Fish kairomone-induced defenses in crustacean zooplankton: on the diversity of strategies, mechanism, and environment

Cohen, Jonathan H.Predator chemical cues, or kairomones, induce behavioral and morphological defense strategies in zooplankton. For example, several species become more responsive to light following exposure to fish kairomones. These behavioral changes likely impact diel vertical migration (DVM). A nearly universal behavior amongst zooplankton, DVM generally describes the nighttime ascent to feed and daytime descent to avoid visual predators. Although predator avoidance was proposed as the adaptive significance of DVM decades ago, we know little about the mechanism by which kairomones alter photobehavior. In addition, several zooplankton species exhibit kairomone-induced morphological defenses (e.g. spines), although previous reports of morphological plasticity have been generally limited to freshwater zooplankters. Despite laboratory and field evidence of kairomone-induced defenses, further work is needed to quantify the effective concentration of kairomone molecules in marine environments. ☐ Here, I first evaluated the mechanism by which kairomones enhance photoresponses in zooplankton. Comparing behavior and visual physiology (electrophysiology, eye structure), I found that kairomones altered photobehavior by increasing visual sensitivity at the photoreceptor level in the larvae of two marine crab species, Rhithropanopeus harrisii and Hemigrapsus sanguineus, as well as in a branchiopod crustacean, Artemia spp. Using similar behavioral experiments, I also found that signaling by a ubiquitous neurotransmitter, γ-aminobutyric acid (GABA), is required for detection and/or processing of predator kairomones in larval H. sanguineus. In addition, larvae lost the ability to detect kairomones after exposure to low pH/high CO2, over timescales that reflect diel/tidal pH cycles in coastal ecosystems (12 h). The mechanism of this pH effect differs from that described in fish, and the loss of kairomone-induced photosensitivity at low pH may be adaptive in these zooplankton under diel-cycling pH. ☐ In addition to behavioral defenses, crab larvae have spines. In some species, including R. harrisii, these spines are known to aid in predator defense. The freshwater crustacean zooplankton, Daphnia, exhibit drastic spine elongation after exposure to predator kairomones, but similar phenotypic plasticity has not been observed in estuarine or marine crustacean zooplankton. Here, I assessed the effect of developmental kairomone exposure on the morphology of crab larvae (R. harrisii and H. sanguineus). Kairomone exposure resulted in slightly elongated spines in larval R. harrisii as well as decreased consumption by a planktivorous fish, Menidia mendia, suggesting that the observed spine elongation is an inducible defense. ☐ The described behavioral and morphological defenses are induced by fish kairomones. In estuarine and marine systems, these signaling molecules are derived from body mucus and include sulfated glycosaminoglycans (sGAGs). Little work has been done to quantify these cues in marine environments or to assess whether kairomone concentrations used in laboratory studies reflect natural scenarios. During a two-year field study, I applied quantitative chemical and behavioral assays to measure these kairomones in an estuarine environment. I found that sGAG concentration and zooplankton photosensitivity were positively related to fish quantity. Further, sGAG concentration was similar between field samples and mucus extracts used in previous laboratory experiments, supporting that kairomone-induced changes to zooplankton behavior are not an artifact of laboratory experiments. ☐ The results of this dissertation have important implications to evolutionary biology, namely the evolution of sensory systems. For example, we can now compare the neural mechanisms that mediate kairomone-induced photobehavior in crustaceans to other zooplankton and ancestral defense mechanisms. More broadly, DVM impacts biogeochemical cycles and ecological interactions in aquatic environments. Hence, assessing the response of migrating zooplankton to environmental change (e.g. acidification, predator abundance) is essential in predicting ecosystem health. Although previous laboratory work has provided immense insight to zooplankton behavior in a controlled environment, there is still a great need for complementary fieldwork.University of Delaware, School of Marine Science and PolicyPh.D