Native frogs (Rana pirica) do not respond adaptively to alien toads (Bufo japonicus formosus) 100 years after introduction

Abstract

Biological invasions adversely affect the survival of many native species, but long-term consequences of the novel pressures imposed by invaders on natives are less clear. If natives can adapt to the presence of the invader, the severity of impact will decline with time. On Hokkaido, Japan, alien toads (Bufo japonicus formosus) are highly toxic to native frog tadpoles (Rana pirica) that attempt to eat their hatchlings. Therefore, the arrival of toads potentially imposes selection pressure on native frogs in the context of behavioral response (feeding aversion) and physiological resistance to toad toxins. Here, we compared the consumption tendency and toxin resistance of R. pirica from several sites with different histories of toad invasion (0 to >100 years exposure). We found no evidence of adaptive response to invasive toads. The vast majority of R. pirica tadpoles from all sites readily consumed toad hatchlings and died, regardless of time since invasion or whether hatchlings were from sympatric versus allopatric toad populations. In contrast, tadpoles of a closely related species (Rana ornativentris), which co-occurs naturally with B. j. formosus on Honshu, readily consumed toad hatchlings without ill effect. Our results indicate that the lethal toxic effect of the alien toads on native frogs on Hokkaido is maintained over long time periods without mitigation through adaptation.

A biological invasion reduces rates of cannibalism by Japanese toad tadpoles

“…To add to this area of research, we compared rates of cannibalism by a toad species (Japanese common toad, Bufo japonicus ) that has been translocated from the island of Honshu (native range) to the northern island of Hokkaido (invasive range). The translocation occurred around 100 years ago, similar to the timescale of the invasion of Australia by cane toads 20 , 21 . Like Australia, Hokkaido had no native bufonid species prior to the invader’s arrival 20 , 21 .…”

“…The translocation occurred around 100 years ago, similar to the timescale of the invasion of Australia by cane toads 20 , 21 . Like Australia, Hokkaido had no native bufonid species prior to the invader’s arrival 20 , 21 . These similarities between the two bufonid species which share life histories 22 , provide a unique opportunity to test whether (1) invasion affects intensity of cannibalism among amphibians in the same ways, and (2) if any such changes are due to evolved shifts in vulnerability of eggs and hatchlings versus predatory behaviour of tadpoles.…”

“…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 .…”

“…In contrast, B. japonicus is toxic to amphibians within its invasive range, including on Hokkaido, as these species have no evolutionary history of exposure to bufonids 20 , 21 . On Hokkaido, tadpoles of Rana pirica consume invasive B. japonicus hatchlings, but are almost always killed by the toxins 20 , 21 , 28 , 30 .…”

Alien toxic toads suppress individual growth and phenotypic development of native predatory salamanders

“…Bufo j. formosus is a toad species native to the eastern area of Honshu Island, the main island in the Japanese archipelago. Bufo j. formosus has been introduced into multiple locations on Hokkaido Island, starting ~ 100 years ago and continuing until several decades ago (Saito, 2002;Naito & Shiga, 2016;Okamiya et al, 2021). This alien toad has now established populations in several areas on Hokkaido (Asahikawa, Sapporo, Muroran and Hakodate; Naito & Shiga, 2016;Saito, 2002).…”