Are toxic effects of alien species affected by their prey? Evaluation by bioassay with captive-bred toad embryos and a vulnerable predator

Abstract

Toads of the Family Bufonidae possess neurotoxins (bufadienolides) which are generally considered to be synthesized de novo. Thus, invasive toad species pose a threat to native predators via toxic effects. However, the influence of diet on toad toxicity is poorly understood. We evaluated the effect of diet on toxicity of embryos of the invasive toad Bufo japonicus formosus in Japan, using native tadpoles (Rana pirica) as a bioassay. Specifically, we compared the toxicity of embryos spawned by captive toads reared entirely on non-toxic prey versus embryos spawned by wild toads. Embryos of captive-reared toads and wild toads were comparable in terms of toxic effects: all tadpoles that consumed a toad embryo died, irrespective of origin of embryos. Embryo toxicity appears to be via parental (likely maternal) provisioning. Our study indicates that adult B. j. formosus produce toxins (likely bufadienolides) in amounts sufficient for embryos to be fatal to native predator tadpoles irrespective of whether the adult diet contains toxins. Thus, the toxic effects of invasive B. j. formosus on R. pirica, and possibly on other sensitive native predator species, are likely to be widespread and occur regardless of variation in prey biota in invaded areas in Japan.

A biological invasion reduces rates of cannibalism by Japanese toad tadpoles

“…Detailed studies in Australian cane toads have shown that toxins released from eggs close to the time of hatching attract cannibalistic larvae, and also induce foraging responses by those larvae 13,33,34 . A similar situation is plausible with the Japanese toads, that also produce eggs containing toxins (as evidenced by high mortality rates of toad-naïve predators consuming those eggs or hatchlings: 16,17,[23][24][25] ). The decrease in rates of cannibalism in invasive populations of Japanese toads thus might re ect a lower attraction to such cues by conspeci c larvae and a decrease in toxin content, a change in toxin composition, or a decrease in rates of toxin release by embryos.…”

“…Adult B. japonicus exhibit geographic variation in toxin (bufadienolide) composition within their native range 36 . Because the toxins in B. japonicus eggs and hatchlings are maternally-invested 24,25 , similar geographic variation presumably also occurs in the toxin composition of toad embryos. However, whether the toxin composition of B. japonicus in the invasiverange (Hokkaido) differs from that of native-range populations remains to be determined.…”

“…Predation typically is high on the hatchling stage: that is, larvae that have hatched out from the egg capsule but have not yet attained locomotor capacity 16,23 . Although the eggs and hatchlings of Japanese common toads contain maternally-invested toxins 24,25 , amphibian taxa that are native to Honshu (and hence, have a long history of sympatry with the toads) readily consume invasive toad hatchlings and can tolerate those toxins (predatory frog tadpoles: Rana ornativentris, predatory salamander larvae: Hynobius nigrescens; 16,17 .…”

“…The situation is different in the invasive range on Hokkaido, where the hatchlings of invasive toads are toxic to amphibian species native to that island (which have no evolutionary history of exposure to bufonids). On Hokkaido, tadpoles of Rana pirica readily consume invasive toad hatchlings, but are almost always killed by the toxins 16,17,23,25 . Native Hokkaido salamander larvae (Hynobius retardus) also readily consume invasive toad hatchlings, with survival rates varying from 6 to 77% among populations 16,23 .…”

A biological invasion reduces rates of cannibalism by Japanese toad tadpoles

“…Hatchlings typically experience high levels of predation pressure by aquatic predators prior to attaining locomotor capacity 20 , 28 . The eggs and hatchlings of B. japonicus contain maternally-invested toxins 29 , 30 ; such toxins often act as a deterrent against aquatic predators 31 . However, amphibians that are native to Honshu and hence, have a long history of sympatry with B. japonicus , readily consume invasive-range B. japonicus hatchlings and can tolerate those toxins, including predatory frog tadpoles ( Rana ornativentris ) and salamander larvae ( Hynobius nigrescens ) 20 , 21 .…”