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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 inter - esting 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 specifi- cally, 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. Keywords HIREC · Communication · Behavioural plasticity · Parental care · Territoriality · Tadpoles Introduction of recent and current human-induced rapid environmental changes (HIREC), such as habitat destruction/fragmenta- Environmental changes, including shifting continents and tion (Pimm and Raven 2000), climate change (Parmesan climatic fluctuations, have been shown to prompt diverse and Yohe 2003), and exposure to novel biotic (e.g. exotic responses in organisms across a wide range of taxa (Ricklefs species, pathogens, and parasites: Lockwood et al. 2013) and Schluter 1993; Rosenzweig 1995) throughout evolu- and abiotic (e.g. environmental pollutants: Rohr et al. 2006) tionary time. However, the unprecedented scale and pace stressors, represent new challenges for many species which have not experienced such rapid changes in their evolution- ary past (Palumbi 2001). The impact of HIREC on the natu- * Lia Schlippe Justicia ral world is colossal (Wake and Vredenburg 2008; Cowie email@example.com et al. 2022), affecting the availability of important resources * Bibiana Rojas (i.e. food and shelter; Fahrig 2003), altering conspecific and firstname.lastname@example.org heterospecific interactions (Tuomainen and Candolin 2011; Department of Interdisciplinary Life Sciences, Konrad Candolin and Wong 2012), and ultimately threatening many Lorenz Institute of Ethology, University of Veterinary species and populations (Pimm and Raven 2000; Wake and Medicine Vienna, Savoyenstraße 1, 1160 Vienna, Austria Vredenburg 2008; Cowie et al. 2022). Department of Biology and Environmental Science, For many animals, survival and reproduction in rapidly University of Jyvaskyla, P.O. Box 35, 40014 Jyväskylä, changing environments are expected to be shaped by the Finland Vol.:(0123456789) 1 3 acta ethologica plasticity of their behavioural responses (Hendry et al. 2008; (Alonso-Alvarez et al. 2012). Thus, an individual’s invest- Sih et al. 2011; Sih 2013; Wong and Candolin 2015). Some- ment in parental care depends on the value of their exist- times, behavioural changes may be enough for an individual ing offspring in relation to future reproductive opportuni- to adapt to new conditions or can provide additional time for ties (Alonso-Alvarez et al. 2012; Royle et al. 2012). Under genetic adaptation to occur (Pigliucci 2001). For example, changing environmental conditions, both the energetic costs great tits (Parus major) in urban environments have learnt of care for the parents and the fitness benefits for the young to adjust their song frequency to avoid interference from city could be altered, influencing population recruitment (Alonso- noise (Slabbekoorn and Peet 2003), while northern quolls Alvarez et al. 2012; Ratikainen et al. 2018). In the face of (Dasyurus hallucatus) in Australia have learnt to avoid low resource availability, parents can, for instance, reduce eating highly-toxic invasive cane toads (Rhinella marina) their current investment into offspring with the expectation (Kelly and Phillips 2017). However, species can also show of better reproductive opportunities in the future (Winkler maladaptive responses in HIREC scenarios, such as sea 1987). This decline in care quality, in turn, can cause long- turtle hatchlings following artificial light instead of natural term changes in the behaviour of the offspring, including cues (Tuxbury and Salmon 2005), or aquatic insects ovipos- aggressiveness and boldness (Armstrong 2019), cognition iting on asphalt or glass that resembles the surface of the (Bredy et al. 2004), and F1’s parental behaviour (Gromov water (Kriska et al. 1998, 2008), causing serious population 2009). Research conducted in songbirds, for example, has declines (Tuomainen and Candolin 2011; Robertson et al. shown that nutritional stress during early development stages 2013). In other cases, behavioural changes can determine (when songbirds depend on their parents for food), negatively which individuals will survive and reproduce under novel affects brain development and male song quality in adulthood conditions, acting as a driving force in evolutionary pro- (Nowicki et al. 2002). In rodents, offspring who are groomed cesses (West-Eberhard 2003; Crispo 2007; Tuomainen and less frequently during early postnatal periods exhibit lower Candolin 2011). Thus, changes in behaviour will directly spatial learning and memory in adulthood (Liu et al. 2000; influence how species evolve under HIREC. Bredy et al. 2004). Decreased investment in the face of chal- While individual behavioural responses will affect popu- lenging environmental conditions is not the rule, however, as lation dynamics on a local scale, the effect of HIREC on some parents appear to increase their workload in the face of sociality and interspecific interactions has far-reaching sub-optimal conditions (Vincze et al. 2017). Ultimately, the ecological implications for broader community dynamics. adaptability of parental behaviour/cooperation appears to be Environmental changes can directly and indirectly influ- the most accurate predictor of species successfully overcom- ence the way in which individuals interact, not only with ing the varied pressures of global change in the wild (Vincze other species (e.g. predators and prey, hosts and parasites) et al. 2017). but also with each other (Candolin and Wong 2012). Social Behavioural responses to global change largely dif- interactions, ranging from choosing a mate to providing fer between species. Amphibians are excellent models to offspring with care, can be affected by HIREC in multiple study such responses owing to their broad range of social ways (Croft et al. 2008). For