Invasive predators induce plastic and adaptive responses during embryo development in a threatened frog

Abstract

Invasive predators can strongly affect native populations. If alien predator pressure is strong enough, it can induce anti-predator responses, including phenotypic plasticity of exposed individuals and local adaptations of impacted populations. Furthermore, maternal investment is an additional pathway that could provide resources and improve performance in the presence of alien predators. We investigated the potential responses to an alien predator crayfish (Procambarus clarkii) in a threatened frog (Rana latastei) by combining field observations with laboratory measurements of embryo development rate, to assess the importance of parental investment, origin and exposure to the crayfish cues. We detected a strong variation in parental investment amongst frog populations, but this variation was not related to the invasion status of the site of origin, suggesting that mothers did not modulate parental investment in relation to the presence of alien predators. However, cues of the invasive crayfish elicited plastic responses in clutches and tadpoles development: embryos developed faster when exposed to the predator. Furthermore, embryos from invaded sites reached Gosner’s development stage 25 faster than those from non-invaded sites. This ontogenetic shift can be interpreted as a local adaptation to the alien predator and suggests that frogs are able to recognise the predatory risk. If these plastic responses and local adaptation are effective escape strategies against the invasive predator, they may improve the persistence of native frog populations.

Presence of an alien turtle accelerates hatching of common frog (Rana temporaria) tadpoles

“…Studies examining predator effects on the developmental rates of both eggs and larvae are rare because few predators consume both eggs and larvae simultaneously. Muraro et al (2021) used a stage-nonspecific predator (Procambarus clarkii) and found, in concordance with our results, a reduction in hatching time in Rana latastei embryos. However, they did not study larval development.…”

“…Finding a general tendency in the phenotypic plasticity responses of prey across a broad range of animal predators (different taxa and feeding spectra), environmental and experimental conditions is a challenge even in anurans themselves (Relyea et al 2018). However, in frogs, the earlier hatching time was generally associated with smaller size at hatching (Capellán and Nicieza 2007;Chivers et al 2001;Ireland et al 2007;Laurila et al 2002) and lower developmental stage (Capellán and Nicieza 2007;Chivers et al 2001;Ireland et al 2007;Laurila et al 2002;Muraro 2021), and our results confirm this relationship. In some cases, earlier hatched tadpoles performed higher growth rate and reached the size of later hatched tadpoles at metamorphosis (Capellán and Nicieza 2007).…”

“…Native and naive prey may fail to detect the novel predator adequately as a dangerous threat, resulting in no (Cox and Lima 2006;Sih et al 2010) or inefficient antipredator responses to counter the predator's attack strategies (Sih et al 2010;Strauss et al 2006). However, when responses in hatching time in naive prey are detected, they are often explained by the presence of syntopic, taxonomically related predators (Melotto et al 2021;Muraro et al 2021;Sih et al 2010), although the time since invasion may also play an important role (Gomez-Mestre and Díaz-Paniagua 2011; Nunes et al 2013). Our results suggested that a common evolutionary history is not necessary for a detectable response.…”

Presence of an alien turtle accelerates hatching of common frog (Rana temporaria) tadpoles

“…Muraro et al (2021) used a stage-nonspecific predator (Procambarus clarkii) and found, in concordance with our results, a reduction in hatching time in Rana latastei embryos. However, they did not study larval development Ireland et al (2007).…”

“…Native and naive prey may fail to detect the novel predator adequately as a dangerous threat, resulting in no (Cox and Lima 2006;Sih et al 2010) or inefficient antipredator responses to counter the predator's attack strategies (Sih et al 2010;Strauss et al 2006). However, when responses in hatching time in naive prey are detected, they are often explained by the presence of syntopic, taxonomically related predators (Melotto et al 2021;Muraro et al 2021;Sih et al 2010), although the time since invasion may also play an important role (Gomez-Mestre and Díaz-Paniagua 2011; Nunes et al 2013). Our results suggested that a common evolutionary history is not necessary for a detectable response.…”