landscapes. Landscape variables, comprising landscape compositional heterogeneity (using the Shannon diversity index of all land cover types except buildings and roads), landscape configurational heterogeneity (using landscape edge density), breeding habitat diversity (using the number of five waterbody types available as breeding habitats), and areas of forest were also measured for each 1-km radius landscape. We found that the amount of forest in each agricultural landscape had a significant positive relationship with rice frog abundance, and breeding habitat diversity was positively related to the BCI of male rice frogs. However, body condition was negatively impacted by landscape configurational heterogeneity. Our results suggested the importance of non-agricultural habitats in agricultural landscapes, such as waterbodies and forest, to benefit rice frog population persistence.
... For example, movement may be a contributing factor in diet composition, as the related strawberry poison frog (O. pumilio) has been observed to move less in pasture land compared to forest habitats [45]. Indeed, we observed that frogs in the pasture were active for a shorter period of time in the morning compared to the forest frogs. ...
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Much of the world’s biodiversity is held within tropical rainforests, which are increasingly fragmented by agricultural practices. In these threatened landscapes, there are many organisms that acquire chemical defenses from their diet and are therefore intimately connected with their local food webs. Poison frogs (Family Dendrobatidae) are one such example, as they acquire alkaloid-based chemical defenses from their diet of leaf litter ants and mites. It is currently unknown how habitat fragmentation impacts chemical defense across trophic levels, from arthropods to frogs. We examined the chemical defenses and diet of the Diablito poison frog (Oophaga sylvatica), and the diversity of their leaf litter ant communities in secondary forest and reclaimed cattle pasture. Notably, this research was performed in collaboration with two high school science classrooms. We found that the leaf litter of forest and pasture frog habitats differed significantly in ant community structure. We also found that forest and pasture frogs differed significantly in diet and alkaloid profiles, where forest frogs contained more of specific alkaloids and ate more ants in both number and volume. Finally, ant species composition of frog diets resembled the surrounding leaf litter, but diets were less variable. This suggests that frogs tend to consume particular ant species within each habitat. To better understand how ants contribute to the alkaloid chemical profiles of frogs, we chemically profiled several ant species and found some alkaloids to be common across many ant species while others are restricted to a few species. At least one alkaloid (223H) found in ants from disturbed sites was also found in skins from pasture frogs. Our experiments are the first to link anthropogenic land use changes to dendrobatid poison frog chemical defenses through variation in leaf litter communities, which has implications for conservation management of these threatened amphibians.
... Temperature determines the rates of biochemical reactions, serves as a metabolic constraint, and often has an outsized effect on ecological parameters for both ectotherms and endotherms, including movement (Huey and Stevenson 1979;Angilletta Jr. et al. 2007;Angilletta Jr. and Angilletta 2009;Dillon et al. 2010;Nowakowski et al. 2013;Nowakowski et al. 2015;Frishkoff et al. 2019). The responses of animal populations to rapidly changing thermal environments will be shaped by their temperature exposure, which is determined by local microclimates and behavior, and their temperature sensitivity, which is governed by evolved thermal traits (Todd and Andrews 2008;Kearney et al. 2009;Huey et al. 2012;Scheffers et al. 2014). ...
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ContextThermal traits likely mediate organismal responses to changing thermal environments. As temperatures increase, predicting species responses will depend on understanding how thermal traits vary within and among individuals and across time and space.Objectives We evaluated variation in thermal traits within and among individual Mojave Desert Tortoises, using GPS telemetry to quantify movement performance and animal-mounted sensors to measure carapace temperatures.Methods We constructed thermal performance curves (TPCs) based on movement velocity and assessed variation in associated thermal traits by sex, season, and proximity to roads. We also examined the temperature-dependence of monthly home ranges and the frequency of high-displacement movements.ResultsIndividuals exhibited lower variation in upper critical temperatures (CTmaxE) than in other traits, such as optimum temperatures and lower critical temperatures for movement. All thermal traits varied within individuals, either by season or proximity to roads. We also found that monthly home range size and the frequency of high-displacement movements increased with the time individuals spent within their optimal temperature range; however, this effect was only apparent during months with greater rainfall.Conclusions Low standing variation in CTmaxE suggests that this trait may be constrained, limiting potential changes through acclimation or selection in warming environments. Our results demonstrate the modifying effect of rainfall on temperature-space use relationships and highlight the dependence of thermal traits on ecological and landscape contexts. Field-based TPCs derived from GPS movement tracks provided ecologically-relevant estimates of thermal traits and suggest an informative framework for unifying elements of thermal biology and spatial ecology.
