Ecosystem services provided by dung beetles in Australia

Although there are nearly 500 species of native dung beetles in Australia, most are adapted to small, hard, dry, pelletised marsupial droppings and not to dealing with the large, moist deposits of cattle. In 1788, Governor Arthur Phillip arrived at Botany Bay with five cows, two bulls, 44 sheep and seven horses: this signalled major changes in Australia. Now there are about 27 million cattle, whose annual dung production has a dry matter content of about 42 million tonnes. Until CSIRO introduced exotic dung beetles in the 1960s, the dung of these herbivores sat on the soil surface, sometimes for years, locking up organic matter, smothering pasture and polluting waterways. CSIRO introduced 53 exotic dung beetle species, of which 43 were released to the Australian mainland between 1965 and 1985. Twenty-three of these have become established, many of which have reached the natural limits of their distribution. I consider the reason for the failure of the other 30 species to establish and briefly review previous contributions to examining the role of dung beetles in delivering ecosystem services, noting that much of the published literature concerns laboratory studies. New field data are then examined on the way in which introduced species are transforming dung communities and the ecosystem services they provide. The capacity of deep-tunnelling dung beetles to transform the soil profile is examined along with their effects on pasture production and the flow of nutrients from dung on pasture. The biocontrol capacity of dung beetle activity is considered in relation to the native bush fly, Musca vetustissima, the introduced buffalo fly, Haematobia irritans exigua, and dung-borne intestinal parasites (helminths and Cryptosporidium). The rationale for introducing additional species to Australia is considered.     

SEASONAL ABUNDANCE OF MUSCA VETUSTISSIMA WALKER AND OTHER CATTLE DUNG FAUNA IN CENTRAL AUSTRALIA

Abstract
Bush flies, Musca vetustissima attracted to a human, and arthropod fauna attracted to fresh cattle dung in 24 hours, were sampled every 2 weeks for 2 years (1980–1982) near Alice Springs in central Australia. Substantial rain fell in both summers, but it was more prolonged in the second. The bush fly occurred and bred throughout the year, although its abundance was usually low. The only major increase in bush fly abundance occurred after the first summer's rainfall caused the growth of new herbage. This was followed by increased feeding on dung by adult flies and intensified breeding. Bush fly abundance was low in the second summer, despite evidence of a long period of continuous breeding. A variety of dung-feeding and predatory beetles and also mites was almost always present, although numbers were usually low. The introduced dung beetles Euoniticellus intermedius and Onthophagus gazella numerically dominated samples. Dung fauna abundance also increased after significant rainfall, particularly in the second summer. Dissections of the dung beetles showed that they bred at these times.     

Breeding of the bush fly,Musca vetustissima Walker,in an over-wintering area during winter and spring

Field experiments in an area of south-western Australia where bush fly (Musca vetustissima) adults occur permanently, showed that it overwintered by continuous breeding; but only two to three generations occurred between June and September. Low survival of eggs and larvae in the food (cattle dung) from May to August was associated with rainfall rather than low temperatures. High egg-adult survival occurred in late August; lower egg and larval survival in September and early October was attributed partly to dung fauna. Egg and larval survival was high in late October until December but predation or parasitization caused low survival of puparia outside the dung. Experimental and wild adult flies were largest and therefore most fecund in early spring; smaller wild flies in late spring appeared to result from larval competition for food. Simultaneous high egg-adult survival, high fecundity and rapidly decreasing generation times in late winter and early spring provide a basis for explaining the major increase in adult bush fly abundance observed in some areas in mid-spring.     

Populations of the bush fly (Musca vetustissima Walker) in arid Australia

Populations of the bush fly Musca vetustissima were usually low in arid south-western Australia. Herbaceous plants that grew only after rain resulted in changes to cattle dung that increased its attractiveness to bush flies for oviposition in laboratory tests. Larvae reared in such dung consistently produced large flies of high fecundity, and larval survival was usually high. Similar responses to the dung were evident from examination of flies sampled in the field. Although greatly increased bush fly abundance was possible only after major improvement in cattle dung, it was not a general phenomenon as immature survival did not always increase. Even major population increases resulted from periods of high immature survival that were brief relative to the duration of favourable dung. Nematodes Heterotylenchus sp. appeared to be an important mortality factor of the immature stages at such times. Build-up of high bush fly populations occurred only in cattle-grazing areas, but base-level abundance was similar regardless of the presence of cattle. Almost all female flies were gravid when cattle dung was unfavourable for breeding, and in areas without cattle. In arid areas, acceptable oviposition sites probably are more limiting than are sources of protein for oögensis.     