example, ship noise reduces behaviours and their wide distribution across latitudes and the ability of Lusitanian toadfish (Halobatrachus didacty - climates, being found in all continents except Antarctica. lus) to detect conspecific acoustic signals, essential for mate Furthermore, their key position in trophic webs, their role attraction (Vasconcelos et al. 2007), while water turbidity as sentinel species and bioindicators of ecosystem health reduces male-male competition in three-spined stickleback thanks to their sensitivity to environmental changes, and (Gasterosteus aculeatus), compromising the honesty of their dramatic decline around the globe (Hopkins 2007) agonistic signals, which are relevant indicators of parent- make them a useful system to study the impact of human ing ability (Wong et al. 2007). Similarly, human disturbance disturbances. In fact, amphibians are considered the most can directly reduce the nest attendance of bearded vultures threatened vertebrate class on the planet (Stuart et al. 2004; (Gypaetus barbatus), increasing the probability of breeding Wake and Vredenburg 2008; Nori et al. 2015; IUCN 2020; failure (Arroyo and Razin 2006). Cordier et al. 2021), primarily due to habitat fragmentation/ Social interactions have a critical effect on individual fit- destruction and the spread of a pathogenic fungus (Daszak ness (Allee et al. 1949) and, consequently, on population et al. 2003; Pounds et al. 2006; Cordier et al. 2021). dynamics. Parental care, for example, is known to enhance One of the most emblematic and well-studied groups the offspring’s fitness by increasing their survival, growth of amphibians showing complex and diverse social behav- and/or quality, and, ultimately, their lifetime reproductive iours are Neotropical poison frogs (Dendrobatidae) and their success (Royle et al. 2012). Despite the obvious benefits for closest relatives (Aromobatidae), altogether referred to as the offspring, parental care comes at a cost to the caregiver the superfamily Dendrobatoidea (Cope 1865; Grant et al. in the form of energy expenditure, loss of mating opportuni- 2006) and hereon referred to as ‘poison frogs’ for simplicity. ties, and increased predation risk while tending their young Distributed from Nicaragua in Central America to Bolivia 1 3 acta ethologica in South America, poison frogs generally inhabit tropical physical combat (Fig. 1A; Pröhl 2005). Defending these rainforests (Summers and Tumulty 2014), often in areas that territories is often crucial to male reproductive success, as are under severe degradation, and exhibit a large diversity courtship, mating, and oviposition take place therein (Pröhl in mating systems, parental care strategies, and communica- 2005). In most species, males perform parental care, which tion modalities (reviewed in Summers and Tumulty 2014). consists of clutch attendance and larval transport (Fig. 1B) Males generally defend long-term territories from conspecif- from terrestrial oviposition sites (e.g. leaf litter and leaves ics through so-called advertisement calls and, if necessary, on bushes) to water bodies such as streams, temporary Fig. 1 Poison frogs and their unique social behaviours may be impacted pointed at by the arrows) by desiccation of nurseries; G Ranitomeya by global change. A Males of Dendrobates tinctorius engaged in physi- ventrimaculata parents (pointed at by the dashed arrows) lay clutches cal combat, where often one male pushes, kicks, and gets on top of (pointed at by the solid arrow) in bromeliads occupied by a large tad- the other trying to press them against the substrate; B male Ameerega pole in periods of low rainfall to increase the survival probabilities of hahneli transporting his tadpoles (pointed at by the arrow) to a body of the tadpole therein; H O. lehmanni is highly threatened due to illegal pet water; C tadpole (pointed at by the arrow) transport is done by females trade activities. Males are thought to be more likely to be found by col- in Oophaga granulifera; D habitat disturbance can alter the way in lectors because of their vocalisations (see the inflated vocal sac pointed which colours are perceived by con- and heterospecifics, as shown in O. by the arrow); I Andinobates bombetes adjusts their calling behaviour to pumilio, and thus affect communication systems; E males of D. tincto- avoid interference caused by traffic noise. Photo credits: Bibiana Rojas rius are in charge of clutch (pointed at by the arrow) attendance; F cli- (A, B, C, E, F, G); Justin P. Lawrence (D); Mileidy Betancourth (H); mate change can increase the risk of tadpole death (agonising tadpoles Fernando Vargas (I) 1 3 acta ethologica ponds, or small pools of water formed in plant structures for territorial species, they provide more stable temperature (i.e. phytotelmata) (Summers and Tumulty 2014). Tadpoles and humidity conditions than open areas with little canopy are confined in these water bodies until completing meta- (Duellman and Trueb 1994). The dependence on suitable morphosis (Weygoldt 1987; Lehtinen et al. 2004; Summers microhabitats together with the obligate use of small water and McKeon 2004; Schulte et al. 2020). While uniparen- bodies for reproduction or development make many Neo- tal male care is the basal reproductive strategy in poison tropical frogs particularly vulnerable to HIREC (Donnelly frogs (Weygoldt 1987; Carvajal-Castro et al. 2021), multiple and Crump 1998; Touchon and Warkentin 2009). lineages have evolved biparental or exclusive female care, where females transport tadpoles (Fig. 1C) and feed them Habitat loss and climate change with unfertilised trophic eggs (Summers et al. 1999a). The transition to female or biparental care has been suggested to Many tropical regions are subject to unprecedented rates of be the result of using small phytotelmata with scarce food habitat loss (Lewis et al. 2015; Taubert et al. 2018). Over the resources (Brown et al. 2010; Carvajal-Castro et al. 2021), last decade, deforestation patterns in the Amazonian rain- and biparental care has been proposed as the precursor of forest have switched from localised large forest clearings monogamy (Brown et al. 2008, 2010; Summers and Tumulty to geographically spread small-scale deforestation events 2014; Tumulty et al. 2014). It is precisely the interaction driven by agricultural intensification, land-use change, and between the diverse sexual and social systems of poison natural resource exploitation (i.e. mining and logging activi- frogs, combined with the pressing effects of HIREC, that ties) (Grau and Aide 2008; Hugo 2008; Kalamandeen et al. makes this group a relevant model through which to test and 2018). Small-scale deforestation pressures are expected to understand the impacts of global change. affect more remote areas and populations. This type of defor - Although global change is expected to influence social estation is also recognised as one of the main causes of more behaviours in several ways, surprisingly little is known about frequent and intense anomalies in the Amazonian hydro- how these effects take place in wild populations of poison logical cycle, such as extreme weather events (i.e. El Niño frogs. Moreover, most studies analyse environmental stress- Southern Oscillation, hereafter El Niño) and dry spells dur- ors independently, often underseeing potential interactions ing the rainy season (Lovejoy and Nobre 2018), which may and synergic effects. For example, while tadpoles manage to be further exacerbated by global warming (Jiménez-Muñoz cope with predator-induced stress and low concentrations of et al. 2016). Both the loss of habitat and more frequent cli- pesticides separately, when exposed to both at the same time matic anomalies can affect poison frogs in multiple ways they show substantial mortality (Relyea and Mills 2001). throughout their life stages, potentially leading to different Further research combining animal behaviour and conser- behavioural responses and adaptations. vation biology (Caro 1999) is necessary to identify species- specific relevant HIREC and to understand how they may Disruption in communication systems adapt (or not) their behaviours accordingly. Only by doing so, we may be able to evaluate populations’ vulnerability Habitat alteration through small-scale deforestation can to global change, develop predictive models and focus con- directly affect conspecific communication in two differ - servation efforts (Schroeder et al. 2011). Here, we illustrate ent ways. First, because human-made gaps are known to key points about the potential impacts of, and responses to, have increased radiation and higher temperatures than other HIREC using Neotropical poison frogs’ social behaviours as areas of the forest (Vitt et al. 1998), male calling behav- a model system. We specifically focus on territoriality and iour can become unsustainable over long periods of time. parental care behaviours, as they could be of special impor- This is because, in degraded conditions, males would be tance due to their capacity to buffering offspring against more exposed and thus could incur higher evaporative water HIREC. Using this information as a baseline, we identify loss and potential overheating. These physiological stress- knowledge gaps and formulate new testable hypotheses to ors entail behavioural consequences as, in the mid-to-long assess (1) the nature and magnitude of HIREC impact on term, males would be unable to devote as much time to wild populations of poison frogs, and (2) potential parental attract females and advertise territory ownership. Second, care and aggression responses to these HIREC. variations in the forest’s light environment can make an ani- mal’s appearance change too (Endler 1993), which has been Impacts of global change on poison frogs proven crucial in the courtship behaviour of some lekking bird species (Théry and Endler 2001). The detectability of Poison frogs depend on a wide variety of microhabitats in the variable colour patterns found in D. tinctorius, likewise, different life stages. Leaf litter and phytotelmata, for exam- has been shown to differ depending on whether they are seen ple, serve as primary breeding sites, shelters, and nurseries under an open or closed canopy (Rojas et al. 2014). While for poison frogs; in addition to being defendable resources this has been studied mostly in the context of predator–prey 1 3 acta ethologica interactions, such differences in detectability in response to mortality was generally higher in aquatic sites due to greater the surrounding light environment could be particularly rel- predation risk, altered rainfall patterns driven by climate evant for species in which colour patterns play a role in mate change increased clutch dehydration risk, shifting the opti- choice (e.g. O. pumilio: Summers et al. 1999b; Maan and mal site choice by parents from terrestrial to aquatic habi- Cummings 2008; Yang et al. 2019) or underlie differences tats over the span of only 40 years. D. ebraccatus clearly in other behavioural patterns such as boldness or aggressive- provides an excellent system to measure the success of the ness (e.g. O. pumilio: Rudh et al. 2013; Pröhl and Ostrowski adaptive decision-making by parents; however, whether or 2011; Crothers and Cummings 2015; O. granulifera: Willink not poison frogs are as flexible in their use of oviposition et al. 2013, 2014). Importantly, human-driven habitat dis- and tadpole deposition sites requires further research. For turbance may not only affect the light environment but also terrestrially-breeding frogs, buffering the negative effects the structure of the forest floor, which can alter detectability of HIREC could largely depend on the parents’ capacity and visual contrast, thus causing potential interference in to select specific microhabitats with