... For example, movement may be a contributing factor in diet composition, as the related strawberry poison frog (O. pumilio) has been observed to move less in pasture land compared to forest habitats [42]. Indeed, we observed that frogs in the pasture were active for a shorter period of time in the morning compared to the forest frogs. ...
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Much of the worlds biodiversity is held within tropical rainforests, which are increasingly fragmented by agricultural practices. In these threatened landscapes, there are many organisms that acquire chemical defenses from their diet and are therefore intimately connected with their local food webs. Poison frogs (Family Dendrobatidae) are one such example, as they acquire alkaloid-based chemical defenses from their diet of leaf litter ants and mites. It is currently unknown how habitat fragmentation impacts chemical defense across trophic levels, from arthropods to frogs. Thus, we examined the chemical defenses and diets of the Diablito poison frog (Oophaga sylvatica), and the diversity of their leaf litter ant communities in secondary forest and reclaimed cattle pasture. We found that forest and pasture frogs differed in diet and alkaloid profiles, where forest frogs contained more of specific alkaloids and ate more ants. We also found that the leaf litter of forest and pasture frog habitats differed in ant community structure. Finally, ant species composition of frog diets resembled the surrounding leaf litter, but diets were less variable. This suggests that frogs tend to consume particular ant species within each habitat. To better understand how ants contribute to the alkaloid chemical profiles of frogs, we chemically profiled several ant species and found some alkaloids to be common across many ant species while others are restricted to a few species. Our experiments are the first to link anthropogenic land use changes to dendrobatid poison frog chemical defenses through variation in leaf litter communities, which has implications for conservation management of these threatened amphibians.
... In addition to the evolutionary history of species, regional environmental conditions can mediate community responses to habitat conversion. For example, negative effects of habitat loss and fragmentation on α-diversity appear to be most pronounced in warm, tropical climates (30), possibly owing to large increases in temperatures and thermal stress in fragments and the surrounding converted habitats (31)(32)(33)(34). Similarly, we expect that taxonomic and phylogenetic β-diversity between natural and converted habitats vary with latitude and elevation because regional climate will affect the magnitude of microclimatic differences between natural and converted habitats. ...
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Significance Widespread conversion of natural habitats to human land use creates evolutionarily novel environments and causes declines of native species. Stemming biodiversity loss requires an understanding of why some species persist while others decline in these novel habitats. We analyzed survey data of amphibian species from around the globe to determine whether closely related species respond similarly to habitat conversion. We find that species that persist in converted habitats tend to come from the same clades within the amphibian tree of life and that by favoring these widely distributed clades, habitat conversion leads to nonrandom extirpations and loss of evolutionary history. Our results show that the identity of winners and losers during the Anthropocene can be tightly linked to their evolutionary history.
... This indicates that the percentage of forest cover in the landscape reduces the difference in amphibian biodiversity between organic and conventional rice wetlands in Kerala. Forest in agricultural landscapes is known to facilitate mobility between different habitat types during seasonal migration of amphibians (Fahrig et al. 2011;Nowakowski et al. 2013). My results also indicate that conventional amphibian abundance is positively correlated to percent of forest in the landscape, which suggests that forest in the surrounding landscape improves quality of habitat for amphibians in conventional fields. ...
