Seasonal Abundance and Reproductive Output of the Dung Flies

Bulletin of Entomological Research (2008) 98, 397–403 doi:10.1017/S0007485308005713 Ó 2008 Cambridge University Press Printed in the United Kingdom First published online 25 February 2008

Seasonal abundance and reproductive output of the dung ﬂies Neomyia cornicina and N. viridescens (Diptera: Muscidae)

R. Wall *, E. Anderson and C.M. Lee School of Biological Sciences, University of Bristol, Woodland Road, Bristol, BS8 1UG, UK

Abstract

The seasonal abundance and reproductive output of two common, but little studied, dung-breeding flies, Neomyia cornicina and N. viridescens, were examined in artificial cow pats in pastures in southwest England in 2001 and 2004. In 2001, the numbers of both Neomyia species increased slowly over summer to show a sharp seasonal peak in late August and early September. There was no significant effect of mean temperature, mean relative humidity or dung water content on abundance or seasonally de-trended abundance. High levels of aggregation were seen between pats and, when present, greater numbers of N. cornicina emerged than N. viridescens. Neomyia cornicina was present in 13% of 240 artificial standardized pats put out in 2001, at a median of 19 adults per colonized pat; N. viridescens was present in 8% of artificial pats at a median of three adults per colonized pat. In 2004, N. cornicina emerged from 46% of the 94 artificial pats put out at a median of three adults per colonized pat, while N. viridescens emerged from only 12% of pats at a median of one adult per colonized pat. Flies were also collected in 2004, using sticky-traps and hand nets. Again, free-flying N. cornicina appeared to be more abundant in the field than N. viridescens; 162 N. cornicina were caught compared to 44 N. viridescens over the same sampling period. The size of each adult female was recorded and ovarian dissection was used to determine the numbers of eggs matured. Female N. viridescens were significantly larger than the N. cornicina and matured significantly higher numbers of eggs. Gravid N. viridescens matured a mean of 37.1 (+16.9) eggs, whereas gravid N. cornicina matured a mean of 28.8 (+13.2) eggs. The reasons why the larger, more fecund, N. viridescens adults are less abundant in the field or emerging from pats than N. cornicina are unknown. Further work is required to identify the nature and cause of the mortality experienced by the larvae of these species and the ecological differences and functional specialisation which allows co-existence to be maintained.

Keywords: cattle-dung, decomposition, Diptera, insect, mortality, Neomyia, oviposition

(Accepted 24 October 2007)

*Author for correspondence Fax: 00 44 (0)117 925 7374 E-mail: [email protected]

Downloaded from https://www.cambridge.org/core. University of Athens, on 23 Sep 2021 at 21:25:59, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0007485308005713 398 R. Wall et al.

