Certified Natural

Indicators of Bio-Diversity – field audit system 

Prepared by: A Davis, C Scholtz, P Dooley, N Bham & Ute Kryger

Scarabaeine dung beetles as indicators of biodiversity, habitat transformation and livestock treatment effects in agro-ecosystems

Adrian L.V. Davis¹, Clarke H. Scholtz¹, Peter Dooley², Naeem Bham³ & Ute Kryger¹

¹ Dept of Zoology & Entomology, University of Pretoria, Lynnwood Rd, Pretoria, 0002 South Africa

² The Natural Products Group, P.O. Box 8538, Eden Glen, 1613 South Africa

³ Novartis South Africa, Animal Health, P.O. Box 92, Isando, 1600 South Africa

Abstract

As integral members of pasture ecosystems in warmer climates, scarabaeine dung beetles are useful as bioindicators for maintaining high biodiversity in untransformed pastoral regions (high species richness) and for maintaining pasture health (large populations, high dung burial) in both untransformed and intensively farmed regions. We outline the use of dung beetles variously as biodiversity, ecological or environmental indicators at each of three spatial scales, regional, local, and pasture. At regional scale, analyses of differences in species richness and distribution are useful both for determining regional boundaries, thus defining limits within which local comparisons are valid, and for defining differences in biogeographical composition of local faunas. At local scale, differences in species assemblage structure are useful for characterizing differences between natural and transformed habitats both for certification and marketing of meat produced under natural conditions, and for conservation issues. At pasture scale, differences in species assemblage structure between dung containing pesticide residues and that lacking residues are useful both for screening old and new avermectin or synthetic pyrethroid products for relative toxicity, and for developing more environmentally-friendly pest control practices. At each of the three scales, we list stated goals, provide an overview of approach and past results, and make proposals for future research.

Introduction

Indicators for environmental conservation in agro-ecosystems have received a great deal of recent attention. Despite extensive discussion in a special issue of Agriculture, Ecosystems & Environment (2001, volume 87, number 2), an acceptable universal framework for their application is still lacking. This is due to various degrees of incompatibility between different systems (Riley 2001), which were designed for a multiplicity of differing applications at different spatial and temporal scales. However, despite this lack of uniformity, the use of indicators remains desirable as a basis for management decisions in agro-ecosystems. In the present publication, we describe and review several applications of scarabaeine dung beetles as agricultural indicators. One application is in defining natural biogeographical regions and faunal

distribution centres to facilitate or validate structural comparisons between local species assemblages in

natural and intensively farmed systems (an already established approach). A second application is for a

characterization of pasturage from natural to heterogeneous to totally transformed, in terms of dung beetles, for use in marketing of natural meat products produced under certified natural conditions (a new development by The Natural Products Group (Pty) Ltd, South Africa according to a registered and copyrighted protocol). A third application is to promote the development of environmentally friendly pest control practices in livestock farming from natural to relatively intensive systems by bioassay, i.e. by examining the relative toxicity of dung residues of different products at different concentrations to beneficial non-target fauna (scarabaeine dung beetles) under different conditions in the field and laboratory (an already established approach).

In a review of terrestrial insects as bioindicators, McGeoch (1998) has made recommendations for determining the suitability of a selected insect group for any intended application. These have been proposed as a nine-step protocol, which may be reduced to three principal criteria. The first criterion is the category (biodiversity, ecological or environmental) and scale (regional or local) of indication. The second is the specific objectives of the application without which null hypotheses cannot be developed. The third is the data collection and rigorous statistical testing of the group to ensure that it is suitably sensitive to fulfill the study objectives and permit well-supported decision-making.

Scarabaeine dung beetles are an obvious choice for indicators in the present application as they are an integral part of livestock pasture ecology in the warmer, moister climatic regions in which they are centred, i.e. within the 45^o latitudinal limits in areas receiving >250 mm annual rainfall and subject to >15^o C mean annual temperature (Halffter 1991, Davis & Scholtz 2001, Davis et al. 2002). Their principal importance lies in the maintenance of pasture health as a result of their dung burying habits. Dung burial has the effect of removing wastes from the surface, recycling the contained nutrients, and reducing exposure of livestock to contained parasites (Waterhouse 1974). Problems with pasture health in Australia before the introduction of dung beetles adapted to cattle dung, included the loss of grass cover due to persistence of unburied pads, the development of rank unpalatable grass growth around these pads, the leaching of nutrients in surface rain water runoff, and the build-up of large populations of fly pests (Bornemissza 1976).