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Agriculture is the most extensive global land use and a leading cause of biodiversity loss. Organic farming is often promoted as a means of reducing agricultural impacts on biodiversity by reducing or avoiding chemical fertilizers and pesticides, and can result in a 30 percent increase in biodiversity for some species in some systems. A potential trade-off is that organic agriculture can lower crop yields, thereby requiring a greater land area to meet crop production goals. In this study, I examined whether forest cover surrounding rice wetlands can reduce the trade-off between biodiversity and productivity via comparison of paired organic and conventional farms. I compared abundance, Simpson diversity, and rarefied richness of amphibians, and abundance of arthropods in organic and conventional rice wetlands in four districts in Kerala, southern India, from July to October of 2016. I selected 31 organic rice fields and paired each with a nearby conventional field. Pairs were located to maximize the variation in forest cover in the landscape surrounding the fields. Farmers provided data on mean rice yields of each farm. Amphibians were significantly more abundant and diverse in organic fields, and species composition differed from those of conventional fields. Arthropods were more abundant in organic fields. While mean yield (tons of rice/hectare) of organic farms was significantly lower than in conventional farms, landscape context ameliorated the trade-off between productivity and biodiversity. In organic fields surrounded by more forest patches, rice yields did not decrease as much compared to the landscapes with less forest, while the increase in biodiversity (as compared to nearby conventional agriculture) was not as large. My results suggest that forested landscapes reduce the trade-off between biodiversity and productivity in rice fields in Kerala. These results could aid in designing agricultural ecosystems that maximize biodiversity benefits. For example, promoting more diversified tree-based agroecosystems, and protecting remaining uncultivated areas in the landscape could improve farmland biodiversity while minimizing the impacts to the agricultural productivity of the landscape. Furthermore, in intensively managed landscapes comprised of cropland and urban land cover, organic farming may have a larger effect on biodiversity than in landscapes with more forest cover.
... Tadpoles develop on land until one of the parents transports them on their back to suitable aquatic nurseries (Wells, 2007;Weygoldt, 1987). The ability to home back after translocations has been demonstrated in several poison frog species (Nowakowski et al., 2013;Pašukonis et al., 2013;Pichler et al., 2017), but the sensory and spatio-cognitive mechanisms underlying this ability remain unknown. Recent tracking studies revealed that territorial males of the poison frog Allobates femoralis can return to their territory via a direct path after translocations of up to 400 m. ...
... Microhabitat selection and macrohabitat affiliations have also been correlated with thermal tolerances; species with high heat tolerances were affiliated with open microhabitats ( Brusch et al. 2016) and warm natural habitat types ( Duarte et al. 2012). Thermoregulation in warm habitats is coupled with evaporative water loss ( Tracy 1976;Tracy et al. 2013), and habitatspecific rates of water loss have been associated with survival and dispersal limitation in altered landscapes ( Nowakowski et al. 2013Nowakowski et al. , 2015Watling & Braga 2015). Collectively, these studies suggest a potentially integral role of thermal biology in shaping species responses to habitat modification. ...
Article
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Human activities often replace native forests with warmer, modified habitats that represent novel thermal environments for biodiversity. Reducing biodiversity loss hinges upon identifying which species are most sensitive to the environmental conditions that result from habitat modification. Drawing on case studies and a meta-analysis, we examined whether observed and modelled thermal traits, including heat tolerances, variation in body temperatures, and evaporative water loss, explained variation in sensitivity of ectotherms to habitat modification. Low heat tolerances of lizards and amphibians and high evaporative water loss of amphibians were associated with increased sensitivity to habitat modification, often explaining more variation than non-thermal traits. Heat tolerances alone explained 24–66% (mean = 38%) of the variation in species responses, and these trends were largely consistent across geographic locations and spatial scales. As habitat modification alters local microclimates, the thermal biology of species will likely play a key role in the reassembly of terrestrial communities.
... Tadpoles develop on land until one of the parents transports them on their back to suitable aquatic nurseries (Wells, 2007;Weygoldt, 1987). The ability to home back after translocations has been demonstrated in several poison frog species (Nowakowski et al., 2013;Pašukonis et al., 2013;Pichler et al., 2017), but the sensory and spatio-cognitive mechanisms underlying this ability remain unknown. Recent tracking studies revealed that territorial males of the poison frog Allobates femoralis can return to their territory via a direct path after translocations of up to 400 m. ...