favourable structures. communication between conspecifics (Barnett et al. 2021). Dendrobates tinctorius, for example, is a terrestrial-breeding Furthermore, because poison frog colouration is partly based frog with clutch attendance (Fig. 1D) and uniquely flexible on carotenoid pigments acquired through the diet (Twomey deposition choices compared to other species that also use et al. 2020), changes in the prey community availability ephemeral pools as nurseries. D. tinctorius fathers trans- driven by habitat disturbances could also alter the coloura- port tadpoles to diverse pools that range enormously in tion of individuals. In fact, several studies have shown that their vertical position (0– > 20 m), size (19 mL to − 270 a diet rich in carotenoids can indeed produce changes in L), and chemical composition (pH = 3 to − 7) (Fouilloux colouration (Brenes-Soto and Dierenfeld 2014; Umbers et al. et al. 2021). We hypothesise that, when faced with the pres- 2016; Stückler et al. 2022) and increase the reproductive sures of HIREC, species that can access (and tolerate) a success of captive frogs (Ogilvy et al. 2012; Dugas et al. wider variety of nurseries will fare better than those with 2013). Thus, changes in prey availability could affect the narrower options. Species with flexible behaviour may also intake of carotenoids or their precursors and, in turn, affect benefit from modulating care investment based on climatic intraspecific communication, particularly in species where conditions, e.g. when desiccation risk is high parents spend colouration plays an important role in mate selection, as additional effort accessing especially deep/stable nurser - mentioned above. ies compared to potentially more relaxed, “riskier” choices throughout a consistently rainy season. Furthermore, we Increased care and aggression under HIREC: a parent’s predict sites with denser canopy cover as well as abundant perspective leaf litter and vegetal structures (e.g. fallen branches and hollow trunks) to provide more stable microclimate con- Reduced vegetation cover and longer dry spells could result ditions for successful egg development. Nevertheless, dif- in higher egg mortality due to dehydration, especially for ferent microhabitats may be weighed differently depending amphibian species with nonaquatic eggs (Touchon and on species-specific biological and life-history requirements. Warkentin 2009). For example Delia et al. (2013) found that Therefore, a better understanding of the microhabitat use of offspring of the glass frog Hyalinobatrachium fleischmanni, species both in undisturbed and disturbed areas is essential a species with parental care, had higher mortality rates in to implement effective conservation efforts. years of low rainfall. Similar situations could arise in poi- On the other hand, to compensate for adverse environ- son frogs due to the high susceptibility of their terrestrial mental conditions, parents may adjust the intensity and clutches to evaporative water loss; in Allobates paleovarzen- frequency of clutch attendance to guarantee offspring sur - sis, for instance, only 8.6% of the clutches survived until vival (see examples in invertebrates (Dick et al. 1998), fish the transporting stage following an El Niño event compared (Green and McCormick 2005), reptiles (Stahlschmidt and to ~ 70% survival during a standard season (Rocha et al. DeNardo 2010), and birds (Vincze et al. 2017)). Males of 2021). H. fleischmanni , for example, increase both the frequency There are several behaviours that may help adult poison and time spent on egg care in response to a reduction in frogs reduce the vulnerability of their eggs to HIREC. On relative humidity (Delia et al. 2013). One of the most com- the one hand, choosing suitable oviposition sites is particu- mon ways anurans provides egg attendance is by placing larly important if larvae are unable to leave these sites when their body over the eggs to reduce evaporative water loss conditions become unfavourable. For example, in the tree or directly moistening the eggs through physical contact frog Dendropsophus ebraccatus, a unique species which can with the ventral integument (Wells 2010). Although this flexibly choose between aquatic and nonaquatic deposition behaviour has been suggested for some poison frogs (Souza sites, changes in rainfall patterns since 1972 have altered et al. 2017), it is not ubiquitous across the family (Rocha oviposition-site selection (Touchon 2012). Although egg et al. 2021). Furthermore, some amphibians can increase 1 3 acta ethologica the amount of glycoprotein-rich jelly cores, jelly layers, or males, more competition among females, and, as a result, an matrices surrounding the clutches, which protect embryos increase in filial cannibalism events. from dehydration and predators (Delia et al. 2020). So far, Finally, because egg attendance and territorial defence little research has focused on the potential egg attendance may become more energetically demanding under harsh plasticity that poison frogs may present under environmental environmental conditions, we hypothesise that alternative stress. Considering that egg attendance conflicts with other care strategies such as plastic biparental care and monog- fitness-related activities, such as foraging and mating (e.g. amy could become favoured over evolutionary time. This is Delia et al. 2013), investigating the trade-offs of parental the case in the Atlantic labrid fish Symphodus tinca, which decisions under environmental changes is essential to predict changes from no parental care to uniparental care when tem- population dynamics. Therefore, if the costs of maintaining perature and predators increase during the breeding season the current clutch surpass their fitness benefits, we would (Van den Berghe 1990), or in plovers (Charadrius spp.), predict individuals to reduce their parental care effort or where temperature