There are a number of further advantages of scarabaeine dung beetles as pasture indicators (Davis 2002). During a long evolutionary history dominated by ecological specialization to dung (Davis et al. 2002), they have developed specialized associations with particular regional and local environmental conditions at a fine-grained spatial scale owing to their relatively small body size. In particular, clear associations are shown with climatic regions (Kirk & Ridsdill Smith 1986, Davis & Dewhurst 1993, Davis 1997, Allsopp 1995) and with soil, vegetation and dung types (e.g. Nealis 1977, Cambefort 1982, Doube 1983, 1991, Davis 1994, 1996a). As members of the ground fauna, these associations are related to environmental variables (Davis et al. in press) rather than to chemical or taxonomic composition of vegetation as in many plant-associated insects (e.g. Meurer-Grimes & Tavakilian 1997). Although association with particular environmental factors may not be synonymous with usefulness as bioindicators, McGeoch et al. (2002) have already demonstrated that dung beetles do have a good capacity as ecological indicators of environmental differences or of habitat change. Furthermore, their alpha taxonomy is fairly advanced and easy methods exist for quantitative collection of field data using dung-baited pitfall traps (Davis 2002).

In the present publication, the application of dung beetles as indicators for the classification and characterization of natural systems is a necessary starting point in order to assess the effects of the historical trend from natural to agro-ecosystems. However, the narrative is essentially aimed at conservation applications in agro-ecosystems. The stated goals may be summarized as the maintenance of a natural system in relatively unmodified situations and the maintenance of pasture health in both natural and intensively farmed situations. We give a brief overview of some relevant literature with the intention of identifying gaps in available data and refining methodological approaches for attaining the stated goals. We also suggest the future direction of activities based on the stated goals and the selected methods. For spatial studies, we variously use all three categories of indication suggested by McGeoch (1998) (biodiversity, ecological, environmental) at three scales of activity (regional, local, and individual pasture). At a temporal scale, studies may be only 24-48 h in duration to detect spatial differences between regions and habitats or similar repeated over a longer term to detect suspected ecological changes or to chart the effects of known environmental transformation.

Indicators of effects related to regional dominance of climatic, edaphic or vegetative characteristics

Stated goals

1)      The determination of regional differences in biodiversity, taxonomic composition, and species abundance structure (these are usually related to climatic factors although edaphic and vegetative characteristics may also vary at regional scale, e.g. rain forests, winter rainfall shrublands, sandy deserts, with edaphic factors independent of climate and vegetative factors dependent on climate).

2)      The determination of natural regional boundaries for defining the spatial limits within which valid and meaningful species abundance comparisons may be made between local species assemblages from natural to transformed habitats.

3)      The determination of geographical distribution centres defined in terms of dung beetle species group distribution.

4)      The division of local species assemblages into geographical groups (derived from 3) in order to define their proportional biogeographical composition, thus facilitating comparison between assemblages unlimited by spatial boundaries.

Overview

There is a limited body of work on dung beetle biodiversity. Several studies (Cambefort 1991, Davis et al. 2002) examine the global distribution of the 14 tribes and subtribes and 235 genera listed by Hanski & Cambefort (1991), but this is data-limited to a continental scale. An alternative approach makes a global-level comparison of 46 widely separated, local faunas (Davis et al. 2002), which does provide some insight into sub-continental patterns. However, there are relatively few detailed studies on biodiversity, major distribution centres, and endemism of scarabaeine dung beetles at sub-continental scale (e.g. Lumaret 1979, Kirk & Ridsdill Smith 1986, Davis & Dewhurst 1993, Allsopp 1995, Lumaret & Lobo 1996, Davis 1997). In most regions, it is difficult to execute such studies due to the many taxonomic errors in museum reference collections, the inexactitude of many locality labels, the absence of collation of reliable distribution data, and the patchy nature of collections. Few surveys have been conducted systematically or exhaustively across regions or entire species ranges. Even the extensive CSIRO reference collection of Southern and East African dung beetles (collected over 15 yr during the programme to introduce dung beetles into Australia – Bornemissza 1979) is suitable only for defining major sub-continental regions, and is insufficient for spatial resolution at a smaller scale (Davis 1997, Koch et al 2000).

