Abstract
Living in mix-species aggregations provides animals with substantive anti-predator, foraging and locomotory advantages while simultaneously exposing them to costs, including increased competition and pathogen exposure. Given each species possess unique morphology, competitive ability, parasite vulnerability and predator defences, we can surmise that each species in mixed groups will experience a unique set of trade-offs. In addition to this unique balance, each species must also contend with anthropogenic changes, a relatively new, and rapidly increasing phenomenon, that adds further complexity to any system. This complex balance of biotic and abiotic factors is on full display in the exceptionally diverse, yet anthropogenically degraded, Great Barrier Reef of Australia. One such example within this intricate ecosystem is the inability of some damselfish to utilize their own chemical alarm cues within degraded habitats, leaving them exposed to increased predation risk. These cues, which are released when the skin is damaged, warn nearby individuals of increased predation risk and act as a crucial associative learning tool. Normally, a single exposure of alarm cues paired with an unknown predator odour facilitates learning of that new odour as dangerous. Here, we show that Ambon damselfish, Pomacentrus amboinensis, a species with impaired alarm responses in degraded habitats, failed to learn a novel predator odour as risky when associated with chemical alarm cues. However, in the same degraded habitats, the same species learned to recognize a novel predator as risky when the predator odour was paired with alarm cues of the closely related, and co-occurring, whitetail damselfish, Pomacentrus chrysurus. The importance of this learning opportunity was underscored in a survival experiment which demonstrated that fish in degraded habitats trained with heterospecific alarm cues, had higher survival than those we tried to train with conspecific alarm cues. From these data, we conclude that redundancy in learning mechanisms among prey guild members may lead to increased stability in rapidly changing environments.
Highlights
Reef compared to those that were not trained[16]
We ask whether a species that is affected by coral degradation, in this case the Ambon damselfish, Pomacentrus amboinensis, can learn the identity of unknown predators in degraded coral from direct conditioning with alarm cues from a closely related species, the whitetail damselfish (P. chrysurus), whose alarm cues are resistant to the effects of coral d egradation[12]
The response of the fish to the predator was affected by an interaction between coral environment and conditioning treatment (F2,76 = 22.8, p < 0.001, Fig. 1, see Supplementary Table 2), meaning that the effect of conditioning was contingent upon the coral environment in which the fish were maintained
Summary
Reef compared to those that were not trained[16]. Likewise, Ambon damselfish (P. amboinensis) that underwent predator training had a 3.5 times greater survival upon recruitment to the reef[17]. In the current experiment, we conditioned predator-naïve Ambon damselfish to recognize the odour of predatory dottyback (Pseudochromis fuscus) as risky by exposing them to conspecific alarm cues (positive control), heterospecific alarm cues or seawater (negative control) in tanks containing water from either healthy or degraded corals. We followed this laboratory investigation by directly testing whether fish that have undergone survival training with conspecific and heterospecific alarm cues in healthy versus dead coral environments have higher survival when stocked onto the reef. Assessing survival in the wild is the best way to test the importance of learning redundancy
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