stochasticity increased male parental even abandon clutches completely, as seen in other taxa (e.g. cooperation during incubation (Vincze et al. 2017). Given birds: Bustnes and Erikstad 1991; Öberg et al. 2015; fish: that some poison frogs can show parental flexibility and a Suski and Ridgway 2007). parent can take over tadpole transport when the other par- It is noteworthy that in territorial species, such as most ent goes missing (for more details see next section), we dendrobatid frogs (Pröhl 2005), the trade-off between encourage future studies to investigate whether flexibility defending territories and attending multiple clutches simul- can be found in other parental care behaviours such as egg taneously may become magnified under habitat loss. Habi- attendance. tat loss and fragmentation can modify species movement as well as the availability of resources and suitable territories Consequences on larval survival and possible evolutionary (Fahrig 2003), which can alter the carrying capacity of the trajectories under HIREC area in different ways. Firstly, habitat fragmentation could reduce population density if edge effects are negative (e.g. The alteration of forest habitats for different human land- increased predation pressure), or if the fragmented habi- uses as well as changes in climate patterns can also affect tat is not able to sustain larger populations (Mullu 2016). poison frogs during larval and adult stages by modifying the Given that the costs of mate search in females depend on availability and quality of important resources and micro- the number of suitable mates available, a lower population habitats. For example, by clearing primary forest and reduc- density could detract energy and time from tadpole care in ing the canopy cover, the ground becomes more exposed species with female egg-feeding and tadpole transport. By to solar radiation, which increases near-ground temperature contrast, the remaining patches of habitat could also increase and, in turn, phytotelmata desiccation risk (del Pliego et al. population density by concentrating the surviving individu- 2016; Rivera-Ordonez et al. 2019). This is especially con- als from the disturbed habitat (Mullu 2016). In the result- cerning given that the depletion of some resources (e.g. bro- ing smaller and densely packed habitat patches, aggression meliad phytotelmata) has been related to serious population rates between highly territorial individuals may increase declines in some poison frog species (Pröhl 2002; Vargas- due to a higher number of encounters and more competition Salinas and Amézquita 2013; Meza-Joya et al. 2015). for limited resources and territories (Fisher et al. 2021). In Phytotelmata are used in multiple poison frog species to male tree lizards (Urosaurus ornatus), for instance, aggres- deposit their tadpoles (Weygoldt 1987; Summers and McKeon sive interactions between individuals are more frequent in 2004; Lehtinen et al. 2004; Rojas 2014, 2015; Schulte et al. resource-limited burned sites than in resource-rich habitats 2020; Fouilloux et al. 2021), can naturally vary in water vol- (Lattanzio and Miles 2014). More energy spent on territo- ume, nutrient composition, food sources, stability as well as rial defence could translate into a reduced ability to attract the risk of competition and predation (Lehtinen et al. 2004). further mates or attend multiple clutches, directly influenc- Consequently, parents have to assess all these different eco- ing mating systems. This conflict between aggression and logical factors, which can be highly unstable and vary in direct care of offspring has been found in multiple animals space and time (Rudolf and Rödel 2005; Schulte and Lötters (e.g. Lissåker and Kvarnemo 2006; DeAngelis et al. 2020). 2013), and adapt their deposition strategy according to this Importantly, filial cannibalism occurs in some dendrobatid information (Webb et al. 1999; Schulte and Lötters 2013). frogs, both in adult males when taking over a new terri- Furthermore, the size of these breeding pools has been asso- tory (e.g. Allobates femoralis: Ringler et al. 2017) and in ciated with the evolution of different parental care strategies females to decrease parental investment of a mate in unre- (e.g. trophic egg feeding and biparental care evolved in spe- lated clutches (e.g. Dendrobates auratus: Summers 1989). cies using smaller pools; Brown et al. 2010). The selection Thus, we predict that higher densities and lower resource of suitable rearing sites will play a key role in the successful availability could also lead to more territorial intrusions by development and survival of their offspring (Refsnider and 1 3 acta ethologica Janzen 2010), and thus will have direct effects on the popu- others by exploiting alternative food supplies (i.e. feeding lation recruitment for multiple species. However, HIREC on other tadpoles of either the same (cannibalism) or dif- might further exacerbate the instability and availability of ferent species). Cannibalism can have major consequences good-quality phytotelmata, imposing multiple novel costs on at the population level for some species, eliminating large parental care and territoriality. Because these stressors could proportions of offspring or entire cohorts in extreme cases be especially pronounced in small phytotelmata, species with (Polis 1981). That is the case in Ranitomeya (formerly Den- parental care strategies such as egg feeding could be particu- drobates) ventrimaculata, where only one tadpole survives larly affected. Importantly, nursery desiccation is already in most pools regardless of the number of tadpoles deposited considered one of the most common abiotic causes of tadpole therein (Summers 1999). mortality (Fig. 1E), even in tropical rainforests where annual We hypothesise that a reduction in the number of suitable rainfall is very high (Murphy 2003; Rudolf and Rödel 2005; phytotelmata