There have been extensive environmental changes during the period over which existing museum reference collections were constructed. Climatic and soil type boundaries will have remained largely stable but vegetation type physiognomy and indigenous mammal ranges have been altered radically. In general, distribution data do not distinguish between collections made in natural or transformed habitats nor do they usually specify the dung type, as this information is rarely recorded on locality labels. Thus, data reflect the distributions of taxa collected on unknown dung types and at different temporal stages of the trend from natural to fragmented to totally transformed, since history and extent of change varies from region to region. Although there has been widespread range restriction in indigenous megaherbivores, the dung of domestic stock, particularly cattle and sheep, remain widespread. Therefore, the widespread changes in vegetative physiognomy are of principal importance to baseline data on dung beetles in agro-ecosystems. In general, there are two possible extremes in population response to habitat fragmentation (e.g. Roslin & Koivunen 2001). Strict specialists undergo range reduction with metapopulation formation or even extinction. Generalists or moderate specialists with higher vagility and greater ecological flexibility may colonize all suitable remaining or newly created habitat patches. In moderately fragmented regions, mixed data from natural and transformed localities may be adequately separated using multivariate analysis to provide a good assessment of natural or fragmentation induced distribution patterns. For example, in an analysis of dung beetle distribution in Southern Africa, Davis (1997) showed that many coarse dung specialists were characterized by a fragmented distribution in game reserves where large, indigenous, non-ruminant mammals and their coarse-fibred droppings are still abundant. In the same analysis, some species of the group with the most widespread distributions may occur unnaturally in the Western Cape where they are most abundant in pastures (Davis 1993) cleared of the once regionally dominant natural shrubland. However, this occurrence is marginal in terms of the species group distribution centre in the moister eastern part of the summer rainfall region (Davis 1997).

Of three principal approaches used for defining regional biodiversity patterns in scarabaeine dung beetles, the two most useful for application in agro-ecosystems are the definition of geographical regions and species distribution centres. Studies of range size and relative endemism (Allsopp 1999, Lumaret & Lobo 1996) are more useful for conservation issues. The geographical region-centred approach defines discrete regions by identifying boundaries between local faunas using turnover (beta diversity), nestedness/lack of nestedness and/or similarity/dissimilarity coefficients. These approaches are reviewed by Williams (1996) and are used in dung beetle studies by Lumaret (1979), Martín-Piera et al. (1992), Allsopp (1995), Jay Robert et al (1997), Davis et al. (1999), and Lobo & Halffter (2000). A, perhaps, more realistic taxon centred approach defines overlapping species group distribution centres using similarity coefficients and clustering or ordination, possibly, with mapping of cluster distributions (Kirk & Ridsdill Smith 1986, Davis & Dewhurst 1993, Davis 1997, Davis et al 1999, Davis et al 2002). It is not useful to discuss the relative merits of the two approaches, as both are useful in different applications. The geographical region approach may be used to define the boundaries of natural regions within the agro-ecosystem in order to define the limits within which direct comparisons of species abundance composition are valid. The taxon centred approach may define the distributional centres of species groups permitting a standardized comparison between the proportional biogeographical compositions of any local assemblages independent of spatial limits, i.e. within the area studied for defining distribution centres. These methods have been used to good effect to define biogeographical patterns in the southern African fauna (Davis 1997, 2002) where distributions are centred primarily on climatic regions or in transition zones (Davis 1997). Numbers of species range from 64 in the cooler drier southwest to 386 in the warmer moister northeast climatic regions (Davis 2002 – probably underestimated) with similar patterns shown by species richness of local assemblages (12-33 in the southwest, 77-113 in the northeast). On the east coast, there are clear differences in proportional biogeographical composition between assemblages of transformed (dominated by east coastal endemics and widespread taxa) and natural habitats (dominated by localized Maputaland and east coastal endemics) (Davis et al. 2002) and well-defined biogeographical boundaries across the eastern mountain escarpment within which local assemblages also have clearly different biogeographical compositions (Davis et al. 1999).

Suggested future direction of research

1)      There is a need to improve the accuracy of identifications in existing reference collections so that further distribution data may be extracted and collated. This database may then be used to define major regional centres and regional limits in the many areas for which this knowledge is presently lacking. Figure 1 shows that, at present, distribution centres or regional dung beetle faunas are only defined for Southern and East Africa, Australia, Iberia, Southern France, and the Mexican transition zone, with endemism patterns described in the Mediterranean basin for Southern Europe and North Africa (Lumaret & Lobo 1996).

