Behavioural responses of carnivorous marsupials (Planigale maculata) to toxic invasive cane toads (Bufo marinus)

The arrival of a toxic invasive species may impose selection on local predators to avoid consuming it. Feeding responses may be modified via evolutionary changes to behaviour, or via phenotypic plasticity (e.g. learning, taste aversion). The recent arrival of cane toads (Bufo marinus) in the Northern Territory of Australia induced rapid aversion learning in a predatory marsupial (the common planigale, Planigale maculata). Here, we examine the responses of planigales to cane toads in north‐eastern Queensland, where they have been sympatric for over 60 years, to investigate whether planigale responses to cane toads have been modified by long‐term exposure. Responses to toads were broadly similar to those documented for toad‐naïve predators. Most Queensland planigales seized (21 of 22) and partially consumed (11 of 22) the first toad they were offered, but were likely to ignore toads in subsequent trials. However, unlike their toad‐naïve conspecifics from the Northern Territory, the Queensland planigales all survived ingestion of toad tissue without overt ill effects and continued to attack toads in a substantial proportion of subsequent trials. Our data suggest that (i) learning by these small predators is sufficiently rapid and effective that selection on behaviour has been weak; and (ii) physiological tolerance to toad toxins may be higher in planigales after 60 years (approximately 60 generations) of exposure to this toxic prey.     

Evidence that catecholaminergic systems mediate dynamic colour change during explosive breeding events in toads

Many animals communicate by rapidly (within minutes or seconds) changing their body coloration; however, we know little about the physiology of this behaviour. Here we study how catecholaminergic hormones regulate rapid colour change in explosive breeding toads (Duttaphrynus melanostictus), where large groups of males gather and quickly change their colour from brown to bright yellow during reproduction. We find that both epinephrine (EP) and/or norepinephrine (NE) cause the toads'' skin to become yellow in minutes, even in the absence of social and environmental cues associated with explosive breeding. We hypothesize that natural selection drives the evolution of rapid colour change by co-opting the functional effects of catecholaminergic action. If so, then hormones involved in ‘fight or flight’ responses may mechanistically facilitate the emergence of dynamic visual signals that mediate communication in a sexual context.     

Involvement of carbohydrate moieties of the toad egg vitelline coat in binding with fertilizing sperm

Vitelline coats (VC) were isolated from the eggs of Bufo japonicus , and were added with sperm in reconstituted salt solution, which mimics the physiological role of jelly envelopes, to determine the rates of sperm binding per unit area (0.2 mm²) of VC. The rate of sperm binding to VC from uterine eggs was high, but was low to VC from coelomic eggs and eggs activated in 1/20 De Boer's solution (DB) and moderately low to VC from eggs activated in DB. The binding rate increased when VC from coelomic eggs were treated with extracts of the pars recta portion of the oviduct. The sperm that bound to VC were not acrosome-reacted and their binding to VC required both a low salinity, assuring motility of sperm, and sufficiently high levels of Ca²⁺ and Mg²⁺. The rate of sperm binding was reduced by either coexisting solubilized VC materials, periodate-oxidation of VC or the pretreatment of VC with Fab fragments of anti-VC antibodies, which reacted mostly to carbohydrate residues of VC glycoproteins. Sperm-VC binding assays in combination with gel-filtrated VC components revealed that the fractions containing 36–39 kDa components were most effective both in inhibiting the binding and in neutralizing the antibody induced inhibition of binding. These results indicate that carbohydrate moieties in 36–39 kDa glycoproteins of VC, exposed as a result of hydrolysis by the oviducal pars recta protease, are involved in binding with fertilizing sperm.     

Dynamic sexual dichromatism in an explosively breeding Neotropical toad

Sexual selection often promotes the evolution of elaborate colour signals in males, but the importance of sexually selected colour signals remains poorly studied in amphibians. We used reflectance spectrometry to document pronounced sexual dichromatism and dramatic colour change in Bufo luetkenii, a toad that breeds in large aggregations at the onset of the rainy season in Costa Rica. Our observations suggest that males fade rapidly from a vibrant lemon yellow to a dull brown once they have paired with a female. We demonstrate this by showing that males are much brighter than females and that unpaired males are more colourful than males in amplexus. We also show that coloration fades rapidly when males are briefly held captive. This is, to our knowledge, the first study to document such dynamic change in male coloration and sexual dichromatism in anurans.     

The ontogeny of kin recognition in tadpoles of the toadBufo melanostictus (Anura; Bufonidae)

The ontogeny of kin recognition and influence of social environment on the development of kin recognition behaviour was experimentally investigated in tadpoles of Bufo melanostictus that lived in aggregations and showed low larval dispersion. Embryos and tadpoles of the toad were reared as (i) kin only, (ii) with kin and non-kin (separated by a mesh screen), and (iii) in isolation. They were tested for the ability to discriminate between (i) familiar siblings and unfamiliar non-siblings, (ii) familiar siblings and familiar non-siblings and, (iii) unfamiliar siblings and unfamiliar non-siblings. All tadpoles were fed on boiled spinach before conducting trials. Preference of test tadpoles to associate near the end compartments whether empty or containing members of specific stimulus groups was assessed using a rectangular choice tank. When tested in tanks with empty end compartments, the test tadpoles showed random distribution and thus no bias for the apparatus or the procedure. In the presence of kin/non-kin in the end compartments a significantly greater number of test tadpoles spent the majority of the time near familiar or unfamiliar kin rather than near familiar or unfamiliar non-kin. Kin discrimination ability persisted throughout larval development. Familiarity with siblings is not required for discriminating kin from non-kin, and kin discrimination ability is not modified following exposure to non-kin. Also, involvement of dietary cues is unlikely to be the prime mechanism of kin recognition inB. melanostictus unlike in some other anurans.     

Opposite effects of cooling on twitch contractions of skeletal muscle isolated from tropical toads (Leptodactylidae) and northern frogs (Ranidae)

Cooling increases the twitch force of frog skeletal muscle (Rana temporaria; Rana pipiens), but decreases the twitch force of tropical toad muscle (Leptodactylus insularis). Action potentials and intramembranous charge movement in frog and toad fibers were slowed identically by cooling. Cooling increased the integral of twitch Ca²⁺ detected by aequorin in frog fibers (1.4-fold), while also decreasing the peak and slowing the rate of decay. Conversely, cooling decreased the integral (0.6-fold) and the peak of twitch Ca²⁺ in toad fibers, without affecting the rate of decay. The difference in entire Ca²⁺ transients may account for cold-induced twitch potentiation in frogs and twitch paralysis in toads. In sustained contractions of toad fibers, cooling markedly decreased maximum force caused by: (i) tetanic stimulation, (ii) two-microelectrode voltage clamp steps, (iii) high [K⁺], or (iv) caffeine. Maximum force in sustained contractions was decreased moderately by cooling frog fibers. Rapid rewarming and simultaneous removal of high [K⁺] or caffeine during a sustained contraction, caused toad muscle force to rise towards the value corresponding to the warm temperature. This did not occur after removing high [K⁺] or caffeine from toad fibers kept in the cold. Transmission electron micrographs showed no relevant structural differences. Parvalbumins are thought to promote relaxation of frog muscle in the cold. The unique parvalbumin isoforms in toad muscle apparently lack this property. Accepted: 27 August 1998