Introduction species; egg-to-adult development for dung beetles may require several months, whereas the development of larval Dung is a rich resource. It can be highly abundant and flies may require only one to two weeks. During this period, relatively predictable in its occurrence compared with other larvae must also be able to survive high levels of predation patchily distributed resources, such as carrion, particularly within the pat. where large populations of grazing vertebrates are present. The dung-breeding flies Neomyia cornicina (Fabricius) and Herbivore dung is very similar to leaf litter in composition, N. viridescens (Robineau-Desvoidy) (Diptera: Muscidae) are consisting mainly of water and undigested plant material widespread and abundant in cattle pastures. Neomyia along with the products of metabolism, gut epithelial cells cornicina is widely distributed throughout the Holarctic, and a distinct array of micro-organisms (Marsh & Campling, Neotropical and Oriental regions, while N. viridescens is 1970; Greenham, 1972; Stevenson & Dindal, 1987; Aschen- thought to be restricted to the Palearctic. They can be seen born et al., 1989). As a result, the insect community that alighting on fresh droppings and are conspicuous iridescent inhabits this environment is particularly diverse, consisting green-coloured muscids, with a characteristic iridescent of as many as 400 species (Hanski, 1991; Skidmore, 1991). As frons and face. Adult females oviposit batches of eggs in well as high species diversity, the dung environment cavities near the surface of the pat and the egg batches of supports a large number of individuals. It has been several females may be aggregated in the same cavity estimated that a single cow can support an insect community (personal observation). Neomyia spp. are important compo- at least one fifth its own weight purely on the food left in its nents of the dung community but have also been used as faeces (Laurence, 1954) and an individual dung pat may indicator species in studies of the cow-dung invertebrate contain 1000 or more insect inhabitants (Laurence, 1954; community, since they are highly sensitive to the presence of Hanski, 1991). insecticide residues (Gover & Strong, 1995, 1996; Sommer The dung-colonizing insects play a particularly important et al., 2001; Iwasa et al., 2005; Lumaret et al., 2005). However, role in ecosystem function; the timely decay of plant and despite being abundant in the field and widely used in the animal remains is essential to the carbon and nitrogen cycles, laboratory, the basic ecology of these two species is not well soil fertility and the population dynamics of a wide diversity understood; N. viridescens in particular has been little of species at a range of trophic levels. The importance of studied. As a complicating factor, the nomenclature and these invertebrate colonizers in pat decomposition has been taxonomy of these species has been confused; the classic clearly demonstrated by exclusion experiments, where mesh study by Hammer (1941) in Denmark uses the name covers have been used to prevent colonization. Lumaret & Cryptolucillia caesarion. The name Orthellia caesarion has been Kadiri (1995) found that pats from which all insects were particularly widely employed (e.g. Stoffolano & Streams, excluded for one month, took 1.7 to 2.2 times longer to 1971) as has Orthellia cornicina (Wardhaugh & Rodriguez- completely disintegrate than uncovered pats. Holter (1979) Mendez, 1988). There is one report which uses the term also showed that selective exclusion of nocturnal colonizers, Orthellia viridis for flies collected in the south of France (Kirk, particularly Aphodius rufipes L., by covering pats overnight 1992). Whether the various Palearctic studies examined during the first week, resulted in only half of the only N. cornicina or did not differentiate N. cornicina from disappearance found in freely exposed pats. Exclusion of N. viridescens is unknown, but the latter is probable. The aim insects from cow pats for only two days following deposition of the present work, therefore, was to examine the seasonal resulted in a significant increase in the amount of dung that abundance and reproductive output of both N. cornicina and remained after 35 days (Lee & Wall, 2006a). Furthermore, N. viridescens in cow dung in pastures in southwest England several authors have shown that a range of insecticides and to attempt to identify possible ecological differences between anthelmintics administered to livestock and excreted in these two species. faeces may, under some circumstances, kill dung-colonizing insects and retard decomposition (Wall & Strong, 1987; Madsen et al., 1990; Sommer et al., 1992; Strong et al., 1996; Methods and materials Floate, 1998; Floate et al., 2005). Seasonal abundance While tropical dung communities dominated by dung- burying scarabaeid beetles can completely remove a dung The pattern of seasonal abundance was examined in an pat in a few hours (Anderson & Coe, 1974; Hanski, 1991), area of permanent grassland pasture on a farm located dung disappears much more slowly in temperate regions, approximately 20 km southwest of Bristol, UK. The pasture over periods of weeks or months, or even sometimes years used was grazed by a dairy herd of about 250 Holstein- given the occurrence of unfavourable winter or drought Friesian cows and a small number of sheep. The majority of conditions. This slower decomposition allows a complex the cattle were let out to pasture in mid-May and were community of insects to develop in and around the dropping rotated between contiguous fields until mid-October, when during its degradation. Even in temperate regions, however, they were brought back in for the winter. The cattle were not the successional changes in the dung usually make it treated with anthelmintics while maintained in the milking suitable for only one generation of most insects, so in- herd. dividuals must be able to disperse and colonize new pats Batches of ten artificially-constructed cow pats, formed during their life. Hence, selection pressures acting on adults from fresh dung, were placed out each week between the and larvae are very different. Adults must be highly mobile 21st May and 29th October 2001 to allow for insect and able to find new resource (dung) patches in which to lay colonization. When pats were required, fresh dung from eggs, while larvae do not disperse far, but must complete several cows was collected from the milking parlour during their growth before the dung is exhausted or no longer afternoon milking. This was thoroughly mixed to ensure suitable for their development. Clearly, these development uniform constituency and texture and used immediately. rates and selective pressure also vary with the colonising Using a hand-held spring balance, 1.5 kg of fresh dung was