available in a territory will force parents to BR, CF pers. observ.). transport their tadpoles longer distances until deposition sites, Some authors have suggested plastic feeding behaviour as increasing direct and indirect associated costs. For example, one possible mechanism to deal with phytotelmata desicca- transporting individuals might directly increase their mortality tion. According to this hypothesis, some poison frog species risk by presumably spending more time exposed to potential would switch from avoiding tadpole/egg deposition in pools predators (Rojas and Endler 2013; Pašukonis et al. 2019), as already containing conspecifics (to minimise predation: well as indirectly reduce their fitness by investing less time Caldwell and Araújo 1998; Summers 1999) to systemati- and energy on territorial defence and mating opportunities cally depositing them with conspecifics, which can be a form (Pašukonis et al. 2019). From the larvae point of view, in den- of food resource. For example, in Ranitomeya ventrimacu- drobatid species where adults transport tadpoles singly into lata, clutches are laid more often in bromeliad axils where phytotelmata, travelling longer distances would mean leav- there is already a tadpole towards the end of the rainy season ing siblings unattended for longer periods of time and, thus, (Fig. 1F) (Poelman and Dicke 2007). This way, parents are increasing their probability of dying from desiccation, preda- thought to accelerate their older offspring’s development and tion or fungal infection. All these costs may, in turn, become increase their chance to reach metamorphosis before tempo- accentuated in human-disturbed habitats, where different rary pools dry out, which can happen within days. Likewise, microclimatic conditions, vegetation cover, and assemblages older tadpoles of the species Ranitomeya variabilis may feed of predators pose new threats and increased stress (Knowlton on younger siblings when resources are low (Brown et al. and Graham 2010). One possible behavioural response that 2009). However, although cannibalising conspecific tadpoles might be favoured to reduce the costs of transporting tadpoles provide higher nutritional value than other prey for some longer distances could be to transport as many tadpoles as amphibian species (e.g. Crump 1990), the direct benefits of possible at the same time. Ringler et al. (2013) found a signif- cannibalism through enhanced growth rates in poison frogs icantly positive correlation between the distance of Allobates have not been disentangled from the benefits of eating ‘just’ femoralis males to their home territories during tadpole trans- another (i.e. heterospecific) tadpole. Instead, tadpole canni- port and the number of tadpoles on their back, suggesting that balism is thought to be the result of indiscriminate predatory the number of tadpoles that parents decide to take up at once behaviour to eliminate potential competitors (Caldwell and is influenced by the distance to suitable water bodies. This Araújo 1998; Summers and McKeon 2004). Furthermore, would mean that at least some species of poison frogs may be weaker avoidance or even active choice of pools with con- capable of adjusting their behaviour depending on the avail- specific tadpoles at the end of the rainy season could also ability of tadpole deposition sites and buffer to some degree be the result of less suitable sites available or parents using their reduction due to HIREC. Another response to deal with tadpole presence as a cue for pool quality and persistence, increased parental costs (i.e. longer transporting distances) as is the case in Dendrobates tinctorius (Rojas 2014). This that could be favoured over evolutionary time is the appear- last idea is further supported by a study on Edalorhina perezi ance of female parental care plasticity in otherwise uniparen- (Leptodactylidae), which also loses their sensitivity to inver- tal male care systems. Because most female poison frogs do tebrate predators late in the rainy season (Murphy 2003). not defend territories (Pröhl 2005), they might gain consider- A reduction in the number of suitable nurseries could also able fitness benefits by flexibly taking over parental duties and lead to the convergence of site choice by multiple parents, increase the survival chances of the clutches in which they potentially from multiple species that in “normal” condi- have already invested significant time and energy. Female tions would select for smaller/more unstable pool types (e.g. parental care plasticity has been previously reported in some bromeliads). Consequently, we predict that under HIREC the poison frogs (e.g. Allobates femoralis, Dendrobates tinctorius, overall larval density in pools will increase, and competition Anomaloglossus beebei) where, in absence of the male car- between tadpoles from the same or different species could egiver, females show compensatory parental care behaviour become stronger, potentially benefitting certain species over by transporting tadpoles both under laboratory (Ringler et al. 1 3 acta ethologica 2015; Fischer and O’Connell 2020) and natural conditions (Betancourth-Cundar et al. 2020). The global amphibian pet (Ringler et al. 2013; Rojas and Pašukonis 2019; Pettitt 2012). trade is also widely recognised as one of the main drivers of However, this plasticity has not been found in other close the worldwide spread of amphibian pathogens such as the species like Allobates paleovarzensis (Rocha et al. 2021). chytrid fungus Batrachochytrium dendrobatidis (hereafter Finally, human-transformed habitats may also affect par - Bd) (Fisher and Garner 2007), one of the most dramatic ents' orientation capacity by attenuating their familiarity examples of newly-emerged pathogens, which causes the with sensory cues. For example in Oophaga pumilio, ori- infectious disease chytridiomycosis. Therefore, it is not sur- entation