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These authors contributed equally to this work Summary statement Three-striped poison frogs (Ameerega trivittata) can navigate home via a direct path from areas exceeding the range of their routine movements. Abstract Most animals move in dense habitats where distant landmarks are limited, but how they find their way around remains poorly understood. Poison frogs inhabit the rainforest understory where they shuttle tadpoles from small territories to widespread pools. Recent studies revealed their excellent spatial memory and the ability to home back from several hundred meters. It remains unclear if this homing ability is restricted to the areas that had been previously explored or if it allows the frogs to navigate from areas outside their direct experience. Here we used radio-tracking to study the navigational performance of three-striped poison frog translocated outside the area of their routine movements (200-800 m). Translocated frogs returned to their home territory via a direct path from all distances and with little difference in orientation accuracy, suggesting a flexible map-like navigation mechanism. These findings challenge our current understanding of mechanisms and the sensory basis of amphibian orientation.
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Context Habitat destruction is the leading threat to terrestrial biodiversity, isolating remnant habitat in a matrix of modified vegetation. Objectives Our goal was to determine how species richness in several broad taxonomic groups from remnant forest was influenced by matrix quality, which we characterized by comparing plant biomass in forest and the surrounding matrix. Methods We coupled data on species-area relationships (SARs) in forest remnants from 45 previously published studies with an index of matrix quality calculated using new estimates of plant biomass derived from satellite imagery. Results The effect size of SARs was greatest in landscapes with low matrix quality and little forest cover. SARs were generally stronger for volant than for non-volant species. For the terrestrial taxa included in our analysis, matrix quality decreased as the proportion of water, ice, or urbanization in a landscape increased. Conclusions We clearly demonstrate that matrix quality plays a major role in determining patterns of species richness in remnant forest. A key implication of our work is that activities that increase matrix quality, such as active and passive habitat restoration, may be important conservation measure for maintaining and restoring biodiversity in modified landscapes.
Article
Agricultural expansion continues to drive forest loss in species-rich tropical systems and often disrupts movement and distributions of organisms. The ability of species to occupy and move through altered habitats likely depends on the level of contrast between natural forest and surrounding land uses. Connectivity models, such as circuit theory models, are widely used in conservation biology, and their primary input consists of resistance surfaces representing movement costs associated with landscape features. Cost values are most frequently determined by expert opinion, which may not capture relevant levels of contrast among features. We developed resistance surfaces using experiments that represent different local mechanisms hypothesized to affect connectivity for two Neotropical amphibian species. Response ratios were calculated to translate experimental results to cost values used in connectivity modeling. We used relative abundance data in three land-cover types to generate resistance surfaces for evaluating independent support of models derived from experiments. Finally, we analyzed agreement among movement pathways predicted for each species and among three commonly used connectivity measures: Euclidean, least cost, and resistance distances. Experiments showed that extreme microclimates associated with altered habitats significantly increased desiccation and mortality risk for both species. Resistances estimated from microclimate experiments were concordant with those from survey data for both species. For one focal species, resistance estimates derived from predator encounter rates were also highly correlated with abundance-derived resistances. There was generally low agreement among the three alternative distance measures, which underscores the importance of choosing connectivity models that are most appropriate for the study objectives. Overall, similarity among linkages modeled for each species was high, but decreased with declining forest cover. Our results highlight the value of experiments for drawing inferences about processes in resistance modeling, as well as the need to consider model differences and species-specific responses when developing strategies to maintain connectivity.