weighed out and circular pats, 4–5 cm deep with a diameter 1000 of approximately 19 cm, were produced using a polythene former. The former was removed once the pat had been created. Plastic netting (2 cm mesh) was placed under the pats to assist with their recovery; the netting was not considered likely to have affected invertebrate movement, 100 given the size of the dung-colonising species relative to the mesh width. Samples of the dung used were brought back to the laboratory for analysis of their water content (Lee & Wall,

2006b). Throughout the study, daily temperature and Number humidity were recorded at the study site using an 10 automated weather station (DataHog, Skye Instruments Ltd, Llandrindod Wells, UK). Artificial pats were left exposed in the field for one week to allow colonization, following which they were retrieved. After collection, each pat was returned to the laboratory, 1 placed onto a thin layer of sawdust on a polythene sheet and 0 50 100 150 200 250 put in an individual fine-mesh bag, at approximately 20– Time (days) 25C, to await the emergence of invertebrate colonizers. The mouth of the mesh bag was attached to a plastic collecting Fig. 1. The numbers of Neomyia cornicina () and N. viridescens beaker and, as they emerged, insects were funnelled from (L), recovered from batches of ten artificial 1.5 kg cow pats the mesh bag into the beaker, where they quickly died. This placed out at weekly intervals at farm 1 in southwest England funnel system helped to ensure that there was no recoloniz- between May and November (day 1: 1st of May 2001). Zero ation of dung by newly-emerged insects in the laboratory. counts not shown. All insects to emerge were collected and counted; however, only the data for the adult Neomyia are presented here. Details of the other insects recovered from these pats are from July to September 2004. At each inspection, all green- given elsewhere (Lee & Wall, 2006b). coloured Diptera were removed and returned to the lab- All adult Neomyia to emerge were identified to species oratory where Neomyia were identified, sexed and counted level. The two Neomyia species were differentiated using the under a binocular microscope. chaetotaxy of the thorax; N. cornicina has two pairs of dorso- For each female collected in a hand-net or on the sticky- central and two single acrostichal bristles on the prescutum, target, its left wing was removed and mounted on a sheet of whereas N. viridescens has the pairs of dorso-central bristles paper using sticky-tape. The wing was then examined under only. a binocular microscope and the length of the posterior cross vein between the fourth and fifth longitudinal veins (dm-cu between veins CuA1 and M; McAlpine, 1981) was measured Comparison between farm types to give an index of size. Subsequently, the abdomen of each In 2004, Neomyia abundance was studied in two areas of female was detached from the thorax using a pair of dis- % permanent grassland pasture. The first site was the same as secting scissors and placed in Ringer’s solution (0.9 saline) was used in 2001 (farm 1), while the second was an organic on a glass microscope slide. Using mounted needles and beef farm located approximately 5 km north of Bristol (farm under a dissecting microscope, the ovaries were gently 2), and grazed by approximately 130 South Devon beef cattle removed from the abdomen and teased apart. Egg follicles over an area of 210 acres. In this year, batches of 1 kg cow within the ovaries were measured to the nearest 0.025 mm pats (approximately 15 cm in diameter) were formed each using an eye-piece graticule. The number of mature eggs was week from fresh dung as described above. Five pats were counted. placed out each week at each farm between the 28th of June and the 3rd of September. The artificial pats were left exposed in the field for 3–5 days to allow colonization, Results following which they were retrieved, returned to the Seasonal abundance and distribution laboratory and treated as described previously. A total of 1681 N. cornicina and 123 N. viridescens emerged successfully from the 240 artificial cow pats placed out Reproductive output in the field during the summer of 2001. Individuals of both Neomyia In 2004, at both farms, flies were collected at 3–5 day species first appeared in the cow pats placed out into the intervals using a hand-held net as they alighted on cow pats. field on day 56 (25th June), with low numbers (15 or less) in In addition, at farm 1, flies were trapped using 40-cm-sided each batch until those placed out between days 119 and 133 square white targets (Wall et al., 1992) covered by a (27th August–10th September), when they showed a sharp polybutene-based non-setting adhesive (Oecotak, Oecos Ltd, peak followed by a rapid decline (fig. 1). Multiple regression Kimpton UK). Each target was baited with 500 ml of fresh analysis found no significant effects of mean temperature, cow dung which was replaced weekly. Five targets were mean relative humidity or dung water content on either the placed vertically around the edges of the cattle pastures at log10 transformed abundance or the abundance data after it least 100 m apart with the support-pole pushed into the had been de-trended to remove the seasonal pattern. For the ground, so that the target base was approximately 30 cm later analysis, a third order polynomial regression was above ground level. Targets were inspected every 3–4 days plotted through the seasonal abundance data, and the