2)      There is a need to expand existing databases to improve the spatial resolution, definition and accuracy of biogeographical analyses. This subdivision of major regions to a finer-grained scale may only be achieved through the systematic collection of more detailed distribution data (see Lumaret (1979); a fine grained biogeographical analysis of southern France using dung beetle data from 731 sites defines 25 biogeographical subregions).

3)      It may be useful to design surveys according to flora-defined regions. In South Africa, exploratory surveys in five out of 14 floral subregions of the highveld grassland biome (Low & Rebelo 1996) showed differences in dung beetle species richness across rainfall and altitude regimes (Table 1), and distinct differences in species abundance structure in a series of different natural and transformed habitats from the moister east to the drier west (Fig. 2). It would clearly be useful to conduct full subregional surveys within all major regions.

Indicators of effects related to local transformation from natural habitat to agro-ecosystem

Stated goals

1)      Conservation of biodiversity and pasture health through maintenance of a natural environment or a heterogeneous environment with sufficiently large natural fragments remaining to support specialists and to maximize species richness and diversity.

2)      A within-farm characterization of habitats from natural to disturbed to improved pasture to feed lots in terms of dung beetles.

3)      A between-farm characterization of natural versus transformed habitats in terms of dung beetles.

4)      Certification of farms with a high proportion of natural grass and high indigenous dung beetle diversity as “natural” for natural products marketing.

5)      Random selection or nomination of specific farms for testing with optional random repeats to maintain standards.

Overview

In many warmer regions, there is a well-advanced trend (Pimm 2001) towards transformation from entirely naturally vegetated, through a heterogeneous mosaic of natural and transformed patches, to entirely modified as an agro-ecosystem. Such a trend is accompanied by changes in the dung beetle fauna. One might predict that the extent of the change would depend on the magnitude of physiognomic / microclimatic differences to those of the original vegetative cover. However, in terms of species richness and abundance, there are some conflicting results from the relatively few conservation-orientated, habitat fragmentation studies on dung beetles that examine the effects of converting natural vegetation to agro-ecosystem pasture (Table 1). These conflicts probably result from the balance between species loss versus species gain through immigration, and the differing local population dynamics within each resulting species assemblage. Species gain is greater where the transformed habitat both lies physically close and has become ecologically closer to those in adjacent ecosystems. Thus, in the examples of forest transformation to clear cuts or pasture (Table 1), there is a great loss of shade specialists from the extensive Neotropical forests (Klein 1989, Halffter et al. 1992, Medina et al. 2002), whereas in the South African coastal forests, there is a net loss of shade specialists but these are replaced by a large number of non-shade specialists from the adjacent inland savanna ecosystem (Davis et al. 2002). However, in all cases, there is relatively low similarity in species abundance between forest and transformed unshaded habitats (Table 1) compared to the higher similarity between forest patches (e.g. in South Africa: species composition = 57.9-67.9% similarity, species abundance composition = 71.8-82.7% (Davis et al. in press)). In winter rainfall shrublands of South Africa, there has been extensive transformation (Davis 1993, Heijnis et al. 1999) to arable lands and pastures. Whereas shrubland localities retain the characteristic winter rainfall biota, pasture dung beetle faunas comprise both sizeable proportions of mostly autumn / spring active taxa of the winter rainfall region and mostly summer active taxa derived from the adjacent summer rainfall system (Davis 1993). As a result, data from open shrubland and nearby pastures show little difference in species richness values, mostly moderate similarity in species composition but mostly low species abundance similarity (Table 1). The high similarity between natural and transformed habitats in West Coast National Park may result from the fact that the pasture was an island of sparse cover within the natural shrubland. In the highveld grasslands of South Africa where sources for highland immigrants are lacking, there was marked species loss, low to moderate similarity in species composition and moderate similarity in species abundance between natural and improved pastures in a highly transformed region of KwaZulu-Natal (Table 1, Davis et al. 1999).