Chapter
Organisms live in heterogeneous environments; they grow, reproduce, disperse, and die in landscapes that are spatially variable and temporally dynamic. Understanding the interactions of organisms with their environment is, of course, a major focus of ecology; understanding the interactions of organisms with the spatial heterogeneity in their environment is a key emphasis of landscape ecology. Much research relating organisms to landscape pattern was motivated by issues associated with and . In many landscapes worldwide, expanding human land use has caused natural habitats to decline, and remaining habitat often has been apportioned into small, isolated patches (Fig. 7.1). Landscape ecologists have mounted field studies, developed simulation models, and conducted experiments to understand and predict the consequences of habitat fragmentation for a wide variety of organisms (e.g., Debinski and Holt 2000; Fahrig 2003; Lindenmayer 2006; Collinge 2009). To maintain biodiversity (the abundance, variety, and genetic constitution of native animals and plants), ecologists also recognized the need for a landscape perspective to complement population, community, and ecosystem considerations (Franklin 1993). It is not only the local habitat amount and quality that matters for organisms, but also the composition and configuration of the surrounding landscape. John Wiens laid out many of these considerations in 1976 in a seminal review article, “Population dynamics in patchy environments,” which still makes for excellent reading. In the introduction, Wiens wrote:
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Translocation experiments, in which researchers displace animals then monitor their movements to return home, are commonly used as tools to assess functional connectivity of fragmented landscapes. Such experiments are purported to have important advantages of being time efficient and standardizing 'motivation' to move across individuals. Yet, we lack tests of whether movement behavior of translocated birds reflects natural behavior of unmanipulated birds. We compared the routine movement behavior of a tropical hummingbird (Phaethornis guy) to that of experimentally translocated individuals. We tested for differences in site-selection patterns during movement at two spatial scales (point and path levels). We also compared movement rates between treatments. Behaviors documented during translocation experiments reflected those observed during routine movements. At the point level, both translocated and non-translocated birds showed similar levels of preference for mature tropical forest. At the path level, step selection functions showed both translocated and non-translocated hummingbirds avoiding movement across non-forested matrix and selecting streams as movement corridors. Movement rates were generally higher during translocation experiments. However, the negative influence of forest cover on movement rates was proportionately similar in translocation and routine movement treatments. We report the first evidence showing that movement behavior of birds during translocation experiments is similar to their natural movement behavior. Therefore, translocation experiments may be reliable tools to address effects of landscape structure on animal movement. We observed consistent selection of landscape elements between translocated and non-translocated birds, indicating that both routine and translocation movement studies lead to similar conclusions regarding the effect of landscape structure and forest composition on functional connectivity. Our observations that hummingbirds avoid non-forest matrix and select riparian corridors also provides a potential mechanism for pollen limitation in fragmented tropical forest.
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It is imperative to identify farming systems that support biodiversity. Amphibians are the most threatened class of vertebrates globally and are particularly sensitive to the impacts of agricultural intensification. While it is known that areas of natural cover are important for amphibians in farmland, it is unknown whether cropped areas of the landscape can be structured in ways that benefit them. We examine relationships between anurans (frogs and toads) and farmland heterogeneity (structural complexity of cropped areas). We hypothesize that anurans benefit from higher compositional and configurational heterogeneity via increased prey resources and refuge habitat, and facilitation of movement. We measure compositional heterogeneity as crop diversity and configurational heterogeneity as mean field size in agricultural landscapes. We predicted that anuran richness and abundance are positively related to crop diversity and negatively related to mean field size. We surveyed 34 agricultural landscapes in eastern Ontario, Canada, representing gradients in farmland heterogeneity, for anuran richness and abundance. We used a multi-model inference approach to calculate and compare model-weighted mean coefficients to determine the direction and relative importance of landscape variables on anuran response variables. While species richness and abundance were most strongly related to the amount of forest in the landscapes, anuran abundance was also negatively related to mean field size (i.e. positive association with configurational heterogeneity). In addition, the presence of one species, American Toad, was positively associated with crop diversity. Our results suggest that conserving natural habitats such as forest is the most effective means of maintaining anuran diversity and abundance in agricultural landscapes, but that increasing the landscape configurational heterogeneity through reduction of crop field sizes can provide an additional strategy to enhance anuran abundance.
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The interaction between homing and parental care offers insights about the motivational aspects underlying movement patterns in animals. For species that care for offspring at fixed locations, offspring mortality in the absence of care might impact a parent’s motivation to home after being displaced from young. We tested whether homing motivation is related to parental care in the glassfrog Centrolene savagei (Centrolenidae), a species with extended male care and territoriality. Specifically, we evaluated how parental status (i.e. caring for eggs vs unmated yet territorial males) and translocation distance impacts homing motivation. Along a stream located in the Central Andes of Colombia, we translocated 23 male C. savagei between 5 and 80 m away from their reproductive territories. We found that both parental status and translocation distance impacts homing motivation, as caring males were more likely to return to their initial territories after translocation. Seven of the 16 caring males and one of the seven unmated males returned to the initial capture site. While unmated males might be motivated to home if reproductive territories are a limited resource, our results support that caring males exhibited much higher motivation to home. It is possible that the fitness benefits accrued from caring for vulnerable offspring alters the cost-to-benefits of homing, and thus accounts for a greater frequency of homing among caring males. This study contributes to understanding how aspects of life history (e.g. parental care) relate to homing motivation in vertebrates.