3.5 12 2001 3 10

2.5 8 2 6 1.5

Number of pats 4 1 Mean fly number (+1) 2 0.5

0 0 12 5 1015202530354045 50 55+ Site Number of adult flies per pat

Fig. 2. The detransformed mean log10 number (+1) of Neomyia 35 cornicina () and N. viridescens (L)(+detransformed 95% confidence intervals) recovered from batches of five artificial 30 1 kg cow pats placed out at weekly intervals at farms 1 and 2 in 2004 southwest England between June and September (day 1: 1st of May 2004). 25

residuals were then treated as the independent variable in 20 the multiple regression analysis. Neomyia cornicina was present in 31 pats (13%); and, 15 where it was present (excluding zero counts), a median of 19 Number of pats adults (interquartile range 54) emerged from each pat. 10 Although numbers were generally relatively low, for one pat placed out on day 126 (3rd September), 266 N. cornicina 5 were recovered from this pat alone (fig. 2). Neomyia viridescens was present in 18 pats (8%); and, where it was 0 present (excluding zero counts), a median of three adults 5 10152025303540 (interquartile range = 6) emerged from these pats (fig. 2). Number of adult flies per pat Both species were found together in only nine pats. Analysis of variance of the log10 (+1) transformed number of each Fig. 3. The number of pats from which adult Neomyia cornicina species showed that N. cornicina were significantly more (solid bars) and Neomyia viridescens (open bars) emerged in abundant than the N. viridescens (F = 15.2, P < 0.001). frequency classes of five, in 2001 (upper) and 2004 (lower). Of the 94 pats put out in 2004, N. cornicina emerged from 43 (46%). A median of three adults emerged from each pat (interquartile range = 5) and only six pats gave rise to more for small sample size) suggests that the incidence of co- than ten N. cornicina (fig. 2). Neomyia viridescens emerged occurrence was significantly greater than expected in 2001 from only 11 of the 94 pats (12%) and all of these gave rise to (x2 = 21.1, P < 0.001) but not in 2004. less than five adults, at a median of one adult per pat (interquartile range = 1) (fig. 2). Both species were found Reproductive output together in only five pats. Again, analysis of variance of the log10 transformed number of each species showed that there One hundred and thirty nine female N. cornicina were were significantly fewer N. viridescens than N. cornicina at caught by the traps and 23 by the hand-nets; 39 (28.1%) and both farms (F = 34.03, P < 0.001) but that the numbers of both 12 (52.2%) of these females contained mature eggs, respec- species were higher at the dairy farm than the organic beef tively. There were no differences in the size of the females or farm (F = 5.42, P = 0.02; fig. 3). There was no significant numbers of eggs they were maturing for females caught by interaction between farm type and Neomyia species (F = 2.87, the two capture methods, which were, therefore, pooled for P = 0.09). subsequent analysis. Overall, a mean of 28.8 (+13.2) eggs If oviposition by the two species had occurred at random were matured by the gravid female N. cornicina and larger in the available pats (240 in 2001 and 94 in 2004), the females matured significantly larger numbers of eggs probability of co-occurrence in each year can be calculated as (F = 17.25, P < 0.001; fig. 4). This relationship persists even if the product of the proportionate occurrence of each species the three largest females are removed from the analysis. multiplied by the number of pats available, which gives an A total of 27 N. viridescens were caught by the traps and expected co-occurrence in two pats in 2001 and five pats in 17 in the hand net. Of these, 11 in the trap were gravid 2004. This can be compared to the nine and five pats where (40.7%) as were 13 of those caught by the hand net (76.5%). co-occurrence was actually recorded in 2001 and 2004, There were no differences in the size of the females or respectively. Chi-squared analysis (with Yeats’ correction numbers of eggs they were maturing for females caught

