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Oecologia (1992) 90:417-421 Oecologia Springer-Verlag 1992 Predator: non-predator ratios in beetle assemblages Kevin J. Gaston 1, Philip H. Warren 2, and Peter M. Hammond 1 1 Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK 2 Department of Animal and Plant Sciences, PO Box 601, The University of Sheffield, Sheffield S10 2UQ, UK Received November 7, 1991 / Accepted in revised form January 22, 1992 Summary. In common with samples from less taxonom- ically constrained studies, significant correlations exist between the numbers of predatory and non-predatory species in assemblages of terrestrial beetles. Under log- arithmic transformation the relationship can be de- scribed reasonably well by a straight line. Explanations for predator: non-predator relationships based on the dynamics of trophic interactions (e.g. competition for prey types or enemy-free space) seem insufficient to ex- plain this pattern, because within beetle assemblages the necessary interactions are so few. Of other proposed determinants, those based on the relationship of local and regional species pools, on energetics, or on non- trophic factors seem the most plausible candidates for explaining proportionality amongst beetles. Much of the deviation from the overall pattern can be accounted for by sampling method and latitude. Temperate samples have a higher proportion of predatory species than tropi- cal, whilst litter and pitfall trap samples have higher proportions of predatory species than Malaise trap and fogging samples. Key words: Coleoptera Predator-prey ratios- Trophic structure It seems now firmly established that an underlying regu- larity exists in the relative numbers of predatory and non-predatory (often termed 'prey') species in com- munities (e.g. Evans and Murdoch 1968; Cohen 1977; Moran and Southwood 1982; Briand and Cohen 1984; Jeffries and Lawton 1985; Stork 1987; Lockwood et al. 1990). However, whilst it is clear that the number of predator species is approximately proportional to the number of prey species, the detailed form of the interac- tion remains uncertain. Moreover, although several mechanisms have been proposed to explain the pattern (e.g. Cole 1980; Jeffries and Lawton 1984, 1985; Mithen and Lawton 1986), much work remains to be done to Correspondence to: K.J. Gaston distinguish satisfactorily between their effects and estab- lish their relative importance. A great deal could yet be learned through documentation of the occurrence and form of relationships between numbers of predatory and non-predatory species. To date, study of relationships between numbers of predatory and non-predatory species has been largely limited either to taxonomically relatively unconstrained samples of communities, or at least to the bulk of meta- zoan organisms within them. Nonetheless, there are hints that similar patterns exist within substantially more lim- ited assemblages (e.g. Arnold 1972; Faaborg 1985). In this paper we seek to determine whether regularities occur in the relative numbers of species of predators and non-predators in terrestrial beetle assemblages. Beetles are a significantly more varied and speciose taxon than those of previous studies. The occurrence of relationships here may have profound implications for the further development of theory to explain such patterns. The data Data on numbers of predatory and non-predatory species were collated for a wide variety of samples of terrestrial beetle assem- blages. The bulk of these samples [the exceptions being those of Stork (1987 and pers. comm.)] derive from studies carried out by one of the authors (PMH; see Hanski and Hammond 1986; Ham- mond 1990a; Purvis and Hammond 1990; and unpublished), who also sorted and classifiedthe species in these cases. In each instance, the predator class includes species with predatory larvae in which adults either take little food or feed on other materials, and also par- asitoids. The latter category rarely accounts for more than 1% of total beetle species in a sample. For full explanation of how trophic group assignations were made see Hammond (1990a). In general, the accuracy of sorting to trophic groups, depending as it does on an imperfect knowledge of the species biologies, is unlikely to better 90% on average. For predators, however, relatively few errors are likely, especially in temperate samples. Samples represent a wide variety of sampling methods (e.g. Malaise, flight intercept, pitfall and yellow pan traps, insecticidal fogging, litter sampling), habitats (e.g. oak, beech and mixed wood- land, tropical moist forest), micro-habitats (e.g. tree canopies, litter) and climatic regions (temperate, tropical). No standardisation was possible with regard to the duration or extent of each sample. For