depends both on the distance and the habitat type prising that Bd has recently been detected in dendrobatid (forests or pastures) (Nowakowski et al. 2013). Thus, given species in the wild. that males often select tadpole deposition sites outside of Bd is known to be responsible for the mass mortalities in their territories or core areas (Ringler et al. 2013; Pašukonis many amphibian populations and some species extinctions et al. 2019), parents’ ability to find good rearing sites in worldwide (Daszak et al. 2003; Lips et al. 2005; Pounds the first place, or to return to selected phytotelmata in the et al. 2006). Indeed, Bd prevalence in Dendrobatidae was case of tadpole feeding species, could be impaired. To date, recently found to be higher than in Bufonidae and Hylidae very little work has explored the manner(s) in which land- in an Amazonian community (Courtois et al. 2015). While use changes influence movement behaviour in poison frogs. the impact of Bd on poison frog populations is still poorly However, it is reasonable to predict that they could have known, in other species it can inhibit the immune response great impacts not only on parental decisions and territorial (Fites et al. 2013), impact their body condition and growth defence but also on population dispersal and gene flow. This (Parris and Cornelius 2004), reduce their locomotion and is, therefore, a subject that merits further investigation. foraging performance (Chatfield et al. 2013; Venesky et al. 2009), and even change their advertisement calls (An and Pet trade, infectious diseases, and pollution Waldman 2016). Moreover, because Bd zoospores are aquatic, species more dependent on water are expected to be In the Amazonian and Chocó rainforests, the fast development the most impacted due to prolonged periods of time exposed of large- and small-scale agriculture, urbanisation, and min- to Bd zoospores (Bielby et al. 2008). Thus, in the scenario ing activities (Fig. 2), especially gold mining (Kalamandeen proposed above, where global change may cause higher et al. 2018; Palacios-Torres et al. 2018), are not only modify- densities of tadpoles sharing rearing sites, Bd transmission ing habitats but also polluting the environment (Folchi 2001; within and between species could exponentially increase. Piscoya Arbañil 2012; Gamarra Torres et al. 2018). Further- Likewise, we predict energetically costly activities such more, accidental or deliberate introduction of exotic species, as parental care and territory defence to be also affected, and, especially the global pet trade in the case of poison because infected individuals may have to relocate energy frogs, are increasing the transmission of and susceptibility from reproduction, calling, or parental care into immune to pathogens and parasites in previously isolated populations defence. This means that infected individuals may be less (e.g. Fecchio et al. 2021; Santos et al. 2021). able to defend their territories or perform parental care, The illegal pet trade is recognised as one of the major which would indirectly cause higher offspring mortality threats to dendrobatid poison frogs (Gorzula 1996; Gaucher rates. Given the importance of social behaviours on popula- and MacCulloch 2010; Nijman and Shepherd 2010; Brown tion dynamics, further research investigating the impacts of et al. 2011; Betancourth-Cundar et al. 2020), as hobbyists Bd on such behaviours is required. are often after exotic colour variants, which can reach exor- In addition, chemical pollutants derived from agriculture bitant prices in the market. This practice has been notably (e.g. herbicides and pesticides) and mining activities (e.g. increasing in South America with the popularisation of the metals and metalloids: Hg, Cu, Co, Zn, and As) can impair internet (Máximo et al. 2021), placing increased risks to the individuals’ immune defences and further increase their sus- anurans of this region. Besides obvious long-term conse- ceptibility to pathogens and diseases (Christin et al. 2003). quences such as decreased genetic diversity, the rarefaction Similarly, when found in low concentrations, they can delay of individuals in natural populations is thought to affect the growth and metamorphosis (Carey and Bryant 1995), cause two sexes differently, with males being at a higher risk of malformations (Unrine et al. 2004; Ferrante and Fearnside being detected due to the conspicuousness of their vocali- 2020), alter fertility and fecundity (Adams et al. 2021), or sations (Fig. 1H) (Betancourth-Cundar et al. 2020), which even cause sex-reversals (Nemesházi et al. 2020), often lead- they use to fend rivals off and to attract females. This can ing to devastating consequences for amphibian populations obviously alter the care provided to offspring, particularly in (Brühl et al. 2013). Increasing evidence demonstrates effects species in which parental care duties are predominantly per- on a wide range of amphibian behaviours, such as reduced formed by males, but it can also result in population declines rates of activity (e.g. swimming, feeding, and breeding) or as the populations end up being heavily female-biased ability of tadpoles to escape predation (Shuman-Goodier 1 3 acta ethologica Fig. 2 Illegal mining. Small- scale deforestation due to illegal mining activities is threatening the habitat of many species of poison frogs in the Ama- zon and the Chocó regions, two of Earth’s biodiversity hotspots. Here, illegal mining activity in Nouragues Natural Reserve, French Guiana. Pho- tos: A) Bernard Gissinger; B) Alexandre David and Propper 2016; Sievers et al. 2019). In two-lined sala- to favour individuals capable of recognising and avoiding manders (Eurycea bislineata), for instance, exposure to sub- egg-laying and rearing sites based on chemical pollutant lethal concentrations of mercury reduced their motivation concentrations. As far as we are