90 10

80 9 8 70 7 60 6

50 5

40 Frequency 4

30 3

Number of mature eggs 2 20 1 10 0 0 5 101520253035404550556065707580 0.7 0.8 0.9 1 1.1 1.2 1.3 1.4 Number of mature eggs Size (mm) Fig 5. Distribution of egg batch sizes for Neomyia cornicina (open N. viridescens Fig 4. The numbers of eggs matured by adult female Neomyia bars) and (solid bars). cornicina of differing body size, where an index of size was measured as the length of the posterior cross vein between the fourth and fifth longitudinal veins (dm-cu between veins CuA1). from 13% and 46% of the pats, while N. viridescens emerged from only 8% and 12% of the pats deployed in 2001 and 2004, respectively. Since most insect larvae cannot disperse by the two methods, which were, therefore, pooled for between pats, their distribution and abundance is primarily subsequent analysis. Overall, a mean of 37.1 (+16.9) eggs determined by the oviposition behaviour of adults and were matured by gravid N. viridescens females, but there was the levels of mortality within the pat (Sowig, 1996). Females no significant relationship between female size and the of most insects deposit their eggs in clutches, and clutch number of eggs matured (F23 = 0.83, P < 0.37). size is a fundamental aspect of the life-history of each The female N. viridescens were significantly larger than species (Godfray & Parker, 1992; Withers et al., 1997). In the N. cornicina (F = 29.1, P < 0.001) and matured significantly patchy ephemeral habitats such as dung, the average patch higher numbers of eggs (F = 5.33, P = 0.02; fig. 5). quality, the probability of finding a suitable patch and the distance between patches influences the range of strategies that are successful (Beaver, 1977; Hanski, 1987; Withers et al., 1997; Thiel & Hoffmeister, 2004). Species Discussion breeding in rarer, less predictable but high quality habitat Despite the large number of studies that have been patches should typically deposit their eggs in large clutches; undertaken on the biology of components of the cow dung while smaller clutch sizes are expected where patches are colonizing invertebrate community, for many species little more frequent and predictable, or of lower quality (Godfray is still known. Adults of N. cornicina and N. viridescens are et al., 1991; Heard, 1998). Carrion breeding blowflies produce good examples of such common dung inhabitants, where relatively large clutches, of between 200 or more eggs information on their basic ecology and functional contribu- (Ives, 1991; Wall, 1993), resulting in high levels of aggre- tion to the decomposition process is lacking; indeed, the gation and severe competition (Holter, 1979; Ives, 1991). In literature would suggest that in many studies the two contrast, dung-breeding Diptera usually oviposit in much species are seldom differentiated. The present study, smaller clutches than carrion-breeding species, because however, has shown that there are a number of fundamental dung is a more predictable and abundant resource. The life-history differences, despite their superficial morpho- mean egg batch sizes for N. cornicina and N. viridescens were logical similarity. Adult females of N. viridescens are signifi- 29 and 37, respectively, which is similar to the egg batch cantly larger than N. cornicina and mature significantly larger sizes found in other dung-breeding flies, such as Scathophaga egg batches. A significant relationship between individual stercoraria L. (Hammer, 1941). female size and the numbers of eggs matured was found for The number of pats in which the two species co-occurred N. cornicina but not N. viridescens, although the latter may was higher than would have been expected by chance in simply reflect the relatively low sample size obtained for this 2001 but not in 2004. However, from these data, it is difficult species in 2004. It is also worth noting that eggs batches were to draw any clear conclusions about whether there was any measured from adult females of unknown age and oviposi- interaction between the two species in their distribution tion history in the field and that this is likely to have between pats. It may simply have been that in 2001 some accounted for a proportion of the variability seen in these pats were more suitable than others for oviposition, perhaps data. as a result of their location in the field. This issue requires Most dung-colonizing species are found in highly further, more detailed study. aggregated distributions, but the degree of aggregation Given the numbers of eggs matured by adult female may vary widely. In the present study, N. cornicina emerged Neomyia, the small numbers of each species generally

