In deep trouble: Habitat selection constrained by multiple enemies in zooplankton

Abstract

Habitat selection behavior is an important predator-avoidance strategy for many organisms. Its particular expression is often explained as the result of a tradeoff between avoiding antagonists and acquiring resources. However, there is need for a broader perspective on this behavior, as organisms are often simultaneously involved in complex antagonistic relationships with multiple types of enemies. We show experimentally that a tradeoff between predator and parasite avoidance may be important in the evolution of habitat selection behavior in the waterflea, Daphnia magna. In this species, negatively phototactic clones suffer less from visually hunting predators by residing in deeper and darker portions of the water column during the day. However, this behavior increases the risk of parasitic infections when the Daphnia are exposed to pond sediments containing parasite spores. Positively phototactic clones, which are at a higher risk of predation, are less exposed to parasite spores in the sediment and consequently suffer less from parasitic infection. We show that the increased risk of infection remains even if the animals change their phototactic behavior on exposure to chemical cues from fish. This tradeoff highlights a substantial cost of predator-induced changes in habitat selection behavior. Tradeoffs caused by multiple enemies may explain genetic polymorphism for habitat selection behavior in many natural populations.I n the face of antagonistic interactions, habitat selection strategies in time and space are essential for the survival of many organisms. Many studies on predation have documented the ecological costs of antipredatory habitat selection behavior, such as reduced food intake, reduced competitive strength, and increased susceptibility to predation by a different kind of predator (1, 2). It has been suggested that such costs favor the evolution of inducible defenses (2) such as diel vertical migration (DVM), which is generally considered to be a predatoravoidance strategy of zooplankton (3-5). In this strategy, the zooplankton reside at greater depths during the day, thus reducing their chance of being detected by visual predators (4, 5). It has been shown that DVM can be induced in several taxa by exposing them to predator kairomones (6-8), i.e., chemical cues that indicate the presence of the predator. Phenotypic variation in induced and constitutive (not dependent on environmental stimuli for activation; ref. 9) DVM has a strong genetic component (8,(10)(11)(12), and the trait shows rapid evolutionary response to changing predator regimes (13).Predators are not the only antagonists that the zooplankton face. Parasites (including pathogens) are common in zooplankton populations, and the fitness costs of infection are severe (14-19). Many parasites produce infective stages within the bottom sediments, where they form long-lasting spore banks (14-16). Because DVM is often so pronounced that the zooplankton reside in, at, or near the bottom sediments during the day (20, 21), we hypothesized that t...

Resistance to a bacterial parasite in the crustacean Daphnia magna shows Mendelian segregation with dominance

“…It is likely that other loci other than the one described here are involved in other steps of the infection process. For example, encounter of the parasite spores, which reside in the sediment, may be dependent on diel vertical migration, which has been shown to have a strong genetic component (Decaestecker et al, 2002). It has also been suggested that genes affecting parasite proliferation within the host might be different from those involved in attachment (Decaestecker et al, 2007;Duneau et al, 2011).…”

Apparent seasonality of parasite dynamics: analysis of cyclic prevalence patterns

“…An earlier study has further shown that O. bayeri spores survive drought (Vizoso et al 2005). Long-lasting parasite spore banks have been found for other Daphnia microparasites and are likely to be important for disease dynamics (Ebert 1995;Ebert et al 1997;Decastaecker et al 2002Decastaecker et al , 2004.…”

The coexistence of hybrid and parentalDaphnia: the role of parasites

“…), all infected females were smaller than non-infected ones (F 1,5 Z56.85, p!0.001). Decaestecker et al (2002) proposed that observed differences in the infection patterns among Daphnia magna clones might be caused by differences in their vertical distributions. If sediment is a source for parasite spores, the infection risk is higher for clones, which perform deeper migrations (known as the 'deep trouble hypothesis').…”