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Despite the impressive growth of knowledge on the phylogenetic systematics of dart-poison frogs and their relatives (Dendrobatoidea) over the past decade, many problems remain to be addressed. We analyzed up to 189 phenomic characters (morphology, behavior, defensive chemicals) and 15 mitochondrial and nuclear loci scored for 564 dendrobatoid and outgroup terminals, including 76 newly sequenced terminals and > 20 previously unanalyzed species, using tree-alignment and the parsimony optimality criterion in the program POY v.5.1.1 and additional analyses of the implied alignment using TNT v.1.5. Even though data coverage was highly heterogeneous, the strict consensus of 639 optimal trees is highly resolved and we detected only one instance of wildcard behavior involving a small clade of outgroup species. The monophyly of the median lingual process (MLP) possessing genus Anomaloglossus is decisively refuted, with the cis-Andean species being sister to Rheobates within Aromobatidae and the trans-Andean species nested within Hyloxalinae, implying two independent origins of the structure in Dendrobatoidea. Although this result was unexpected, it is not surprising given that the MLP evolved at least five times in Asian and African ranoids, including Arthroleptidae, Dicroglossidae, Mantellidae, and Rhacophoridae and either once in the most recent common ancestor of the massive clade Victoranura followed by independent losses or multiple times within component lineages. We restrict Anomaloglossus to the cis-Andean MLP-possessing species, describe a new genus for the trans-Andean MLP-possessing species, and resurrect Paruwrobates for its sister group, which includes Dendrobates andinus (formerly Ameerega), D. erythromos (formerly Hyloxalus and, until recently, Ameerega), and Prostherapis whymperi (formerly Hyloxalus). We also transfer Dendrobates maculatus from Ameerega to Epipedobates, making Ameerega an exclusively cis-Andean group. We describe two new species of the trans-Andean MLP-possessing genus-one from Cerro Tacarcuna, near the Colombo-Panamanian border, and the other from 800-900 m elevation on the western versant of the Colombian Cordillera Occidental (Cauca Department)-bringing the total number of species in the genus to seven. The discrete, round, white to yellowish-brown dots found on the venter of the new species from Cerro Tacarcuna and at least one other trans-Andean MLP-possessing species are formed by large, ellipsoid, densely distributed (up to 80 glands/mm²) granular glands. Although specimens of the new species from Cerro Tacarcuna exuded a noxious milky substance when handled, lipophilic alkaloids were not detected. In addition to the unexpected placement of the trans-Andean MLP-possessing species, major findings include the unexpected placement of Colostethus ruthveni and its undescribed sister species (the "C." ruthveni group) within Dendrobatinae as sister of the newly recognized tribe Dendrobatini (all dendrobatines except Phyllobates and the "C." ruthveni group). We describe a new genus for C. argyrogaster and C. fugax to remedy the paraphyly of Colostethus caused by the placement of those species as sister to Ameerega. Our evidence rejects the sister group relationship of Dendrobates + Oophaga in favor of Dendrobates + Adelphobates, which is consistent with their uniquely low diploid chromosome number of 2n = 18 (2n = 20 in Oophaga). With the exception of Anomaloglossus and Colostethus, all other genera are monophyletic. We recognize several monophyletic species groups-including the Atlantic Forest, trans-Andean, and 22-chromosome groups within Allobates, the An. stepheni, An. megacephalus, and An. beebei groups in Anomaloglossus, the C. latinasus (formed by the C. inguinalis and C. latinasus clades) and C. fraterdanieli groups within Colostethus, and the Am. braccata and Am. rubriventris groups within Ameerega-identify unambiguously optimized phenomic synapomorphies, and summarize patterns in the evolution of the diploid chromosome number, swelling of Finger IV in males, relative length of Fingers II and III, length of Finger V, and testicular and intestinal pigmentation. Finally, we address criticisms of the current taxonomy of Neotropical poison frogs and their relatives, concluding that they are either overstated, misguided, or false, and that the current system of names better communicates knowledge of the diversity of these frogs. Our results highlight the importance of increased taxon sampling, and we conclude by identifying key species to include in future phylogenetic analyses.