recovered from the pats is of considerable interest. In for permission to collect dung and use their farms as field particular, for N. viridescens, numbers were significantly sites. lower than those of N. cornicina, despite the larger clutch sizes of the former. The data suggest that high levels of References mortality may occur in the pats and that this mortality may be relatively higher for N. viridescens than for N. cornicina. Anderson, J.M. & Coe, M.J. (1974) Decomposition of elephant Why this should be the case remains to be determined. dung in an arid, tropical environment. Oecologia 14, 111– Mortality, resulting directly from predation or parasitism or 125. indirectly from the presence and activity of other dung Aschenborn, H.H., Loughnan, M.L. & Edwards, P.B. (1989) A colonizers, has previously been implicated as major deter- simple assay to determine the nutritional suitability of minants of fly abundance in pats (Kirk, 1992). cattle dung for coprophagous beetles. Entomologia Experi- Dung-colonizing Diptera generally reach their peak mentalis et Applicata 53, 73–79. abundance in late summer in southwest English pasture Beaver, R.A. (1977) Non-equilibrium ‘island’ communities: habitats (Lee & Wall, 2006b). In the present study in 2001, Diptera breeding in dead snails. Journal of Animal Ecology both N. cornicina and N. viridescens were only first detected in 46, 783–798. July and then showed a very short, pronounced seasonal Floate, K.D. (1998) Off-target effects of ivermectin on insects and peak in larval abundance of only 1–2 weeks centred around on dung degradation in southern Alberta, Canada. Bulletin pats placed out on September 3rd. It is possible, however, of Entomological Research 88, 25–35. given the highly aggregated distribution of eggs and larvae Floate, K.D., Wardhaugh, K.G., Boxall, A.B.A. & Sherratt, T.N. within pats discussed above, that the detection method used (2005) Fecal residues of veterinary parasiticides: nontarget in the present study, with batches of ten artificial pats effects in the pasture environment. Annual Review of deployed at weekly intervals in 2001, may not have been Entomology 50, 153–179. sufficiently sensitive to detect very low populations earlier in Godfray, H.C.J. & Parker, G.A. (1992) Sibling competition, the year and that considerably greater sample sizes might parent-offspring conflict and clutch size. Animal Behaviour have been needed. In one of the only other similar studies 43, 473–490. that has been carried out previously, Hammer (1941) Godfray, H.C.J., Partridge, L. & Harvey, P.H. (1991) Clutch size. suggested that Neomyia overwinter as adults, become active Annual Review of Ecology and Systematics 22, 409–429. in Spring and then pass through four or five generations, Gover, J. & Strong, L. (1995) Effects of ingested ivermectin on increasing exponentially in abundance in the field over body mass and excretion in the dung fly Neomyia cornicina. summer. The rate of oviposition and larval ectivity would be Physiological Entomology 20, 93–99. expected to be highly dependant on temperature, so the Gover, J. & Strong, L. (1996) Effects of ingestion of dung colonization and subsequent decomposition of a dropping containing ivermectin on aspects of