Predator: non-predator ratios in beetle assemblages

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Oecologia (1992) 90:417-421 Oecologia �9 Springer-Verlag 1992

Predator: non-predator ratios in beetle assemblages Kevin J. Gaston 1, Philip H. Warren 2, and Peter M. Hammond 1

1 Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK 2 Department of Animal and Plant Sciences, PO Box 601, The University of Sheffield, Sheffield S10 2UQ, UK

Received November 7, 1991 / Accepted in revised form January 22, 1992

Summary. In common with samples from less taxonom- ically constrained studies, significant correlations exist between the numbers of predatory and non-predatory species in assemblages of terrestrial beetles. Under log- arithmic transformation the relationship can be de- scribed reasonably well by a straight line. Explanations for predator: non-predator relationships based on the dynamics of trophic interactions (e.g. competition for prey types or enemy-free space) seem insufficient to ex- plain this pattern, because within beetle assemblages the necessary interactions are so few. Of other proposed determinants, those based on the relationship of local and regional species pools, on energetics, or on non- trophic factors seem the most plausible candidates for explaining proportionali ty amongst beetles. Much of the deviation from the overall pattern can be accounted for by sampling method and latitude. Temperate samples have a higher proport ion of predatory species than tropi- cal, whilst litter and pitfall trap samples have higher proportions of predatory species than Malaise trap and fogging samples.

Key words: Coleoptera Predator-prey r a t i o s - Trophic structure

It seems now firmly established that an underlying regu- larity exists in the relative numbers of predatory and non-predatory (often termed 'prey') species in com- munities (e.g. Evans and Murdoch 1968; Cohen 1977; Moran and Southwood 1982; Briand and Cohen 1984; Jeffries and Lawton 1985; Stork 1987; Lockwood et al. 1990). However, whilst it is clear that the number of predator species is approximately proportional to the number of prey species, the detailed form of the interac- tion remains uncertain. Moreover, although several mechanisms have been proposed to explain the pattern (e.g. Cole 1980; Jeffries and Lawton 1984, 1985; Mithen and Lawton 1986), much work remains to be done to

Correspondence to: K.J. Gaston

distinguish satisfactorily between their effects and estab- lish their relative importance. A great deal could yet be learned through documentation of the occurrence and form of relationships between numbers of predatory and non-predatory species.

To date, study of relationships between numbers of predatory and non-predatory species has been largely limited either to taxonomically relatively unconstrained samples of communities, or at least to the bulk of meta- zoan organisms within them. Nonetheless, there are hints that similar patterns exist within substantially more lim- ited assemblages (e.g. Arnold 1972; Faaborg 1985). In this paper we seek to determine whether regularities occur in the relative numbers of species of predators and non-predators in terrestrial beetle assemblages. Beetles are a significantly more varied and speciose taxon than those of previous studies. The occurrence of relationships here may have profound implications for the further development of theory to explain such patterns.

The data

Data on numbers of predatory and non-predatory species were collated for a wide variety of samples of terrestrial beetle assem- blages. The bulk of these samples [the exceptions being those of Stork (1987 and pers. comm.)] derive from studies carried out by one of the authors (PMH; see Hanski and Hammond 1986; Ham- mond 1990a; Purvis and Hammond 1990; and unpublished), who also sorted and classified the species in these cases. In each instance, the predator class includes species with predatory larvae in which adults either take little food or feed on other materials, and also par- asitoids. The latter category rarely accounts for more than 1% of total beetle species in a sample. For full explanation of how trophic group assignations were made see Hammond (1990a). In general, the accuracy of sorting to trophic groups, depending as it does on an imperfect knowledge of the species biologies, is unlikely to better 90% on average. For predators, however, relatively few errors are likely, especially in temperate samples.

