Abstract

Trophic relationships, such as those between predator and prey or between pathogen and host, are key interactions linking species in ecological food webs. The structure of these links and their strengths have major consequences for the dynamics and stability of food webs. The existence and strength of particular trophic links has often been assessed using observational data on changes in species abundance through time. Here we show that very strong links can be completely missed by these kinds of analyses when changes in population abundance are accompanied by contemporaneous rapid evolution in the prey or host species. Experimental observations, in rotifer-alga and phage-bacteria chemostats, show that the predator or pathogen can exhibit large-amplitude cycles while the abundance of the prey or host remains essentially constant. We know that the species are tightly linked in these experimental microcosms, but without this knowledge, we would infer from observed patterns in abundance that the species are weakly or not at all linked. Mathematical modeling shows that this kind of cryptic dynamics occurs when there is rapid prey or host evolution for traits conferring defense against attack, and the cost of defense (in terms of tradeoffs with other fitness components) is low. Several predictions of the theory that we developed to explain the rotifer-alga experiments are confirmed in the phage-bacteria experiments, where bacterial evolution could be tracked. Modeling suggests that rapid evolution may also confound experimental approaches to measuring interaction strength, but it identifies certain experimental designs as being more robust against potential confounding by rapid evolution.

Highlights

  • Empirical and theoretical studies suggest that the structure and strength of trophic links have large influences on ecosystem attributes such as species diversity [1,2], the abundance and productivity of different trophic levels [3,4], and the stability and dynamical behavior of component populations (e.g., [5,6,7,8]).One of the principal methods for assessing the existence and strengths of trophic interactions is an analysis of temporal patterns of change in species abundances [9]; either natural variations in abundance or transient dynamics that occur following natural or experimental disturbances of a steady state

  • Time-series data on changes in species abundance are used to parameterize a multispecies dynamic model, whose parameters can be used to calculate the various summary measures of interaction strength [10]. This approach has some advantages over strictly experimental approaches, such as species removals: in principle, the interaction strengths between all species pairs in a community can be estimated with one experiment, and estimates of direct pairwise interaction strengths are not confounded by indirect effects [9]

  • We report here a phenomenon that we call ‘‘cryptic dynamics,’’ in which the strength or even the existence of a predator–prey trophic link is masked by evolutionary dynamics

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Summary

Introduction

Empirical and theoretical studies suggest that the structure and strength of trophic links have large influences on ecosystem attributes such as species diversity [1,2], the abundance and productivity of different trophic levels [3,4], and the stability and dynamical behavior of component populations (e.g., [5,6,7,8]).One of the principal methods for assessing the existence and strengths of trophic interactions is an analysis of temporal patterns of change in species abundances [9]; either natural variations in abundance or transient dynamics that occur following natural or experimental disturbances of a steady state. Time-series data on changes in species abundance (and possibly on environmental covariates) are used to parameterize a multispecies dynamic model, whose parameters can be used to calculate the various summary measures of interaction strength [10]. This approach has some advantages over strictly experimental approaches, such as species removals: in principle, the interaction strengths between all species pairs in a community can be estimated with one experiment (rather than requiring a comprehensive set of single-species removals), and estimates of direct pairwise interaction strengths are not confounded by indirect effects [9]. A variety of different methodologies have been used, they are all based on estimating the relationship between the abundance of one species and the rate of change in the abundance of a second, and using some summary measure of the strength of this relationship as the estimated interaction strength

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