If transformed pastures are ranked according to the physiognomy of the former natural vegetation (from forest to grassland), there does appear to be a general increase in similarity between assemblages in terms of species abundance (Table 1). Transformation from forest to pasture results in significant changes in various microclimatic factors including increased radiant heat, ambient temperature, light intensity and reduced humidity and also changes in proportional surface cover (Davis et al. 2002). Less visible changes may be partly responsible for the faunal differences that also occur between natural and improved pastures. Changes in density of surface cover would influence surface and soil temperatures, and the retention of soil moisture. Soil moisture content is known to be an important factor for larval survival (Osberg et al. 1994, Sowig 1995). It is unknown how differences between past and present dung types have influenced results in Table 1.

With an increasing trend to intensive farming methods and a decline in food quality, there has been a counter trend towards natural production methods. In the case of meat production, natural methods comprise grazing only on grassland pastures with an absence or limitation of supplementary dry feed and a ban on chemical treatments for growth enhancement. In order to market certified “natural meat”, dung beetles are being used to characterize natural versus transformed conditions, with particular emphasis on natural grassland systems which have survived agro-ecosystem trends to extreme pasture improvement or feed lot development. Because of possible species immigration problems, the indicator methods need to be selected according to the circumstances pertaining to each region. We provide some exploratory examples from natural and transformed patches in the summer rainfall grasslands on the highveld of South Africa where species immigration is not a problem but relative modification of vegetative physiognomy is potentially limited. Comparison of dung beetle species abundance structure for different vegetation types and treatments on four highveld farms (Fig. 3) shows no consistent differences between grassland types and feeding treatments at Balfour; consistent differences between faunas isolated within a mosaic of arable and pasture fragments at Viljoenskroon; fairly consistent separation between natural and transformed pastures at Carolina; and no effect of pasture treatment on the cooler, moister highveld but a consistent effect on the warmer, drier middle veld in a region near Ladysmith dominated by natural grassland. On Foggy Valley near Carolina, there are clear differences in species richness between the mosaic of patches comprising 80% natural Themeda-dominated grassland, 10% fallow pastures previously disturbed by ploughing, and 10% improved pastures of Kikuyu grass (Table 3). One species in particular, Sisyphus alveatus, showed much greater mean abundance (12.73 / trap) in natural grassland than in disturbed (0.10 / trap) or Kikuyu pastures (0.27 / trap). Several others including the uncommon, Scarabaeus caffer, occurred in low abundance only in natural grassland. Further monitoring of the Foggy Valley dung beetle assemblages was conducted for six months after environmental changes to three of the nine study sites in late 2001. Comparison between pre- and post change faunas shows similarities above 60% at four unchanged sites and similarities well below 60% at five sites which included all three modified sites (Table 4). At Foggy Valley, results for species richness, in particular, suggest that partial improvement of pastures would not be detrimental to species richness as long as sizeable fragments of natural grassland are retained. However, interpolation of nature reserves would assist in conserving biodiversity within agro-ecosystems.

Suggested future direction of research

1)      Owing to the largely positive results obtained during preliminary trials, it is proposed to proceed with the use of dung beetles to characterize farms by ranking local within region species richness (where workable such as in highveld grassland where immigrants are absent) and comparing species abundance structure. This will permit a within subregion assessment ranked from “good” to “not so good” in order to certify the more diverse farms with high proportions of natural grassland as “natural” in terms of a registered protocol for marketing meat of high quality produced under natural conditions.

2)      In order to provide data for this assessment, it is proposed to determine the proportions of natural versus transformed habitats on each farm, and to conduct a within farm ranking of these habitats in terms of dung beetles.

3)      As Davis et al (1999) have used high proportional composition of endemics as an indicator of system naturalness; it may be useful to use relative endemism as an additional indicator for certification purposes.

4)      Results from Foggy Valley suggest that individual species may also be useful indicators of naturalness and these may be assessed using the IndVal method described by McGeoch (2002).

5)      In order to standardize results, trapping should be conducted during the season to which dung beetle activity is maximized (December and January in the mid-summer rainfall region of South Africa – Davis 1996b), preferably soon after rainfall when activity and species richness are maximal (Davis 1995).

Indicators of effects of modern pest control agents for livestock in pastures on beneficial non-target fauna

Stated goals

1)      To maintain healthy pastures with high scarabaeine dung beetle species richness, population levels and dung burial.

2)      To conduct both field and laboratory bioassay using dung beetles as indicators to determine the effects of residues voided in dung after treatment with untested older products and newer products developed to improve pest knockdown and counter resistance problems.