Samples represent a wide variety of sampling methods (e.g. Malaise, flight intercept, pitfall and yellow pan traps, insecticidal fogging, litter sampling), habitats (e.g. oak, beech and mixed wood- land, tropical moist forest), micro-habitats (e.g. tree canopies, litter) and climatic regions (temperate, tropical). No standardisation was possible with regard to the duration or extent of each sample. For

418

example, trap catches might represent few or many weeks of trap- ping with one or several traps, and fogging catches may be for one or more trees. In some instances it was possible to combine several samples, produced from the same sampling method in the same area, to generate a number of "summary" data points.

In addition to samples from local assemblages, numbers of '~ 6 predatory and non-predatory species of beetles were determined o. from species lists for several substantially larger regions, Richmond w Park (1000 ha) in Britain (PMH unpub.), Mulu National Park ~ 5 (544 km 2) in Sarawak (Hanski and Hammond 1986; PMH unpub.), O Hammond's (1990a) study region in Dumoga-Bone National Park (500 ha), N. Sulawesi, and the whole of the British Isles (313, ~ 4 650 kmZ; PMH unpub.), e~

It is important to note that although there are many observa- tions, most derive from just a few studies at specific locations in o 3 which only some (sometimes only one) of the possible sampling methods were used. Comparisons of sampling methods and regions Z g 2 are thus confounded by non-independence. Interpretation of signifi- -- cance levels should be accordingly circumspect.

Results

General patterns

The numbers of predatory species are strongly correlated with the numbers of non-predatory species (under log- arithmic transformation to correct skew toward small samples; Fig. 1, r=0.742, n = 156, P<0.001) . The data can be described reasonably well by a straight line rela- tionship, in which the slope of the reduced major axis (Ricker 1973; McArdle 1988) is 0.66 (Fig. 1). There is little evidence of marked non-linearity in the plot of the raw data, but at low sample sizes, an upward spread of data points is evident (Fig. 1). These upwardly spread points come from a single location (location 1, Burnham Beeches) sampled predominantly, though not entirely, by a single method (pitfall traps). This emphasises the prob- lem of confounding methods and studies. Due to its strong influence we have analysed the data both with and without this study. The slope of the relationship with the study removed is 0.895 (r=0.813, n = 110 P<0.001) .

The summary data points have not been included in calculating slopes, as they are cumulative lists including data from other samples on the graph. The fit o f the summary data to the relationship will not therefore be examined quantitatively. Nonetheless, it is clear f rom Fig. 1 that they fit the overall relationship quite well. Numbers of species for the regional assemblages also apparently lie on the same line (Fig. 1).

Region and sampling method

Of particular interest in understanding patterns in tro- phic structure is the comparison of tropical and tem- perate samples, and the effect of sampling method on the "apparent" structure of the community. Such analyses are frequently complicated by the variation in locality, latitude and sampling method. As almost all samples considered in the present study derive from moist forests (whether temperate or tropical) some of these problems are avoided. With appropriate caveats we can make some comparisons.

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Fig. 1. a Relationship between numbers of predatory and non- predatory species of beetles. Open symbols are temperate, closed ones tropical, and squares are summary or regional data points. The solid line in the reduced major axis for all the data and the dashed line for the data without location 1 ; in neither case were the sum- mary and regional points used in the calculations, b Relationship between numbers of predatory and non-predatory species of bee- ties, excluding summary and regional data points. Open triangles, pitfall traps; open squares, Malaise traps, open diamonds, litter samples ;filled triangles, flight intercept traps ;filled squares, fogging samples; filled diamonds, miscellaneous

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Fig. 2a,b. Plot of the magnitude of the mean deviation from the reduced major axis (Fig. 1), of tropical and temperate samples for each sampling method, a for all the data and b with location 1 removed, p, pitfall traps; m, Malaise traps; l, litter samples;

f flight intercept traps; o, fogging samples; i, miscellaneous. Bars are ~: 1 SD

It is clear from Fig. 1 that there is a strong tendency (even removing location 1) for temperate samples to contain a higher proportion of predators than tropical ones. If separate reduced major axes are fitted to tropical and temperate samples (with location 1 included) the slopes differ markedly (btemp =-0.687, btrop = 1.022), but if location 1 is removed the temperate slope becomes 0.99, remarkably similar to that for tropical data. As before, analysis of the pattern is complicated by the influence of sample method and location, but analysis of the perpen-

