Ant and poison dart frog interactions

The ability to use small molecule alkaloids as defensive chemicals has evolved in many organisms, often via trophic interactions due to dietary specialization. Animals with diet-derived defenses must balance food choices to maintain their defense reservoirs along with other physiological needs. However, environmental availability of prey and dietary preferences of vertebrate animals with acquired defenses remains largely unexplored. Here, we test the hypothesis that poison frogs that sequester alkaloids from their arthropod prey display prey preference. We collected alkaloid-defended Diablito frogs (Oophaga sylvatica) and leaf litter samples in five localities in northwestern Ecuador. Additionally, we collected the undefended Chimbo rocket frogs (Hyloxalus infraguttatus) from one locality in which it is living in sympatry with O. sylvatica. We found that both diets and skin alkaloids of O. sylvatica frogs were distinct among localities, and that undefended and sympatric H. infragutt...

PLoS ONE, 2013

Whereas interspecific associations receive considerable attention in evolutionary, behavioural and ecological literature, the proximate bases for these associations are usually unknown. This in particular applies to associations between vertebrates with invertebrates. The West-African savanna frog Phrynomantis microps lives in the underground nest of ponerine ants (Paltothyreus tarsatus). The ants usually react highly aggressively when disturbed by fiercely stinging, but the frog is not attacked and lives unharmed among the ants. Herein we examined the proximate mechanisms for this unusual association. Experiments with termites and mealworms covered with the skin secretion of the frog revealed that specific chemical compounds seem to prevent the ants from stinging. By HPLC-fractionation of an aqueous solution of the frogs' skin secretion, two peptides of 1,029 and 1,143 Da were isolated and found to inhibit the aggressive behaviour of the ants. By de novo sequencing using tandem mass spectrometry, the amino acid sequence of both peptides consisting of a chain of 9 and 11 residues, respectively, was elucidated. Both peptides were synthesized and tested, and exhibited the same inhibitory properties as the original frog secretions. These novel peptides most likely act as an appeasement allomone and may serve as models for taming insect aggression. Citation: Rö del M-O, Brede C, Hirschfeld M, Schmitt T, Favreau P, et al. (2013) Chemical Camouflage -A Frog's Strategy to Co-Exist with Aggressive Ants. PLoS ONE 8(12): e81950.

Journal of Chemical Ecology, 2000

Neotropical poison frogs (Dendrobatidae) contain a wide variety of lipophilic alkaloids, apparently accumulated unchanged into skin glands from dietary sources. Panamanian poison frogs (Dendrobates auratus) raised in a large, screened, outdoor cage and provided for six months with leaf-litter from the frog's natural habitat, accumulated a variety of alkaloids into the skin. These included two isomers of the ant pyrrolizidine 251K; two isomers of the 3,5-disubstituted indolizidine 195B; an alkaloid known to occur in myrmicine ants; another such indolizidine, 211E; two pyrrolidines, 197B and 223N, the former known to occur in myrmicine ants; two tricyclics, 193C and 219I, the former known to occur as precoccinelline in coccinellid beetles; and three spiropyrrolizidines, 222, 236, and 252A, representatives of an alkaloid class known to occur in millipedes. The alkaloids 211E, 197B, and 223N appear likely to derive in part from ants that entered the screened cage. In addition, the frog skin extracts contained trace amounts of four alkaloids, 205D, 207H, 219H, and 231H, of unknown structures and source. Wild-caught frogs from the leaf-litter site contained nearly 40 alkaloids, including most of the above alkaloids. Pumiliotoxins and histrionicotoxins were major alkaloids in wild-caught frogs, but were absent in captive-raised frogs. Ants microsympatric with the poison frog at the leaf-litter site and at an island site nearby in the Bay of Panamá were examined for alkaloids. The decahydroquinoline (−)-cis-195A and two isomers of the pyrrolizidine 251K were found to be shared by microsympatric myrmicine ants and poison frogs. The proportions of the two isomers of 251K were the same in ant and frog.

Proceedings of the …, 2005

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 fro...

Journal of Chemical Ecology, 2016

Poison frogs sequester chemical defenses from arthropod prey, although the details of how arthropod diversity contributes to variation in poison frog toxins remains unclear. We characterized skin alkaloid profiles in the Little Devil poison frog, Oophaga sylvatica (Dendrobatidae), across three populations in northwestern Ecuador. Using gas chromatography/mass spectrometry, we identified histrionicotoxins, 3,5- and 5,8-disubstituted indolizidines, decahydroquinolines, and lehmizidines as the primary alkaloid toxins in these O. sylvatica populations. Frog skin alkaloid composition varied along a geographical gradient following population distribution in a principal component analysis. We also characterized diversity in arthropods isolated from frog stomach contents and confirmed that O. sylvatica specialize on ants and mites. To test the hypothesis that poison frog toxin variability reflects species and chemical diversity in arthropod prey, we (1) used sequencing of cytochrome oxidase 1 to identify individual prey specimens, and (2) used liquid chromatography/mass spectrometry to chemically profile consumed ants and mites. We identified 45 ants and 9 mites in frog stomachs, including several undescribed species. We also showed that chemical profiles of consumed ants and mites cluster by frog population, suggesting different frog populations have access to chemically distinct prey. Finally, by comparing chemical profiles of frog skin and isolated prey items, we traced the arthropod source of four poison frog alkaloids, including 3,5- and 5,8-disubstituted indolizidines and a lehmizidine alkaloid. Together, the data show that toxin variability in O. sylvatica reflects chemical diversity in arthropod prey.