3)      To recommend usage of the pesticides least toxic to beneficial, non-target fauna in dung.

4)      To develop environmentally friendly pest treatment practices for both older and newer products.

Overview

In modern agro-ecosystems, parasites of livestock are commonly controlled using compounds with pesticidal properties, particularly the bio-synthesized avermectins (Ikeda & Omura 1997) or the chemically processed synthetic pyrethroids. The various synthetic pyrethroids are used extensively for the control of ectoparasites (Srivastava et al. 1993, Franc & Cadiergues 1994, Kok et al. 1996) and are administered as pour-ons. The various avermectins are used extensively both for control of ectoparasites (Muniz et al. 1995, Losson et al. 1996, Holste et al. 1997, Miller et al. 1997) and endoparasites (Logan et al. 1996, Flocklay & Deroover 1997), and are administered variously as pour-ons, ingestibles or injectables. The increasing international use of such methods in the 1980’s led to fears of widespread non-target faunal loss and environmental degradation (Wall & Strong 1987). Thus, the wider effect of residues from these treatments is the subject of much past and ongoing research. One major field of study concerns the effect on the beneficial dung beetle fauna of residues voided in dung. To date, tests on the relative toxicity of synthetic pyrethroid in dung (Bianchin et al. 1998, Krüger et al. 1998, 1999) have been fewer than the broad spectrum of tests conducted on the avermectins using both scarabaeine and aphodiine dung beetles as indicators (e.g. Ridsdill Smith 1988, Wardaugh & Rodriguez-Menendez 1988, Wardaugh & Mahon 1991, Halley et al. 1993, Ridsdill-Smith et al. 1993, Strong et al. 1993, 1996, McCracken & Foster 1993, Sommer et al. 1993a, b, Strong & Wall 1994, Krüger & Scholtz 1997, 1998a, b, Floate 1998, Dadour et al. 1999).

The limited number of bioassay studies using scarabaeine dung beetles may be conveniently divided into those conducted in the field and those conducted in the laboratory (Table 5). Field studies have examined the effects of dung containing residues versus controls lacking residues on relative abundances of dung beetle assemblages (Holter et al. 1993, Lumaret et al. 1993, Floate 1998) or those of single species (Wardaugh et al. 1993, Dadour et al. 1999), and have examined changes in assemblage structure (Krüger & Scholtz 1998a, b) both in the short term and the longer term up to one year. Field studies have also focused on the relative amounts of burial from dung pads containing residues versus those without residues (Krüger et al. 1998), Dadour et al. 1999. In selected species, laboratory studies have tested the relative post-treatment duration of toxicity to adults of different concentrations of different products indicated by proportional mortality (Bianchin et al. 1998, Krüger et al. 1999). Laboratory studies have also tested the effects of toxicity on relative breeding success and larval survival in selected species (Sommer & Nielson 1992, Fincher & Wang 1992, Krüger & Scholtz 1997).

            There are conflicting results between modeling and empirical studies on the field responses of dung beetles to pesticide treatment of livestock. Modeling of the toxic effects on dung beetles of avermectin treatment of cattle suggests that there will be field mortality but that this will rarely be greater than 25% in any given season (Sheratt et al. 1998). However, conflicting results between the limited published data in nine empirical field studies examining the effects of injected avermectins and two examining the effects of synthetic pyrethroids provide little direct evidence for strong detrimental influences of pesticide residues on scarabaeine dung beetles in pastures (Table 5). Whereas reduced diversity and increased dominance was shown in a dung beetle assemblage under drought conditions (Krüger & Scholtz 1998a), there was no difference in diversity between pads containing residues and those lacking residues during the rainy season (Krüger & Scholtz 1998b). Only one study has shown a reduction in beetle abundance (Dadour et al. 1999). Most show no reduction (Holter et al. 1993, Krüger et al. 1998) or record an increased degree of attraction to dung containing residues (Wardaugh & Mahon 1991, Holter et al. 1993, Lumaret et al. 1993). Similarly, only one study shows a reduction in dung burial (Dadour et al. 1999) with most showing no reduction (Halley et al. 1993, Sommer et al. 1993a, b, Krüger et al. 1998).

