Parasites as predators: unifying natural enemy ecology

doi:10.1016/j.tree.2008.06.015

Trends in Ecology & Evolution

Volume 23, Issue 11, November 2008, Pages 610-618

https://doi.org/10.1016/j.tree.2008.06.015 Get rights and content

Parasitism and predation have long been considered analogous interactions. Yet by and large, ecologists continue to study parasite–host and predator–prey ecology separately. Here we discuss strengths and shortcomings of the parasite-as-predator analogy and its potential to provide new insights into both fields. Developments in predator–prey ecology, such as temporal risk allocation and associational resistance, can drive new hypotheses for parasite–host systems. Concepts developed in parasite–host ecology, such as threshold host densities and phylodynamics, might provide new ideas for predator–prey ecology. Topics such as trait-mediated indirect effects and enemy-mediated facilitation provide opportunities for the two fields to work together. We suggest that greater unification of predator–prey and parasite–host ecology would foster advances in both fields.

Introduction

Since Anderson and May’s seminal models of parasite–host dynamics [1], the analogy of parasites as predators has provided fundamental insights for the emerging field of parasite–host ecology [2]. Anderson and May drew upon the rich predator–prey literature to derive basic models of parasite–host dynamics [1]. These models have been useful for understanding many parasite–host systems 3, 4, 5, attesting to the value of predator–prey theory as a source of insights into parasite–host ecology. Before then, parasitology and ecology were treated largely as separate areas of inquiry, with parasitologists emphasizing description of species and life cycles and ecologists emphasizing organismal interactions at macroscopic scales. In the last three decades, however, the field of parasite–host ecology has grown in prominence, recently approaching the number of predator–prey publications in 13 top ecological journals (Figure 1). In spite of increased usage of the parasite-as-predator analogy (Box 1) and of the more general term ‘natural enemy’ 6, 7, 8, 9, 10, the two fields remain largely separate. In cases where the parasite-as-predator analogy is valid, predator–prey ecology should have much to offer the nascent field of parasite–host ecology. Likewise, parasite–host ecology should also have concepts to offer predator–prey ecology.

In this paper, we evaluate the parasite-as-predator analogy by discussing the characteristics of parasites that make them similar to and different from predators. We also evaluate the implications of these differences, and we discuss whether and how key concepts developed for predation have been used in the development of hypotheses for parasitism. We then explore new ways that the analogy could be used to derive hypotheses for both fields. We conclude by summarizing the implications and limitations of the parasite-as-predator analogy and calling for greater integration of predator–prey and parasite–host ecology into the more general framework of natural enemy ecology.

Section snippets

Are parasites predators?

Parasitism is sometimes conceptualized as a special case of predation 1, 2, but not all parasites fit the classic definition of a predator. Classically, predation is defined as an interaction in which one organism consumes either all or part of another living organism (the prey), causing a direct negative effect on the prey [11]. Parasitism is a symbiosis in which one organism, the parasite, causes harm to another, the host, which the parasite utilizes as habitat and depends on for resource

Using predator–prey ecology to generate new hypotheses for parasite–host ecology

Despite the successful application of the parasite-as-predator analogy to many questions in parasite–host systems (Box 1), important concepts remain that can provide new and potentially useful hypotheses.

Turning the analogy around: parasites inform predator–prey ecology

Despite being a younger field, parasite–host ecology can offer insights into predator–prey ecology. First, parasite ecologists often focus on controlling disease outbreaks by reducing susceptible host population density to a level below which parasites cannot persist [62]. Resource managers can use this threshold host density as a guide to cull or vaccinate hosts. There have been many successful applications of this theory to controlling and preventing disease outbreaks 63, 64, despite evidence

Conclusions and synthesis

Parasitism is not a specialized form of predation. Rather, parasites and predators are overlapping categories of natural enemies, with fundamental differences arising from the close physical relationship of parasites with their hosts and the consumption of host tissue by predators (Box 2). Thus far, the parasite-as-predator analogy has served both fields well (Box 1). Many concepts from predator–prey ecology, such as hypotheses describing prey responses to temporal variation in predation risk,

Acknowledgements

We thank Bob Holt and an anonymous reviewer for helpful comments. This work was supported by a National Science Foundation grant (DEB 0516227) and a US Department of Agriculture grant (NRI 2006–01370).

Glossary

Acquired immune system: the portion of the vertebrate immune system which responds to novel parasites via directed cell mutation followed by selection for responsiveness to parasite molecules.
Amensalism: interaction in which one organism causes a negative effect on another without being positively or negatively affected in return.
Aposematism: evolution of distinctive warning signals by resistant (often toxic) prey species to discourage predation.
Apparent competition: indirect negative effect of one

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Trends in Ecology & Evolution

ReviewParasites as predators: unifying natural enemy ecology

Introduction

Section snippets

Are parasites predators?

Using predator–prey ecology to generate new hypotheses for parasite–host ecology

Turning the analogy around: parasites inform predator–prey ecology

Conclusions and synthesis

Acknowledgements

Glossary

Trends Ecol. Evol.

Trends Ecol. Evol.

Trends Ecol. Evol.

Ecol. Complex.

Adv. Stud. Behav.

Trends Ecol. Evol.

Trends Ecol. Evol.

Trends Ecol. Evol.

Int. J. Parasitol.

Theor. Popul. Biol.

Trends Ecol. Evol.

Trends Ecol. Evol.

Trends Ecol. Evol.

Trends Ecol. Evol.

Neurosci. Biobehav. Rev.

Regulation and stability of host-parasite population interactions: I. Regulatory processes

J. Anim. Ecol.

Is infectious disease just another type of predator-prey interaction?

Population dynamics of fox rabies in Europe

Nature

Prevention of population cycles by parasite removal

Science

The ecological consequences of shared natural enemies

Annu. Rev. Ecol. Syst.

Extending the principles of community ecology to address the epidemiology of host-pathogen systems

How parasites affect interactions between competitors and predators

Ecol. Lett.

On the role of enemies in divergence and diversification of prey: a review and synthesis

Can. J. Zool.

Ecology: From Individuals to Ecosystems

Parasitism: The Ecology and Evolution of Intimate Interactions

Parasites in food webs: the ultimate missing links

Ecol. Lett.

Seasonality and the dynamics of infectious diseases

Ecol. Lett.

Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging?

Parasitology

Negative effects of changing temperature on amphibian immunity under field conditions

Funct. Ecol.

Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs

Philos. Trans. R. Soc. Lond. B Biol. Sci.

Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis

Am. Nat.

The dynamic nature of antipredator behavior: prey fish integrate threat-sensitive antipredator responses within background levels of predation risk

Behav. Ecol. Sociobiol.

Coping with crowds: density-dependent disease resistance in desert locusts

Proc. Natl. Acad. Sci. U. S. A.

A review of trait-mediated indirect interactions in ecological communities

Ecology

Predation: Direct and Indirect Impacts on Aquatic Communities

Scared to death? The effects of intimidation and consumption in predator-prey interactions

Ecology

The behavior of parasitized animals

Bioscience

Review
Parasites as predators: unifying natural enemy ecology