dicular deviations from the fitted relationship in Fig. 1 ("residuals") suggests that there may be significant effects of region and of sample method, but there is also a significant interaction between the two. This pattern of deviations with respect to region and sample method is summarised in Fig. 2, which plots the mean deviations from the fitted line of temperate and tropical samples by method. Two patterns are evident. First, there is a ten- dency for sampling methods to be consistent in the amount of predator/non-predator bias, e.g. litter sam- pling always seems to give more predator-biased results (i.e. positive deviations from the line), and fogging the most non-predator biased. Second, there is also an over- all tendency for temperate samples to be more predator- biased than tropical samples, i.e. to lie below the 1:1 relationship in Fig. 2. The data for each region separately indicate a significant effect of sample method on devia- tion from the fitted line either including location 1 (ANOVA Temperate - method: F=20.37, df=5,92, P<0.0001, location: F=l .31 , df=12,92, P>0.05; Trop ica l - method: F=3.14, df=5,37, P<0.05, loca- tion: F--1.23, df= 2,37, P>0.05) or excluding it (ANO- VA Temperate - method: F=95.5, df= 1,52, P<0.001, location: F = 0.77, df= 8,52, P > 0.05; Tropical - method: F = 9.67, df= 5,37, P < 0.001, location: F = 0.20, df= 2,37, P > 0.05).

Discussion

The strong relationships between numbers of predatory and non-predatory species in assemblages of beetles are similar to those found in studies across more disparate taxa (e.g. Jeffries and Lawton 1985). Any mechanism purporting to explain relationships between numbers of predatory and non-predatory species must account for the fact that such relationships appear to exist in a group in which the direct trophic interaction of the species is minimal. On the whole predatory beetles do not feed on non-predatory beetles, for most species their food in- cludes, and often consists entirely of, organisms other than beetles: other insects (especially larval Diptera, Homoptera and Collembola), other arthropods (espe- cially Acari) and various other invertebrates (espe- cially Nematoda) (see Hammond 1990b). Beetles may of course simply compose so substantial or such a represen- tative part of terrestrial communities that they reflect the trophic interactions of the community as a whole. If not, then the mechanisms proposed to account for propor- tionality in broader assemblages need to be considered.

A variety of mechanisms have been suggested as ex- planations of general patterns of proportionality in predator and prey species numbers. These are the ran- dom draw (local assemblages comprise species drawn at random from a regional pool; Cole 1980), prey niches (more prey types provide more niches for predators), enemy-free space (the number of prey coexisting with a predator is limited by apparent competition; Jeffries and Lawton 1984, 1985), energy ratios (richness is propor- tional to available energy at each trophic level; Warren and Gaston ms), and common determinants of diversity

420

(factors influencing diversity act similarly upon predators and prey; Warren and Gaston ms). These mechanisms and the general evidence for them are reviewed elsewhere (Warren and Gaston ms). They are undoubtedly very difficult to distinguish, tending to reinforce one another rather than being mutually exclusive. However, explana- tions based on local assemblages being random draws of regional species pools, on energetics, or on non-trophic factors which operate across trophic groups (common determinants), seem the most plausible candidates for explaining proportionality amongst the beetles. The scar- city of direct interactions between the predatory and non-predatory components of the beetle assemblages discussed here, clearly call into question explanations based on the dynamics of trophic interactions (i.e. com- petition for prey types or enemy-free space; Jeffries and Lawton 1984, 1985; Mithen and Lawton 1986).