            There is a somewhat more consistent but less encouraging body of data concerning the responses of scarabaeine dung beetles to pesticide residues in 13 laboratory studies on avermectins (mostly injected into cattle) and two on synthetic pyrethroids. Most studies, except those on moxidectin, showed sublethal or lethal toxic effects to adult dung beetles for a variable post treatment period, with most avermectins also toxic to immatures (Table 5). At recommended dosage rates for livestock, dung was highly toxic for the first few days following treatment (Wardaugh et al. 1993, Sommer et al. 1993a), usually remaining so for the first week (Sommer & Nielson 1992, Dadour et al. 1999), and sometimes for longer periods up to 14 days (Krüger & Scholtz 1997, Wardaugh et al. 2001) but usually diminishing to low levels after the first one to two weeks (Sommer et al. 1993a, Lumaret et al. 1993) although these effects may persist for up to 42 (Dadour et al. 2000) or 56 days (Ridsdill Smith 1988). Most avermectins were lethal to newly emerged adults (Wardaugh & Rodriguez-Menendez 1988, Wardaugh et al. 1993, Dadour et al. 2000) whereas synthetic pyrethroids were also lethal to older adults (Bianchin et al. 1998, Krüger et al. 1999). Except for moxidectin (Fincher & Wang 1992, Wardaugh et al 2001), avermectin products also caused breeding suppression (Wardaugh & Rodriguez-Menendez 1988, Houlding et al 1991, Dadour et al 2000) or mortality of immature stages developing in post-treatment dung (Ridsdill Smith 1988, Sommer et al 1993a, b, Krüger & Scholtz 1997, Dadour et al 2000, Wardaugh et al 2001). Other recorded effects of avermectins include feeding suppression (Wardaugh & Rodriguez-Menendez 1988) and increase in development time of immatures (Lumaret et al. 1993, Krüger & Scholtz 1997). However, the limited tests on synthetic pyrethroids have found no effect on larval mortality and only one instance of breeding suppression at seven days after treatment with flumethrin (Krüger et al. 1999).

            Several different methods of pesticide application are in current use, pour-ons, subcutaneous injection, or injestible sustained-release bolus. There have been only a limited number of tests on the differing effects of application method on non-target fauna. Ivermectin residues released after application by pour-ons were found to be lower than those released after injection, although both reduced the numbers of aphodiine larvae in dung voided 1-2 days after treatment with no effect in dung released 13-14 days after treatment (Sommer et al. 1992). However, sustained-release boluses of ivermectin show a much longer period of toxicity, peaking at 63 days, inhibiting development of larval aphodiines for around 100 to 130 days, and still reducing larval numbers for around 140 days (Errouissi et al. 2001). Clearly, this latter method is, potentially, the least environmentally friendly to scarabaeines.

In conclusion, the various avermectins and synthetic pyrethroids show both differences in action and relative toxicity to adult or immature dung beetles with clear results for toxicity in the laboratory and more equivocal results from the field. Except for moxidectin, there seems to be no overall advantage to using either avermectins or synthetic pyrethroids to reduce non-target effects on dung beetles. Although limited laboratory work indicates that synthetic pyrethroids are mostly non-toxic to immatures, they are lethal to adults in general in the immediate post-treatment period. In comparison, most avermectins are lethal to both new adults and immatures with sublethal effects on older adults. These differences may be related to differences in their chemistry and rates of degradation but little work seems to have been conducted on this aspect of residues. Although there seems to be little difference between the rapid degradation in water by both avermectins (substantial photo-degradation in less than one day – Halley et al. 1993) and synthetic pyrethroids (substantial degradation within 24 h – Agnihotri et al. 1986), longer persistence is observed in a soil/faeces mixture, where it takes 7-14 days for substantial aerobic degradation of ivermectin (Halley et al. 1993). Moxidectin is the least toxic of any treatment but appears to be less toxic overall, which may compromise its selection as a pesticide. Ranking of various avermectins according to their toxicity to fly larvae in dung yielded a result from greater toxicity in doramectin to ivermectin to eprinomectin to least in moxidectin (Floate et al. 2001). Comparison of two avermectins showed that ivermectin did not kill adult aphodiines but suppressed their breeding for seven days whereas moxidectin did not kill nor prevent breeding of aphodiines (Strong & Wall 1994). Finally, Doherty et al (1994) showed that to achieve similar larval mortality of Digitonthophagus gazella resulting from the recommended dosage of abamectin, it was necessary to use a concentration of moxidectin that was 64 times greater.

