Ralph Tollrian

Transgenerational induction of defences in animals and plants

Predators are potent agents of natural selection in biological communities. Experimental studies have shown that the introduction of predators can cause rapid evolution of defensive morphologies and behaviours in prey and chemical defences in plants. Such defences may be constitutively expressed (phenotypically fixed) or induced when predators initially attack. Here we show that non-lethal exposure of an animal to carnivores, and a plant to a herbivore, not only induces a defence, but causes the attacked organisms to produce offspring that are better defended than offspring from unthreatened parents. This transgenerational effect, referred to as a maternally induced defence, is in contrast to the more common defences induced in single individuals within a generation. Transgenerational induction of defences is a new level of phenotypic plasticity across generations that may be an important component of predator–prey interactions.

PREDATOR FUNCTIONAL RESPONSES: DISCRIMINATING BETWEEN HANDLING AND DIGESTING PREY

We present a handy mechanistic functional response model that realistically incorporates handling (i.e., attacking and eating) and digesting prey. We briefly review current functional response theory and thereby demonstrate that such a model has been lacking so far. In our model, we treat digestion as a background process that does not prevent further foraging activities (i.e., searching and handling). Instead, we let the hunger level determine the probability that the predator searches for new prey. Additionally, our model takes into account time wasted through unsuccessful attacks. Since a main assumption of our model is that the predators hunger is in a steady state, we term it the steady-state satiation (SSS) equation. The SSS equation yields a new formula for the asymptotic maximum predation rate (i.e., asymptotic maximum number of prey eaten per unit time, for prey density approaching infinity). According to this formula, maximum predation rate is determined not by the sum of the time spent for handling and digesting prey, but solely by the larger of these two terms. As a consequence, predators can be categorized into two types: handling-limited predators (where maximum predation rate is limited by handling time) and digestion-limited predators (where maximum predation rate is limited by digestion time). We give examples of both predator types. Based on available data, we suggest that most predators are digestion limited. The SSS equation is a conceptual mechanistic model. Two possible applications of this model are that (1) it can be used to calculate the effects of changing predator or prey characteristics (e.g., defenses) on predation rate and (2) optimal foraging models based on the SSS equation are testable alternatives to other approaches. This may improve optimal foraging theory, since one of its major problems has been the lack of alternative models.

The impact of ultraviolet radiation on the vertical distribution of zooplankton of the genus Daphnia

The vertical migration of zooplankton into lower and darker water strata by day is generally explained by the avoidance of visually orienting predators, mainly fish; however, it is unclear why daily zooplankton migration has been maintained in fishless areas. In addition to predation, ultraviolet radiation—a hazardous factor for zooplankton in the surface layers of marine and freshwater environments—has been suspected as a possible cause of daytime downward migration. Here we test this hypothesis by studying several Daphnia species, both in a controlled laboratory system and under natural sunlight in an outdoor system. We selected Daphnia species that differed in their pigmentation as both melanin and carotenoids have been shown to protect Daphnia from ultraviolet light. All Daphnia species escaped into significantly deeper water layers under ultraviolet radiation. The extent to which the daphnids responded to this radiation was inversely linked to their pigmentation, which reduced ultraviolet transmission. These results suggest that ultraviolet avoidance is an additional factor in explaining daytime downward migration. Synergistic benefits might have shaped the evolution of this complex behaviour.

Consumer-food systems: why type I functional responses are exclusive to filter feeders

The functional response of a consumer is the relationship between its consumption rate and the abundance of its food. A functional response is said to be of type I if consumption rate increases linearly with food abundance up to a threshold level at which it remains constant. According to conventional wisdom, such type I responses are more frequent among filter feeders than among other consumers. However, the validity of this claim has never been tested. We review 814 functional responses from 235 studies, thereby showing that type I responses are not only exceptionally frequent among filter feeders but that they have only been reported from these consumers.

Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses.

Phenotypic plasticity is a key factor for the success of organisms in heterogeneous environments. Although many forms of phenotypic plasticity can be induced and retracted repeatedly, few extant models have analyzed conditions for the evolution of reversible plasticity. We present a general model of reversible plasticity to examine how plastic shifts in the mode and breadth of environmental tolerance functions (that determine relative fitness) depend on time lags in response to environmental change, the pattern of individual exposure to inducing and noninducing environments, and the quality of available information about the environment. We couched the model in terms of prey‐induced responses to variable predation regimes. With longer response lags relative to the rate of environmental change, the modes of tolerance functions in both the presence or absence of predators converge on a generalist strategy that lies intermediate between the optimal functions for the two environments in the absence of response lags. Incomplete information about the level of predation risk in inducing environments causes prey to have broader tolerance functions even at the cost of reduced maximal fitness. We give a detailed analysis of how these factors and interactions among them select for joint patterns of mode and breadth plasticity.

Density-dependent effects of prey defences.