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An animal's capacity to recolonize a patch depends on at least two components: its ability to detect the patch and its ability to reach it. However, the disruption of such processes by anthropic disturbances could explain low animal abundance patterns observed by many investigators in certain landscapes. Through field experiments, we compared the orientation and homing success of northern green frogs (Rana clamitans melanota Rafinesque, 1820) and northern leopard frogs (Rana pipiens Schreber, 1782) translocated across disturbed or undisturbed surfaces. We also monitored the path selected by individuals when presented with a choice between a short distance over a disturbed surface and a longer, undisturbed route. Finally, we measured the water loss and behaviour of frogs on substrates resulting from anthropogenic disturbances and a control. When presented with a choice, 72% of the frogs avoided disturbed surfaces. Although able to orient towards the pond of capture when translocated on disturbed surfaces, frogs had a lower probability of homing successfully to the pond than when translocated at a similar distance on an undisturbed surface. Frogs lost the most water on substrates associated with disturbance and in the absence of cover. Our data illustrate that anthropically disturbed areas devoid of cover, such as mined peatlands and agricultural fields, disrupt the ability of frogs to reach habitat patches and are likely explanations to their reduced abundance patterns in such environments.
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Despite the importance assigned to inter-patch movements in fragmented systems, the structure of landscape between suitable habitat patches, the matrix, is often considered as to be of minor interest, or totally ignored. Consequently, models predicting metapopulation dynamics typically assume that dispersal and movement abilities are independent of the composition of the matrix. The predictions of such models should be invalided if that crucial assumption is unverified. In order to test the hypothesis of a patch-specific resistance, we led an experimental study to assess the matrix effects on the movement ability of juvenile Natterjack toads (Bufo calamita). The movement behaviour of first year toadlets, the dispersal stage in this species, was investigated in an arena experiment. Toadlet mobility was assessed in five landscape components that were mimicked in the lab: sandy soil, road, forest, agricultural field, and pasture. We analysed several movement components including move length, speed, efficiency and turning angle distribution. Our results showed that movement ability was strongly affected by the land cover, even if body size modulated the behavioural responses of toadlets. Performances were the best in the arenas mimicking sand and roads, and the worst in the forest arena, toadlet moves being three to five times less effective in the latter. The mobility was intermediate in the two other arenas. We propose here a new method to quantify functional connectivity, based on quantitative estimates of relative values for resistance of landscape components. This method offers a reliable alternative for resistance value estimates to subjective ‘expert advice’ or inference from genetic population structure.
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Landscape connectivity can be viewed from two perspectives that could be considered as extremes of a gradient: functional connectivity (refers to how the behavior of a dispersing organism is affected by landscape structure and elements) and structural connectivity (depends on the spatial con-figuration of habitat patches in the landscape like vicinity or presence of barriers). Here we argue that dispersal behavior changes with landscape configu-ration stressing the evolutionary dimension that has often been ignored in landscape ecology. Our work-ing hypothesis is that the functional grain of resource patches in the landscape is a crucial factor shaping individual movements, and therefore influencing landscape connectivity. Such changes are likely to occur on the short-term (some generations). We review empirical studies comparing dispersal behav-ior in landscapes differing in their fragmentation level, i.e., with variable resource grain. We show that behavioral variation affecting each of the three stages of the dispersal process (emigration, displacement or transfer in the matrix, and immigration) is indeed likely to occur according to selective pressures resulting from changes in the grain of the landscape (mortality or deferred costs). Accordingly, landscape connectivity results from the interaction between the dispersal behavior of individuals and the grain of each particular landscape. The existence of this interaction requires that connectivity estimates (being based on individual-based models, least cost distance algorithms, and structural connectivity metrics or even Euclidian distance) should be carefully evalu-ated for their applicability with respect to the required level of precision in species-specific and landscape information.
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