Suggested future direction of research

1)      There is a need for further laboratory bioassay using standardized methods in order to facilitate comparison. Bioassay should be used both to screen newer products and to compare the relative toxicity of all existing products as a gauge of their likely environmental friendliness. In particular, laboratory results need to be standardized by using the same dung beetle species for bioassay since some species are more susceptible to toxic residues in dung than others (Sommer et al 1993b).

2)      In view of the between-species differences in susceptibility to toxic residues, possible local effects in different regions may be better gauged by conducting laboratory bioassay on suites of different species selected on the basis of their suspected or known substantial contribution to local dung burial. Three criteria should be addressed according to their relevance to dung burial in each instance: (1) numerical dominants, both of smaller or larger body size; (2) different functional groups, either ball rollers or tunnelers; (3) dominants of large body size that play a disproportionate role in dung removal compared to their abundance

3)      Considering the toxic effect of dung residuals in laboratory studies, one would predict some detectable deleterious response in field populations of dung beetles. However, so far, this has been demonstrated in only few studies examining entire assemblages, individual species and/or dung burial (Krüger & Scholtz 1998a, Dadour et al. 1999). Since predicting possible responses of dung beetles to residues in pastures is the ultimate raison d’etre for all studies, further field-monitoring remains a necessary approach. However, it remains difficult to standardize field studies due to the unpredictability of the many spatial and temporal factors that influence results, which may lead to inconsistencies and difficulties in interpretation. However, a few observations may be made in order to strengthen future experimental designs. Measurement of relative attractiveness of treated vs. untreated dung over the short-term is not a good gauge of possible population responses to residuals over the long-term. Longer-term studies are better. However, trap placement needs careful consideration as spatial variability influences results both on a macroscale (habitat differences, particularly soil and vegetation type) and a microscale (local edaphic, surface cover and microclimatic variability, particularly in undulating country). Immigration/emigration effects, partly related to wind direction and emigration from surrounding dung concentrations, or from the study area, obscure the local effects one is measuring. Thus, is the recorded variation due to habitat variability, immigration/emigration or treatment responses? Changes in species composition and abundance over a temporal scale may also be difficult to interpret in the short term due to daily weather effects and in the long term due to weather and seasonal effects. Dung beetle activity is maximized to warm wet conditions. There is a decline in both species richness and abundance during cooler and/or drier day-to-day (Davis 1995) or seasonal conditions (Davis 1996b). Thus, is the recorded variability due to weather and seasonal effects or treatment responses? Clearly, a statistical treatment is required to assess the relative contribution of spatial, temporal and between-treatment variance to results.

4)      There is a need to test if pesticide treatment practices could be made more environmentally friendly by application when dung beetle activity is relatively low, prior to, or after peaks in seasonal activity (Krüger & Scholtz 1997), or during dryer periods (Davis 1995). Clearly, it is necessary to monitor the effects of different methods of application, particularly sustained-release boluses, which result in highly toxic dung residues over the long term (Errouissi et al. 2001).

Conclusions

1)      Owing to the rapid loss of natural habitats and continuing environmental degradation, there is a need to achieve a balance between faunal and floral conservation, and sustainable, economically viable productivity in agro-ecosystems. In livestock farming, there is a choice between quality production on conserved natural pastures versus intensive production of quantity in grain feed lots perhaps with the use of growth enhancers. There is also a choice between ignoring pasture health or promoting it by improving pest treatments so that they are more environmentally friendly to beneficial, non-target fauna.

2)      Indicators are required for characterizing natural versus transformed and environmentally detrimental versus environmentally friendly. Dung beetles are good indicators of biodiversity and environmental quality in agro-ecosystems at a range of spatial and temporal scales owing to:

a)       their specialization to different regional climatic and ecological conditions.

b)       their specialization to existing local edaphic and physiognomic conditions and their sensitivity to changes in these conditions.

c)      their integral role in pasture ecology, which makes them useful for bioassay of the relative toxicity of livestock treatments in pastures.

Acknowledgements

We thank The Natural Products Group and Novartis South Africa, Animal Health, for research funding. Christiaan Deschodt, Craig Tambling, James Roxburgh, James Campbell, Wendy Holtzhausen, and Riaan Maartens provided technical assistance. We also acknowledge the efforts of the many workers who have contributed to the body of cited literature.

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