Salamandra, 2010

An alkaloid-sequestering frog, Dendrobates auratus, and a non-toxic frog, Physalaemus pustulosus were offered as prey to theraphosid spiders, Sericopelma rubronitens. The spiders, which do not use visual cues when hunting, sampled all presented frogs. They rejected, or failed to fully consume, toxic frogs significantly more often than the sympatric non-toxic frogs. Alkaloid sequestration did not protect D. auratus from attacks, but did reduce the risk of being eaten. The spiders are one of only a few documented predators of D. auratus on the Panamanian island of Taboga, and may represent a strong selective force for the high toxicity in this population.

2022

The ability to acquire chemical defenses through the diet has evolved across several major taxa. Chemically defended organisms may need to balance chemical defense acquisition and nutritional quality of prey items. However, these dietary preferences and potential trade-offs are rarely considered in the framework of diet-derived defenses. Poison frogs (Family Dendrobatidae) acquire defensive alkaloids from their arthropod diet of ants and mites, although their dietary preferences have never been investigated. We conducted prey preference assays with the Dyeing Poison frog (Dendrobates tinctorius) to test the hypothesis that alkaloid load and prey traits influence frog dietary preferences. We tested size preferences (big versus small) within each of four prey groups (ants, beetles, flies, and fly larvae) and found that frogs preferred interacting with smaller prey items of the fly and beetle groups. Frog taxonomic prey preferences were also tested as we experimentally increased their ...

Defensive chemicals in anuran skin secretions function in protection against potential predators.Although studies have demonstrated that particular chemicals are effective against certain predators, very little is known about how different chemicals from different species function against the same predators. Understanding how different chemicals function as a defence against similar predators is fundamental to the ecology and evolution of chemical defences in frogs. In the present study, the defensive function of bufadienolide-based defences in adult Rhaebo haematiticus (Bufonidae) were compared with alkaloid-based defences in adult and juvenile Dendrobates auratus (Dendrobatidae) against the same predators. Most bufonids contain synthesized bufadienolides, whereas dendrobatids contain dietary-derived alkaloids. Predation trials were performed with two potential invertebrate predators, Paraponera clavata (bullet ant) and Cupiennius coccineus (ctenid spider), to determine how these predators respond to two different types of frog chemical defence. The non-chemically defended frog Craugastor fitzingeri served as a control in all predation trials. Our results suggest that bufadienolide defences of R. haematiticus and alkaloid defences of D. auratus are equally effective towards bullet ant and ctenid spider predators. The similar avoidance and cleaning behaviours exhibited by these ants and spiders after contact with bufadienolides and alkaloids suggest that both types of defence are unpalatable to these arthropod predators.

Conservation Biology, 2020

Invasive species have major impacts on biodiversity and are one of the major causes of amphibian decline and extinction. Unlike other top ant invaders known to negatively affect larger fauna via chemical defensive compounds, the Argentine ant (Linepithema humile) does not have a functional sting; but nonetheless deploys defensive compounds against competitors and adversaries. We characterised the potential effect of L. humile's venom on amphibian species, using complementary approaches (field and laboratory) and comparative analyses (L. humile vs. native ant species). We estimated levels of ant aggression directed at three native terrestrial amphibians, the composition and quantities of the toxin used, and the mechanisms of toxicity in juvenile amphibians. To determine the potential scope of the threat faced by amphibians, we employed global databases to estimate the number of terrestrial amphibian species whose ranges overlapped with those of L. humile, looking at the IUCN Red List status of those species. We show how juvenile amphibian, co-occurring spatially and temporally with L. humile, are killed in the ant's trails. Laboratory tests revealed that, upon contact, the invasive ants rapidly spray pygidial-gland venom onto the juveniles' permeable skin. Chemical analyses indicate that iridomyrmecin is the compound responsible: following absorption, it accumulates in brain, kidney, and liver tissue, acting at species-dependent doses. Moreover, we estimated that at least 817 terrestrial amphibian species around the world overlap in range with L. humile, and 6.2% of them are classified as threatened by IUCN. Our findings highlight the high potential of the venom to negatively affect amphibian juveniles and provide a basis for exploring the largely overlooked impacts in this ant in its wide invasive range.