aware, however, this abil- to feed (Burke et al. 2010), whereas it impaired swimming ity has been investigated in some anurans but not in poison performance in American toad (Anaxyrus [formerly Bufo] frogs. For example, adults of the grey treefrog (Hyla versi- americanus) larvae (Bergeron et al. 2011). Although chemi- color) avoided ponds for oviposition if contaminated with cal contaminants have also been reported to alter multiple the glyphosate pesticide Roundup (Takahashi 2007). social behaviours such as territorial behaviour in other taxa Social behaviours can also be impacted by an important, (e.g. vom Saal et al. 1995; Bell 2001), to our knowledge, no yet often underestimated, the form of anthropogenically study has addressed this possibility in amphibians. Given driven pollution, noise pollution. For acoustically com- the strong detrimental effects of pollutants on egg and tad- municating species, as is the case of most anuran species, pole survival and development, we would expect selection anthropogenic background noise can mask vocalisations and 1 3 acta ethologica thus disrupt key species-specific communication (Simmons calls and decrease inter-pulse intervals (Clemmens 2014). and Narins 2018). For instance, masking of acoustic signals However, because changes in calling characteristics could could inhibit males’ calling activity (Sun and Narins 2005), potentially be opposed to female mate preferences, future reduce females’ ability to localise male’s advertisement calls research should investigate if such responses could become (Caldwell and Bee 2014), or change female’s mate choice, maladaptive. potentially selecting for less fit males (Barrass 1985) or males with lower quality of parental care (Pettitt et al. 2020). Masked male calls may not only attract fewer females but Conclusions also make territorial calls less audible, affecting male ter - ritorial defence by reducing their ability to detect and dis- 1. HIREC have great impacts on the way organisms interact criminate against conspecific intruders, as shown in birds among them and with their environment, imposing new (Kleist et al. 2016). This, in turn, may translate into more threats for multiple species. Behaviour is often the first conspecific intrusions, aggressive encounters, and increased response to environmental changes, and its plasticity filial cannibalism rates. To cope with anthropogenic noise, can determine how organisms adapt (or not) to HIREC. some species can modify their call characteristics to con- Social behaviour responses, in particular, are of special trast acoustically with noise pollution. For example, Cauca importance given their role in population dynamics (i.e. poison frogs, Andinobates bombetes (Fig. 1I), vocalise in reproductive success and offspring survival). Thus, by moments of low background noise and call less when noise combining animal behaviour and conservation issues, is higher (Vargas-Salinas and Amézquita 2013; Jiménez- we can improve our understanding and predictions of Vargas and Vargas-Salinas 2021), while Bloody Bay poison how susceptible different species and populations are to frogs (Mannophryne olmonae) increase higher frequency HIREC. Fig. 3 Conceptual overview. The main driving forces of HIREC (A that HIREC will particularly threaten juveniles and larvae, where less climate change, B habitat fragmentation, C chemical pollution, and consistent rainfall and higher temperatures will limit the availability D novel pathogens and diseases) interact across habitats implicating and diversity of larval nurseries and increase the desiccation prob- cascading effects on the social behaviours of amphibians. Through- ability of clutches. (II) In response to these threats, we hypothesise out the tropics, these disturbances will impact a large diversity of spe- that parents will both increase care and the flexibility in deposition cies with consequences detectable at every life stage. (I) We predict choices 1 3 acta ethologica provide a link to the Creative Commons licence, and indicate if changes 2. Due to their diverse and complex social behaviours, as were made. The images or other third party material in this article are well as their occurrence in often degraded habitats, poi- included in the article's Creative Commons licence, unless indicated son frogs are an interesting group to study the potential otherwise in a credit line to the material. If material is not included in impacts of and social responses to HIREC (see Fig. 3 for the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will a summary). need to obtain permission directly from the copyright holder. To view a 3. To compensate for negative HIREC impacts, we predict copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . individuals to increase parental care efforts by spending more time attending clutches and transporting tadpoles to further and fewer nursery sites. 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Gaster- toriality, Andrius Pašukonis for making his amphibian vector drawings osteus Aculeatus Animal Behaviour 62(4):775–780. https:// doi. publicly available, Jennifer Devillechabrolle for her help getting photos org/ 10. 1006/ anbe. 2001. 1824 illustrating gold mining activities, and two anonymous referees for their Bergeron CM, Hopkins WA, Todd BD, Hepner MJ, Unrine JM (2011) positive and thoughtful feedback. Many thanks to Mileidy Betancourth, Interactive effects of maternal and dietary mercury exposure have Justin P. Lawrence, Bernard Gissinger, Alexandre David, and Fernando latent and lethal consequences for amphibian larvae. Environ Sci Vargas-Salinas for allowing us to use their photographs. 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acta ethologica – Springer Journals
Published: Aug 3, 2022
Keywords: HIREC; Communication; Behavioural plasticity; Parental care; Territoriality; Tadpoles
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