behaviour in the fly will depend on the weather immediately following deposi- Neomyia cornicina. Physiological Entomology 21, 51–58. tion. While low temperatures appear to lengthen the time Greenham, P.M. (1972) The effects of the variability of cattle during which dung remains attractive to some invertebrates dung on the multiplication of the bushfly (Musca vetustis- (Vessby, 2001), this period still only lasts for a few days and sima Walk.). Journal of Animal Ecology 41, 153–165. in bad weather a dropping may remain completely un- Hammer, O. (1941) Biological and ecological investigations of colonized by insects (White, 1960). The suitability of a flies associated with pasturing cattle and their excrement. dropping as a resource, therefore, relies not only on its Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening physical properties but also on its availability to colonizers at 105, 141–393. a certain time. However, here no relationship between Hanski, I. (1987) Colonization of ephemeral habitats. pp. 155– abundance and any of the weather parameters in the week 185 in Gray, A.J., Crawley, M.J. & Edwards, P.J. (Eds) following deposition was observed. The reasons for this are Colonization, Succession and Stability. Oxford, Blackwell. unknown and few data exist on the relationships between Hanski, I. (1991) The Dung Insect Community. pp. 5–21 in weather conditions and oviposition or larval development in Hanski, I. & Cambefort, Y. (Eds) Dung Beetle Ecology. these species. Differences between the dairy and organic beef Princeton, Princeton University Press. farms in Neomyia abundance were minor and, where Heard, S.B. (1998) Resource patch density and larval aggre- differences were present, abundance was higher on the gation in mushroom breeding flies. Oikos 81, 187–195. dairy than the beef farm. Holter, P. (1979) Effect of dung beetles (Aphodius Spp.) and Precisely how the ecological differences between Neomyia earthworms on the disappearance of cattle dung. Oikos 32, cornicina and N. viridescens translate into functional special- 393–402. isation or how niche separation is maintained is unknown. Ives, A.R. (1991) Aggregation and coexistence in a carrion fly Clearly, further work is required to identify the nature community. Ecological Monographs, 61 75–94. and cause of the mortality experienced by N. viridescens and Iwasa, M., Nakamura, T., Fukaki, K. & Yamashita, N. (2005) N. cornicina. Nontarget effects of ivermectin on coprophagous insects in Japan. Environmental Entomology 34, 1485–1492. Kirk, A.A. (1992) The effect of the dung pad fauna on the emergence of Musca tempestiva (Dipt.: Muscidae) from dung Acknowledgements pads in Southern France. Entomophaga 37, 507–514. We are grateful to the University of Bristol for its financial Laurence, B.R. (1954) The larval inhabitants of cow pats. Journal support of C.L. We would like to thank Andrew Forbes of Animal Ecology 23, 234–260. for his personal interest and helpful comments on this Lee, C.M. & Wall, R. (2006a) Cow-dung colonization and manuscript and Merial Animal Health for financial support decomposition following insect exclusion. Bulletin of Ento- of EA. We are grateful to John Keedwell and Mike Amos mological Research 96, 315–322.