Whatever the explanation for the overall pattern, it seems that much of the deviation from the overall trend can be accounted for by sampling method and latitude. The existence of an effect of sampling method upon observed ratios of predatory to non-predatory species comes as no particular surprise, but it is not clear to what extent these differences represent biases due to methodol- ogy as such, or real features of the different microhabitats sampled by each technique. The results from "standing crop" methods such as litter and soil sampling indicate the strong influence that habitat may have. For example, some 50 % of beetle species in litter samples from lowland tropical forest in Sulawesi were classed as predators by Hammond (1990a) as compared with 29% of species in the total beetle samples from this forest. Much of the same surface fauna as found in litter samples is sampled by pitfall traps, and the high proportions of predators collected in pitfalls would suggest that a habitat factor operates here too; however, as with other activity-based trapping methods pitfall trap samples are biased in other ways (see discussion in Hammond 1990a). On the other hand, differences between Malaise and flight intercept trap catches, although both types of trap intercept flying insects, can largely be explained by examining the nature of the sampling technique. Malaise traps intercept insects that fly upwards or land and climb when they meet a barrier (these are mostly plant-associated species), while intercept traps that work on a "hit and fall" basis, collect a much higher proportion of non-plant associated spe- cies, especially those foraging for resources such as car- rion, dung or other decaying material.

Effects that are from habitat rather than method raise an interesting set of questions about the mechanisms of trophic structuring. In particular, do the predator/non- predator differences in species richness reflect ecological (or evolutionary) responses to patterns of energy flow or availability in different habitats? Data on the corres- ponding habitat-specific variation in other trophic groups (e.g. scavengers, fungivores) would be of much value here. If nothing else, the results echo the establish- ed caution about apparent differences in community structure when these are based on different sampling approaches.

At a broader scale, Brinck (1948) has argued that the

proportions of regional beetle faunas consisting of car- nivorous and phytophagous species, as indicated by selected groups, show latitudinal trends, carnivorous spe- cies accounting for a steadily smaller proportion of the fauna from high northern latitudes, through the tropics and into the southern hemisphere. In contrast, the phyto- phagous portion of the fauna increases from high north- ern latitudes to the equator, does not decrease in the southern hemisphere, and possibly increases in the ex- treme south. Carnivore/phytophage ratios (not equiv- alent to predator: non-predator in excluding, for exam- ple, scavengers and fungivores), thus steadily decrease from extreme northern to extreme southern latitudes. Brinck's (1948) data are largely for islands and incom- plete species lists, but though he cautions that these may affect his results, he still believes them to reflect genuine patterns.

It is hard to evaluate Brinck's (1948) ideas, because it is difficult to relate the groups selected to complete beetle faunas. We find higher proportions of predatory species in samples from temperate regions (exclusively northern) than from tropical ones, suggesting that latitudinal gra- dients may indeed exist. The relationship between these results (alpha diversities) and patterns in regional faunas is hard to establish without knowledge of species rates of turnover (beta diversities). Ratios of predatory to non- predatory species for different regions do, however, provide a further hint that tropical areas do have propor- tionately fewer predators [Britain 0.775 (3905 spp.), Richmond Park 0.827 (1056 spp.), Mulu, Sarawak 0.506 (3795 spp.), Toraut, Sulawesi 0.407 (6273 spp.)]. It is also interesting to note that, although beetles usually make up a substantial part of terrestrial arthropod communities, that proportion tends to vary from one region to another and from ecosystem to ecosystem. For example, Danks (1988) suggests that in North America the proportion of insect species that are beetles declines from mid to high latitudes. One interesting possibility is that if an increase in the proportion of non-beetle insect species with in- creasing latitude reflects a proportional increase in en- ergy flowing through the non-beetle part of the commun- ity, this could actually mean more potential energy avail- able to predatory beetles (i.e. proportionately more non- beetle insects to feed on) and an associated shift in preda- tor/non-predator balance within beetle assemblages with latitude, as the data here and elsewhere suggest. How- ever, this remains speculation which, like the other pat- terns discussed here, requires a good deal more data and experimental work to test.

Acknowledgements. A number of colleagues helped in obtaining sam- ples and particular thanks in this respect are due to Mr. M.J.D. Bren- dell, Prof. J.A. Owen, Dr. H. Read and Dr. N.E. Stork. Prof. J.H. Lawton, Dr. C.J.C. Rees, and Dr. N.E. Stork kindly comment- ed on the manuscript.

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