Asymmetric competition in cattle dung between two species of Onthophagus dung beetle and the bush fly, Musca vetustissima

Abstract.

• 1 Competition in cattle dung pads between two dung beetles, Onthophagus ferox Harold and Onthophagus binodis Thunberg, and the bush fly, Musca vetustissima Walker, was investigated in laboratory experiments, to determine why spring fly abundance in the field did not fall following the introduction of O. binodis.
• 2 At low beetle densities, the number of eggs laid by each species was reduced by the second species. A similar amount of dung was buried by each species alone or by both together.
• 3 At high beetle densities O. binodis egg production was substantially affected by each additional O.ferox, but O.ferox egg production was not affected by each additional O.binodis. Asymmetric competition occurred because O.ferox buried more dung than O.binodis, and a greater proportion in day 1 (pre-emptive dung burial).
• 4 O.ferox caused greater M. vetustissima egg-puparia mortality than O. binodis. Mortality mostly occurred in young M. vetustissima larvae less than 1 day old. Total egg-puparia fly mortality was correlated better with the dung buried on day 1 than dung buried on day 8 (pre-emptive dung burial). O.binodis did not add to fly mortality by O.ferox at high densities because of asymmetric competition between the beetles.

     

Interacting biocontrol programmes: invasive cane toads reduce rates of breakdown of cowpats by dung beetles

Ecological interactions among invasive species can affect not only the success of the invaders, but also their impact on ecosystems in the invaded range. In Australia, both dung beetles (subfamily Scarabaeinae) and cane toads (Rhinella marina) were introduced for biocontrol: the beetles to break down bovine faeces piles (cowpats) that otherwise accumulate and reduce pasture productivity, and the cane toad to consume scarab beetles that eat sugarcane and thus reduce sugar production. The dung beetles have been a success, whereas the toads have been a failure. Our experimental studies show that as well as impacting native fauna directly, cane toads reduce the rate of cowpat breakdown by consuming dung beetles. In the laboratory, dehydrated toads actively sought out cowpats based on scent cues, and in field enclosures, the presence of a cane toad significantly reduced rates of cowpat decomposition. Although toads have benefited from agricultural activities, their spread across Australia likely has reduced the effectiveness of one of the most successful biocontrol programmes ever conducted in that continent.     

Seasonal variations in numbers,biomass and breeding patterns of dung beettles [Coleoptera: Scarabaeidae] in Southern France

Seasonal variations in numbers and biomass and breeding of 28 species ofScarabaeidae-Scarabaeinae andGeotrupidae were studied at 2 temperate sites and 2 mediterranean sites in southern France in 1978 and 1979, using cattle-dung baited pitfall traps. Maximum dung burial occurred when females were parous and ovipositiong (i.e. during spring at the mediterranean sites and summer at the temperate sites). Using biomass as a measure of dung burial the most important spring active beetles at the mediterranean sites were:Budas bison, B. bubalus, Scarabaeus laticollis, Onthophagus lemur andCopris hispanus, and at the temperate sites:C. lunaris, O. vacca, andO. ovatus. These results confirmed the previous choice ofC. hispanus, C. lunaris, B. bison andO. vacca for introduction into Australia. In addition it is suggested thatB. bubalus, S. laticollis andO. lemur be considered for introduction into mediterranean areas of south western Australia to complement those species already introduced for bush fly control.      

Attractiveness of baits to dung beetles in Brazilian savanna and exotic pasturelands

The Brazilian savanna is the second largest ecosystem in Brazil. It is also one of the most endangered, with only 20% of its habitat remaining unchanged. Agriculture and livestock have been indicated as the main agents of destruction of the Brazilian savanna. Brazilian livestock, for example, is the main reason for cultivation of exotic grasses such as Urochloa spp. (from Africa). Dung beetles are widely used in ecological assessment, mainly because they are recognized as bioindicators of environmental changes. Therefore, efficient sampling is required for any research involving the biodiversity of this group. In order to mitigate the lack of information on efficiency of the attractiveness of baits in the endangered Brazilian savanna and in exotic pasturelands, we sampled dung beetles in four native patches of the Brazilian savanna and in four areas of pastures with Urochloa spp. Dung beetles were captured with pitfall traps baited with carcass, cattle dung, human feces and pig dung, with a total sampling effort of 384 traps. We sampled 7544 individuals belonging to 43 species and 18 genera of dung beetles. Thirty‐eight species were collected in the Brazilian savanna and 24 species in exotic pastureland. In both ecosystems traps baited with human feces sampled greater abundance and species richness of dung beetles when compared with the other three baits used. Our results showed that human feces is a reliable, easy and inexpensive bait to sample greater abundance and species richness of generalist dung beetles in both native and exotic habitats, with clear structural differences.     

