Moving south: effects of water temperatures on the larval development of invasive cane toads (Rhinella marina) in cool‐temperate Australia

Abstract

The distributional limits of many ectothermic species are set by thermal tolerances of early‐developmental stages in the life history; embryos and larvae often are less able to buffer environmental variation than are conspecific adults. In pond‐breeding amphibians, for example, cold water may constrain viability of eggs and larvae, even if adults can find suitable thermal conditions in terrestrial niches. Invasive species provide robust model systems for exploring these questions, because we can quantify thermal challenges at the expanding range edge (from field surveys) and larval responses to thermal conditions (in the laboratory). Our studies on invasive cane toads (Rhinella marina) at the southern (cool‐climate) edge of their expanding range in Australia show that available ponds often average around 20°C during the breeding period, 10°C lower than in many areas of the toads’ native range, or in the Australian tropics. Our laboratory experiments showed that cane toad eggs and larvae cannot develop successfully at 16°C, but hatching success and larval survival rates were higher at 20°C than in warmer conditions. Lower temperatures slowed growth rates, increasing the duration of tadpole life, but also increased metamorph body mass. Water temperature also influenced metamorph body shape (high temperatures reduced relative limb length, head width, and body mass) and locomotor performance (increased speed from intermediate temperatures, longer hops from high temperatures). In combination with previous studies, our data suggest that lower water temperatures may enhance rather than reduce recruitment of cane toads, at least in areas where pond temperatures reach or exceed 20°C. That condition is fulfilled over a wide area of southern Australia, suggesting that the continuing expansion of this invasive species is unlikely to be curtailed by the impacts of relatively low water temperatures on the viability of early life‐history stages.

Should I stay or should I go? Complex environments influence the developmental plasticity of flight capacity and flight-related trade-offs

“…Differences in mean temperature can have strong effects on development time, growth rate, and body mass in ectotherms (Ratte, 1985;Atkinson, 1994;Kingsolver et al, 2009;Williams et al, 2012). However, independent of differences in mean temperature, we found that variation in temperature experienced during development also tends to decrease the developmental time and increase the growth rates, and body mass ( Figure 3A-C), consistent with other invertebrates (Ratte, 1985;Atkinson, 1994;Kingsolver et al, 2009;but see Kjaersgaard et al, 2013) as well as vertebrates (Wijethunga et al, 2016;Pepin, 1991;Shine & Harlow, 1996;Booth, 1998). Thus, ectotherms typically benefit from experiencing variable temperatures during their life-histories, as long as the rearing temperatures are within physiological limits (Worner 1992;Shine & Harlow, 1996;Elphick & Shine, 1998;Angilletta, 2009;Fischer et al, 2011;Colinet et al, 2015).…”

No evidence for cold-adapted life-history traits in cool-climate populations of invasive cane toads (Rhinella marina)

“…Such eurythermy may enable the cane toad to breed successfully in a wide range of conditions, and selection to enhance viability at low temperatures accordingly may be weak. Rearing temperature significantly affected many life-history traits, as previously reported by Wijethunga et al [ 6 ], but we lack field data to assess the fitness consequences of variation in traits such as larval duration and size at metamorphosis.…”

“…Although previous work has reported rapid adaptation and behavioural adjustments of cane toads in response to selective forces within tropical and arid environments [ 31 , 32 , 36 , 39 ] and shifts in thermal minimum tolerances in adult toads encountering cool conditions [ 10 , 11 ], we saw no such shifts in life-history traits of the early life-stages of toads in response to water temperature. Although toads in southern Australia are exposed to waterbodies that are substantially cooler than those used for spawning in tropical Australia [ 6 , 40 ] or the toads’ native range [ 41 ], the thermal responses of eggs and tadpoles were very similar in tropical versus temperate-zone populations. In an analogous result, Volpe [ 42 ] found no difference in response to experimental temperature of Incilius ( Bufo ) valliceps embryos from thermally diverse breeding environments (early and late breeding seasons).…”

“…Overall, our results highlight the broad thermal tolerance of Rhinella marina eggs and tadpoles. Substantial numbers of eggs hatched, and tadpoles survived and grew, even at 20°C–cooler than in potential spawning ponds at the southern edge of the toad’s current Australian range [ 6 ]. Such eurythermy may enable the cane toad to breed successfully in a wide range of conditions, and selection to enhance viability at low temperatures accordingly may be weak.…”

“…In ectotherms, environmental temperature controls developmental rates and a wide range of physiological processes [ 1 ]. Traits such as embryonic developmental trajectory, time to metamorphosis, body size at maturity, locomotor performance and growth rate are sensitive to developmental temperature [ 2 – 6 ]. As a result, geographical variation in thermal environments can limit the distribution of a species.…”