Technical Comments

Population Cycles and Parasitism

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Science  24 Dec 1999:
Vol. 286, Issue 5449, pp. 2425
DOI: 10.1126/science.286.5449.2425a

Hudson et al. (1) used anthelmintics to reduce worm burdens in cyclic red grouse (Lagopus lagopus scoticus) managed for shooting, and claimed to have stopped population cycles. Their study may be an important demonstration that wildlife diseases can have a strong impact on host dynamics (2), but the statement that “these results show that parasites were both sufficient and necessary in causing cycles in these populations” (1) seems unwarranted, for two reasons.

First, Hudson et al. based their interpretation on large reductions in the amplitude of the 1989 and 1993 declines in grouse numbers in response to treatment, but their measure of grouse numbers was the number of birds shot, not the population size. Indices of population size such as sequential hunting or trapping statistics invariably overestimate the variance in population size when compared to direct counts (3). Hudson et al. compared numbers of grouse shot with numbers actually counted in one control area and showed that variance in the former was at least tenfold larger than in the latter. No attempt was made to shoot birds in 1989 and 1993 in five out of six untreated control populations (4). If the increased variance caused by the sampling process (shooting) is taken into account, it can be inferred that at least 100 birds per square kilometer were present on the control areas in 1989 and 1993. Further, gamekeepers knew the treatment allocations because they were the people treating grouse with anthelmintics, and this could have significantly biased the shooting effort. Thus, there are insufficient data to accurately estimate differences in cycle amplitude between control and treated areas.

Second, despite Hudson et al.'s claim that cycles were stopped, cyclic fluctuations took place on treated areas where parasitism was reduced. Cycle amplitude varies greatly in red grouse populations (as in other species) with cyclic dynamics (5). Parasite dynamics is thought to be dominated by rainfall—which affects the survival of free-living parasite larvae (6)—in drier parts of Scotland, where low amplitude cycles with periods of up to 10 years take place and where parasites are thought not to cause cycles (6, 7). Thus, observing a reduction in cycle amplitude in response to anthelmintics while retaining cyclic dynamics is entirely consistent with hypotheses relating cyclic dynamics to processes other than parasitism (7). Hudson et al. have provided evidence for reduced fluctuations as a consequence of anthelmintic treatment, but the evidence for a change in fluctuation pattern is equivocal.


Response: Lambin et al. state that we should have used sample counts, not bag records, for our analysis. Their main concern is that the variance in bag records is large at low grouse densities. However, our data show that a decrease in variance only occurred when grouse densities were relatively high, greater than 110 birds per square kilometer (1). Underlying this result is a strong relation between bag records and sample counts that is only slightly confounded by the variance in bag records. In detail, the count data from our main study population show that the variance of the counts fell with the mean grouse density. In other words, at low density there was more variation between counts than at high density because grouse were not evenly distributed across the habitat, but aggregated. At high density, the grouse used all the available habitat and are more evenly distributed.

While we agree that total counts of the whole population would have been useful, this approach would not have been practical. Sample counts would have been less representative than bag records. Moreover, because our description of the population cycles in red grouse (like other cyclic species) is based on indirect estimates of density, we needed to show that our manipulations influenced these indices.

Their second point is that while our manipulations reduced the amplitude of the cyclic fluctuations, there was a residual cycle that could have been caused by some other mechanism. This was predicted from our original model, so the application of Occam's Razor tells us that there is no reason to invoke another mechanism. Based on the preponderance of experimental and monitoring evidence currently available, it is clear that parasites play a dominant role in causing red grouse population cycles (2). In an earlier review of our report, May (3) said of our large-scale experiments that “important ecological questions simply have to be addressed on the right scale—which often means an uncomfortable large scale—even if that means a certain degree of imprecision.” We believe that this is a fair appraisal and helps to address the concerns of Lambin et al.


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