Predator-induced defences inDaphnia longicephala: location of kairomone receptors and timeline of sensitive phases to trait formation

Abstract

The freshwater crustacean Daphnia adapts to changing predation risks by forming inducible defences. These are only formed when they are advantageous, saving associated costs when the defence is superfluous. However, in order to be effective, the time lag between the onset of predation and the defence formation has to be short. Daphnia longicephala develop huge protective crests upon exposure to chemical cues (kairomones) from its predator the heteropteran backswimmer Notonecta glauca. To analyse time lags, we determined kairomone-sensitive stages and the developmental time frames of inducible defences. Moreover, we looked at additive effects that could result from the summation of prolonged kairomone exposure. Kairomones are perceived by chemoreceptors and integrated by the nervous system, which alters the developmental program leading to defence formation. The underlying neuronal and developmental pathways are not thoroughly described and surprisingly, the location of the kairomone receptors is undetermined. We show that D. longicephala start to sense predator cues at the onset of the second juvenile instar, defences develop with a time lag of one instar and prolonged kairomone exposure does not impact the magnitude of the defence. By establishing a method to reversibly impair chemosensors, we show the first antennae as the location of kairomone-detecting chemoreceptors. This study provides fundamental information on kairomone perception, kairomone-sensitive stages, developmental time frames and lag times of inducible defences in D. longicephala that will greatly contribute to the further understanding of the neuronal and developmental mechanisms of predator-induced defences in Daphnia.

Mechanisms underlying the control of responses to predator odours in aquatic prey

“…In Daphnia longicephala, predator odours are detected by sensory systems located on the first antennae (Weiss et al, 2015a), which connect to the deutocerebrum in the central nervous system, where olfactory cues are processed (Weiss et al, 2012c). Similarly, predator odours are detected by receptors located on the rhinophores of the nudibranch Tritonia diomedea (Wyeth, 2006), which form part of the system analogous to olfaction (Di Cosmo and Winlow, 2014).…”

Divergent developmental patterns of induced morphological defenses in rotifers and Daphnia: Ecological and evolutionary context

“…In the formation of head crests in D. longicephala , the developmental window for sensitivity to Notonecta kairomones is delayed until the second juvenile instar, which allows for the formation of the crest in the fourth juvenile instar and all subsequent instars (Weiss et al ). This restriction of the defensive crest to larger instars (late juveniles and adults) matches the vulnerable period of postembryonic development in these Daphnia to notonectids, which select larger prey.…”

“…A similar set of induced defenses is present in both D. cucullata and D. longicephala. The development of a longer tail spine and a stronger, more stable carapace accompanies the formation of the Chaoborus ‐induced helmet in D. cucullata (Laforsch and Tollrian ; Laforsch et al ), as well as the Notonecta ‐induced head crest in D. longicephala (Weiss et al ; Kruppert et al ). Longer tail spines are also associated with the induction of helmets in a variety of other Daphnia species (Dodson , ; Brancelj et al ; Dzialowski et al ; Engel and Tollrian ; Herzog and Laforsch ).…”

“…These defenses are therefore most advantageous in larger, more vulnerable Daphnia instars (adults and larger juveniles), and it is in these larger individuals that crests are best developed. Weiss et al () found that D. longicephala first develops enlarged crests in response to Notonecta kairomones in the fourth juvenile instar and maintains them in subsequent instars if kairomone exposure is continued. No morphological defenses were formed prior to this later stage of juvenile development.…”

Seasonal plasticity in anti-predatory strategies: Matching of color and color preference for effective crypsis

“…For example, the protective morphology of Daphnia crustaceans is induced by chemical cues that signal predator presence (Grant and Bayly ; Weiss et al. ). Plasticity in anti‐predator strategies also occurs in response to abiotic factors such as those that affect the visual background under which species need to escape predator attention.…”