The potential for indirect effects between a weed, one of its biocontrol agents and native herbivores: A food web approach

The safety of biological control is a contentious issue. We suggest that constructing and analyzing food webs may be a valuable addition to standard biological control research techniques, as they offer a means of assessing the post-release safety of control agents. Using preliminary data to demonstrate the value of food webs in biocontrol programs, we quantified the extent to which a key agent has infiltrated natural communities in Australia and, potentially, impacted on non-target species. Using these data, we also demonstrate how food webs can be used to generate testable hypotheses regarding indirect interactions between introduced agents and non-target species. We developed food webs in communities invaded to varying degrees by an exotic weed, bitou bush, Chrysanthemoides monilifera ssp. rotundata, and a key biocontrol agent for this weed in Australia, the tephritid fly, Mesoclanis polana. Three food webs were constructed during springtime showing the interactions between plants, seed-feeding insects and their parasitoids. One food web was constructed in a plot of native Australian vegetation that was free of bitou bush (‘bitou-free’), another in a plot of Australian vegetation surrounded by an invasion of bitou bush (‘bitou-threatened’) and a third from a plot infested with a monoculture of bitou bush (‘bitou-infested’). The bitou-free web contained 36 species, the bitou-threatened plot 9 species and the bitou-infested web contained 6 species. One native Australian herbivore attacked the seeds of bitou bush. M. polana, a seed-feeding fly, was heavily attacked by native parasitoids, these being more abundant than the parasitoids feeding on the native seed feeders. A surprising result is that none of the three species of native parasitoids reared from M. polana were reared from any of the native herbivores. The food webs revealed how a highly host-specific biocontrol agent, such as M. polana has the potential to change community structure by increasing the abundance of native parasitoids. The webs also suggest that indirect interactions between M. polana and native non-target species are possible, these been mediated by shared parasitoids. The experiments necessary to determine the presence of these interactions are outlined.     

The effect of the dung pad fauna on the emergence ofMusca tempestiva [Dipt.: Muscidae] from dung pads in southern France

The emergence ofMusca tempestiva Fallèn, from cow pads in southern France was reduced by a mean of 98% and 96% respectively in nine experiments concluded in 1979 and 1981, by the action of the complete dung fauna. Fauna emerging from dung pads and captured in simultaneous trapping using dung baited pitfall traps consisted of 13 Dipterous species (9 Muscidae, 2 Sepsidae and 2 Sphaeroceridae), 25 Coleopterous species (7 Scarabaeidae, 1 Geotrupidae, 2 Aphodiidae, 3 Hydrophilidae, 12 Staphylinidae), 3 Hymenopterous parasites and 1 species of macrochelid and 2 species of parasitoid mites carried phoretically by the dung beetles. The total number of insects and mites per trap was usually small. The Staphylinidae which included 4Aleochara species of whichAleochara tristits Gravenhorst andA. bipustulata (L.) are known parasitoids of Diptera pupae, and 6 predatory species, were the most abundant insects present. Whilst the overall abundance of insects and mites trapped was relatively low it is probable that the most important factor in the control ofM. tempestiva was the combined influence of the different elements making up the dung pad fauna.     

Generalist dung attraction response in a New Zealand dung beetle that evolved with an absence of mammalian herbivores

1. Dung beetles (Scarabaeidae: Scarabaeinae) are integral parts of many ecosystems because of their role in decomposition of dung; particularly mammal dung, which forms the diet of both larvae and adults. 2. New Zealand dung beetles are unusual as they are flightless and evolved on islands with a highly depauperate mammal fauna and thus without the usual dung resource used by dung beetles elsewhere. The diet of New Zealand dung beetles is unknown. 3. We hypothesised (1) that the endemic dung beetle Saphobius edwardsi would be attracted to a broad range of food types, and (2) that S. edwardsi would be able to survive and reproduce on a range of dung types and puriri (Vitex lucens) humus. 4. Laboratory choice tests identified that S. edwardsi was attracted to a range of mammal, bird, invertebrate, and reptile dung types, but not to non‐dung food sources. Five‐month no‐choice tests found that beetle survival rates were lower for beetles fed with humus compared with those fed on mammal, bird, or invertebrate dung. None of the beetles reproduced. 5. This study suggests S. edwardsi have a strong preference for dung, and are likely to be broad dung generalists in their feeding behaviour.     

