The Components of Predation as Revealed by a Study of Small-Mammal Predation of the European Pine Sawfly, by C. S. Holling (1959)

C. S. Holling proposes to create a comprehensive theory that breaks down predation into two basic components: 1) functional response, or change in number of prey consumed per predator as prey density rises; and 2) numerical response, or change in density of predators as prey density rises. The two main variables he considers are prey density and predator density.

Holling calls the calculation of rate of growth without considering limiting factors “whimsy.” He comments that several researchers (including Nicholson, of the 1934 paper we read on parasite-host dynamics) have focused too myopically on various aspects of predation, and states a need for a more general theory.

Approach: Holling combines field and laboratory experiments. His model system has the advantage that it avoids many complications. In the field, three small mammals prey on one cocooned insect in an even layer of pine needles, under a uniform canopy of pines. The three main predators are the masked shrew (Sorex), the short-tail shrew (Blarina), and the deer mouse (Peromyscus). In the laboratory, variables that are constant in the field could be varied to extend the scope of the results.

In the field, Holling and his associates sample and estimate mammal and cocoon numbers from areas of different prey densities caused by spraying viruses of differing concentrations. In the lab, they vary prey density and the amount and type of alternate food available. The number of prey eaten, in addition to the identity of each predator, can be determined from scrutinizing the marks on the opened cocoons.

Results for basic components: In Figure 1, the functional responses of the three predator species are plotted against prey density. As the density of prey rises, the number of cocoons opened increases in an “S” curve for each predator, which levels out at different densities. The rate of increase is greatest for Blarina, least for Peromyscus, and Sorex is between the two. Analysis of Peromyscus stomach contents in the field, as well as functional response in the lab, support these data.

Figure 3 plots numerical response, or predator density against prey density. Increasing prey density apparently has an effect on prey density for two species. Holling states that for these two species, Sorex and Peromyscus, he has demonstrated that predator density is a “response” to prey density, but as he does not mention any correlation calculations or p-values, we would be justified in remaining skeptical about whether a causal relationship has been established.

The effect of predator density is tested briefly. Different densities do not result in different functional responses, so predator density is not taken into account in the totals for Figure 4.

In Figure 4, Holling combines the functional and numerical “responses” for each species by multiplying them, converts them to percentages, and plots them against prey density. Each shows a peaked curve, which in Blarina only reflects the functional response, since it showed no numerical response.

Results of varying subsidiary components:

Figure 5 is an aesthetically pleasing 3-D graph, showing that one deer mouse does not eat as many cocooned saw flies when they are buried deeper in the sand as when they are buried shallower. Figure 6 shows that one deer mouse decreases its saw fly consumption less when dog biscuits (unpalatable) are available than when sunflower seeds (palatable) are available.

Discussion:

Figure 7 is a theoretical model showing regulation of prey by predators. A horizontal line marks the ranges in percent predation where the prey birth rate = prey death rate. He states that regulation happens “when there is a rise in percent predation over some range of prey densities and an effective birth-rate that can be matched at some density by mortality from predators.” In his rambling discussion, Holling considers various models that have been proposed for oscillations of animal populations. He mentions Nicholson and Bailey’s prediction that oscillations in host (prey) numbers will increase in amplitude, and suggests that small mammal predation (in Holling’s system) can damp oscillations in prey population through the functional and numerical responses.

Holling compares his results to other systems explaining predator-prey interactions, with emphasis on Errington’s concept of compensatory predation. He then postulates four major types of predation in Figure 8, based on combining four different functional response curves with three types of numerical response.

Questions:

1. What do you think of Holling’s use of the term “anthropocentric”? Do you think he is successful in making his focus more objective?

2. What is the main point of this paper? What has Holling actually said, other than that small mammals eat more food when more food is available until they are full, and also sometimes congregate where there is more food?

3. Is statistical analysis really completely absent from this paper?

4. Holling describes various oscillating populations at some length in his discussion, but none of his graphs show oscillations. Why?