Lee, C.M. & Wall, R. (2006b) Distribution and abundance of Stevenson, B.G. & Dindal, D.L. (1987) Insect effects on insects colonizing cattle dung. Journal of Natural History 40, decomposition of cow dung in microcosms. Pedobiologia 1167–1177. 30, 81–92. Lumaret, J.P. & Kadiri, N. (1995) The influence of the first wave Stoffolano Jr., J.G. & Streams, F.A. (1971) Host reactions of of colonizing insects on cattle dung dispersal. Pedobiologia Musca domestica, Orthellia caesarion, and Ravinia l’herminieri 39, 506–517. to the nematode Heterotylenchus autumnalis. Parasitology 63, Lumaret, J.P., Errouissi, F., Galtier, P. & Alvinerie, M. (2005) 195–211. Pour-on formulation of eprinomectin for cattle: fecal eli- Strong, L., Wall, R., Woolford, A. & Djeddour, D. (1996) The mination profile and effects on the development of the effect of faecally excreted ivermectin and fenbendazole on dung-inhabiting Diptera Neomyia cornicina (L.) (Muscidae). the insect colonisation of cattle dung following the oral Environmental Toxicology and Chemistry 24, 797–801. administration of sustained-release boluses. Veterinary Para- Madsen, M., Overgaard Nielsen, B., Holter, P., Pederson, O.C., sitology 62, 253–266. Brochner Jespersen, J., Vagn Jensen, K.M., Nansen, P. & Thiel, A. & Hoffmeister, T.S. (2004) Knowing your habitat: Gronvold, J. (1990) Treating cattle with ivermectin: effects linking patch encounter rate and patch exploitation in on the fauna and decomposition of dung pats. Journal of parasitoids. Behavioral Ecology 15, 419–425. Applied Ecology 27, 1–15. Vessby, K. (2001) Habitat and weather affect reproduction and Marsh, R. & Campling, R.C. (1970) Fouling of pastures by dung. size of the dung beetle Aphodius fossor. Ecological Entomology Herbage Abstracts 40, 123–130. 26, 430–435. McAlpine, J.F. (1981) Morphology and terminology – adults. Wall, R. (1993) The reproductive output of the blowfly Lucilia pp. 9–63, vol. 1 (Monograph 27) in McAlpine, J.F., Peterson, sericata. Journal of Insect Physiology 39, 743–750. B.V., Sherwell, G.E., Teskey, H.J., Vockeroth, J.R. & Wood, Wall, R. & Strong, L. (1987) Environmental consequences of D.S. (Eds), Manual of Nearctic Diptera. Ottawa, Research treating cattle with the antiparasitic drug ivermectin. Branch, Agriculture Canada. Nature 327, 418–421. Skidmore, P. (1991) Insects of the British Cow-Dung Community. Wall, R., Green, C., French, N. & Morgan, K. (1992) Develop- 166 pp. Shrewsbury, UK, Field Studies Council. ment of an attractive target for the sheep blowfly Lucilia Sommer, C., Steffansen, B., Nielsen, B.O., Gronveld, J., Vagn sericata. Medical and Veterinary Entomology 6, 67–74. Jensen, K.-M., Jespersen, J.B., Springborg, J. & Nansen, P. Wardhaugh, K.G. & Rodriguez-Mendez, H. (1988) The effects (1992) Ivermectin excreted in cattle dung after subcuta- of the antiparasitic drug, ivermectin, on the development neous injection or pour-on treatment: concentrations and and survival of the dung-breeding fly, Orthelia cornicina (F.) impact on dung fauna. Bulletin of Entomological Research 82, and the scarabaeine dung beetles, Copris hispanus L., Bubas 257–264. bubalus (Oliver) and Onitis belial F. Journal of Applied Sommer, C., Vagn Jensen, K.-M. & Jespersen, J.B. (2001) Entomology 106, 381–389. Topical treatment of calves with synthetic pyrethroids: Withers, T.M., Madie, C. & Harris, M.O. (1997) The influence of effects on the non-target dung fly Neomyia cornicina clutch size on survival and reproductive potential of (Diptera: Muscidae). Bulletin of Entomological Research 91, hessian fly. Entomologia Experimentalis et Applicata 83, 205– 131–137. 212. Sowig, P. (1996) Duration and benefits of biparental brood care White, E. (1960) The distribution and subsequent disappearance in the dung beetle Onthophagus vacca (Coleoptera: Scar- of sheep dung on pennine moorland. Journal of Animal abaeidae). Ecological Entomology 21, 81–86. Ecology 29, 243–250.