Dung beetle distribution patterns in the Iberian peninsula

A canonical variate analysis was used to summarize the distribution pattern of 30 species of dung beetles (Scarabaeinae) from 162 sites in the Iberian peninsula (Spain and Portugal) in relation to 4 site variables. The best separation of beetle species, obtained using a xerothermic climatic index, was into 3 groups called “mediterranean”, “unrestricted” and “temperate”. Little further separation was achieved using altitude, dung type or soil type. These data are used to select dung beetles for introduction to south-western Australia for bush fly control.

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Résumé On a fait appel à l'analyse de variables canoniques pour résumer le plan de distribution, relatif à 4 variables de localité, de 30 espèces de bousiers (Scarabaeinae) de 162 localités de la Péninsule ibérique (l'Espagne et le Portugal). La meilleure division des espèces, obtenue à l'aide d'un indice xérothermique climatique, se faisait en 3 groupes désignés respectivement comme “méditerranéen”, “ubiquiste” et “tempéré”. Peu de séparation supplémentaire a été obtenue en ayant recours à des facteurs d'altitude, de nature de la bouse ou de type de sol. Ces données ont été employées pour aider à la sélection de bousiers destinés à être introduits en Australie Occidentale pour y combattreMusca vetustissima Walker[Diptera].

     

Mating Status and Choice of Group Size in the Phoretic Fly Norrbomia frigipennis (Spuler) (Diptera: Sphaeroceridae)

The phoretic sphaerocerid fly Norrbomia frigipennis mates on scarabid dung beetles, follows them underground, and lays eggs in the collected dung. We found that male and female flies distribute themselves nonrandomly on beetles with respect to fly group size. The proportion of virgin females increased with group size, and females with mature eggs were most frequently found on beetles carrying fewer flies. Laboratory experiments revealed that mated females avoided larger groups, virgin females seemed to prefer large groups and mated females, small groups. Males showed no such pattern. These results suggest that N. frigipennis can estimate group size, presumably an adaptation with a reproductive function. However, flies did not join hosts on the basis of the sex of already mounted flies.     

Attractiveness of dung beetles (Coleoptera: Scarabaeinae) to faeces from native mammals in different trophic guilds

Dung beetles are predominantly coprophagous and use mammalian faeces as their main food resource and for offspring rearing. However, these resources are generally ephemeral and scarce. The objective of this study was to verify the attractiveness to dung beetles of the faeces of nine native mammal species of the Cerrado biome in different trophic guilds. This study was conducted during the rainy season (October 2016 to March 2017) in two sensu stricto areas of the Cerrado in the Brasília National Park (PNB), Federal District, Brazil. Pitfalls containing faeces of nine mammals native to the region were used as bait (from three herbivores, three carnivores and three omnivores) for the collection of dung beetles. We collected 203 individuals and 19 species, and the most abundant species were Uroxys aff. thoracalis, Oxysternon palemo, Coprophanaeus spitzi and Diabroctis mirabilis. The most attractive faecal bait was from the omnivorous Chrysocyon brachyurus (32.67% of the individuals and 13 species). This study reveals variation in the attraction of dung beetles to native mammal dung of the Cerrado, with more abundance in the faeces of omnivores and carnivores and less in the faeces of herbivores. The species composition in the carnivore baits did not differ from that of the omnivore baits. These data indicate that changes in Scarabaeinae assemblages result from changes in mammal species such as those that have occurred in the Cerrado biome with the conversion to cattle production, which in recent years has caused intense fragmentation of habitats, expansion of agricultural and livestock activities and the introduction of exotic species. The mammal C. brachyurus, vulnerable to extinction in Brazil, should be a focus for future research, since its faeces support a great diversity of dung beetles in the Cerrado.     