Abstract In this study, we show that the protective advantage of a defence depends on prey density. For our investigations, we used the predator-prey model system Chaoborus-Daphnia pulex. The prey, D. pulex, forms neckteeth as an inducible defence against chaoborid predators. This morphological response effectively reduces predator attack efficiency, i.e. number of successful attacks divided by total number of attacks. We found that neckteeth-defended prey suffered a distinctly lower predation rate (prey uptake per unit time) at low prey densities. The advantage of this defence decreased with increasing prey density. We expect this pattern to be general when a defence reduces predator success rate, i.e. when a defence reduces encounter rate, probability of detection, probability of attack, or efficiency of attack. In addition, we experimentally simulated the effects of defences which increase predator digestion time by using different sizes of Daphnia with equal vulnerabilities. This type of defence had opposite density-dependent effects: here, the relative advantage of defended prey increased with prey density. We expect this pattern to be general for defences which increase predator handling time, i.e. defences which increase attacking time, eating time, or digestion time. Many defences will have effects on both predator success rate and handling time. For these defences, the predator’s functional response should be decreased over the whole range of prey densities.

Prey swarming: which predators become confused and why?

When confronted with a swarm of their prey, many predators become confused and are less successful in their attacks. Despite the general notion that this confusion effect is a major reason for prey swarm formation, it is largely unknown how widespread it is and which predator or prey traits facilitate or impede it. We carried out experiments with four predator–prey systems: Aeshna and Chaoborus larvae, but not Libellula and Triturus larvae, became confused when confronted with high Daphnia densities. When combining this result with literature data, we found that predators became confused in 16 of the 25 predator–prey systems studied to date. Tactile predators appear to be generally susceptible, whereas visual predators are susceptible mainly when their prey is highly agile. This difference probably results from the superiority of the visual sensory system. However, while our study is an important step towards the mechanistic understanding of predator confusion, it also reveals how poor this understanding currently is.

A “crown of thorns” is an inducible defense that protects Daphnia against an ancient predator

Genetic data has become an essential part of ecological studies, because the analyses of diversity within and among natural populations may grant access to previously overlooked ecological and evolutionary causalities, especially among cryptic species. Here, we present an example of how phylogenetic analysis of molecular data obtained within a DNA barcoding study, in combination with morphological and ecological data from the field and laboratory experiments, unraveled a striking predator-prey interaction between aquatic organisms. The “crown of thorns,” a conspicuous morphological feature among water fleas of the Daphnia atkinsoni species complex (Crustacea: Cladocera), is considered to represent a species-specific trait. However, our study, initiated by the analysis of sequence variation in 2 mitochondrial genes, shows that this feature is phenotypically plastic and is induced by chemical cues released by Triops cancriformis, the tadpole shrimp (Notostraca). The trait acts as an effective antipredator defense, and is found in several Daphnia lineages coexisting with notostracans. These facts suggest that the “crown of thorns” evolved in coexistence with this ancient predator group.

Chaoborus crystallinus predation on Daphnia pulex: can induced morphological changes balance effects of body size on vulnerability?

Juvenile Daphnia pulex form neckteeth in reponse to chemicals released by predatory Chaoborus crystallinus larvae. Formation of neckteeth is strongest in the second instar followed by the third instar, whereas only small neckteeth are found in the first and fourth instar of experimental clones. Predation experiments showed that body-size-dependent vulnerability of animals without neckteeth to fourth instar C. crystallinus larvae matched the pattern of neckteeth formation over the four juvenile instars. Predation experiments on D. pulex of the same clone with neckteeth showed that vulnerability to C. crystallinus predation is reduced, and that the induced protection is correlated with the degree of neckteeth formation. The pattern of neckteeth formation in successive instars is probably adaptive, and it can be concluded that neckteeth are formed to different degrees in successive instars as an evolutionary compromise to balance prediation risk and protective costs.

Genome-wide analysis of tandem repeats in Daphnia pulex - a comparative approach

BackgroundDNA tandem repeats (TRs) are not just popular molecular markers, but are also important genomic elements from an evolutionary and functional perspective. For various genomes, the densities of short TR types were shown to differ strongly among different taxa and genomic regions. In this study we analysed the TR characteristics in the genomes of Daphnia pulex and 11 other eukaryotic species. Characteristics of TRs in different genomic regions and among different strands are compared in details for D. pulex and the two model insects Apis mellifera and Drosophila melanogaster.ResultsProfound differences in TR characteristics were found among all 12 genomes compared in this study. In D. pulex, the genomic density of TRs was low compared to the arthropod species D. melanogaster and A. mellifera. For these three species, very few common features in repeat type usage, density distribution, and length characteristics were observed in the genomes and in different genomic regions. In introns and coding regions an unexpectedly high strandedness was observed for several repeat motifs. In D. pulex, the density of TRs was highest in introns, a rare feature in animals. In coding regions, the density of TRs with unit sizes 7-50 bp were more than three times as high as for 1-6 bp repeats.ConclusionsTRs in the genome of D. pulex show several notable features, which distinguish it from the other genomes. Altogether, the highly non-random distribution of TRs among genomes, genomic regions and even among different DNA-stands raises many questions concerning their functional and evolutionary importance. The high density of TRs with a unit size longer than 6 bp found in non-coding and coding regions underpins the importance to include longer TR units in comparative analyses.