Influence ofOnthophagus gazella on hornfly,Haematobia irritans density in irrigated pastures

Haematobia irritans (L.) breeding in flood irrigated pastures of the lower Colorado Desert of southeastern California continues to remain unacceptably high during warm seasons (>1,000 adult flies per bovine head) despite the presence of moderately abundant populations ofOnthophagus gazella F. This study suggests that densities of > 40–70 adult beetles per dung pad and giving pronounced dung shredding activity, caused fly mortality of 38–56 %. The continued high abundance of adult horn flies on cattle suggests that at > 50% mortality, the pasture environment still produces sufficient flies to saturate cattle, although emigration might be reduced. Additional species of scarabs may be necessary to increase fly mortality. However, the dung drying activity of existingO. gazella significantly could interfere with resident staphylinid beetle breeding, which was significantly lower in pastures whereO. gazella reached densities of 40 per dung pad. Scarab beetle activity might also impede the introduction of superior predatory species for biological control.      

Dung burial strategies in some South African coprine and onitine dung beetles (Scarabaeidae: Scarabaeinae)

ABSTRACT.

• 1 The dung colonization and dung burial behaviour of twelve crepuscular/nocturnal tunnelling (paracoprid) species of beetles were examined in order to identify mechanisms which might facilitate resource (dung) partitioning. The species were selected from a diverse assemblage of dung beetles, the members of which coexist in the sandy-soil regions of Natal, South Africa.
• 2 The pattern of dung colonization in relation to dung age was examined in the field using baited pitfall traps. Some species, e.g. Onitis deceptor Peringuey, Catharsius tricornutus De Geer and Copris elphenor Klug, showed a marked preference for fresh dung (1–2 days old) whereas other species, e.g. O. viridulus Boheman and Copris fallaciosus Gillet, preferred older dung (3–7 days old).
• 3 Two distinct patterns of dung burial were recognized. In the Coprini, dung burial was complete within 24–48h of pad colonization, and the level of dung burial was similar in the laboratory and in the field. In the Onitini, dung burial occurred progressively over a 12-day period, although the timing of initiation of dung burial varied between species: in O. deceptor nearly all individuals had begun burial within 2 days of pad colonization, whereas only 20% of O. viridulus had commenced dung burial by that time. However, nearly all O. viridulus had buried substantial quantities of dung by day 12.
• 4 The mass of dung buried per pair by the larger coprine beetles (100–300 g) and onitine beetles (400–1000 g) suggests that there is potential for inter- and intraspecific competition, even in pads colonized by relatively few beetles. The colonization and use of dung of different ages are discussed as means of resource partitioning in relation to the relative abilities of species to compete for dung.

     

SEASONAL CHANGES IN FAVOURABILITY OF CATTLE DUNG IN CENTRAL QUEENSLAND FOR THREE SPECIES OF DUNG-BREEDING INSECTS

b
The favourability of cattle dung from a native pasture near Rockhampton, Queensland, as a food source was tested monthly in the laboratory for 2 yr using 3 dung-breeding insects: the buffalo fly, Haematobia irritans exigua De Meijere; the bush fly, Musca vetustissima Walker; and a dung beetle, Euoniticellus intermedius (Reiche). Dung produced by cattle grazing on this pasture during the summer wet season yielded larger flies of both species and more broods from the dung beetle than dung from the same pasture in winter. When reared in summer dung, the buffalo fly almost attained its maximum recorded size but the bush fly and dung beetle reached ca two-thirds maximum recorded size and brood production respectively. Bush flies failed to breed in dung collected for 4 consecutive months in winter each year but survival of buffalo flies showed no seasonal trends.
The early response of the buffalo fly to improving dung quality in late winter/early spring gives it an advantage enabling its populations to increase earlier than those of its competitors, including the dung beetle, E. intermedius.     

Facilitative interactions between an exotic mammal and native and exotic plants: hog deer (<Emphasis Type="Italic">Axis porcinus</Emphasis>) as seed dispersers in south-eastern Australia

Endozoochory by exotic mammalian herbivores could modify vegetation composition by facilitating the dispersal and establishment of exotic and native plant species. We examined the potential for endozoochoric dispersal of native and exotic plants by exotic hog deer (Axis porcinus) in south-eastern Australia. We quantified the germinable seed content of hog deer faecal pellets collected in five vegetation types within a 10,500-ha study area that was representative of their Australian range. Twenty exotic and 22 native species germinated from hog deer faecal pellets and significantly more native species germinated compared to exotic species. Seedlings of the encroaching native shrub Acacia longifolia var. sophorae emerged, but no native trees emerged and the percentage of grasses that germinated was low (11%). The species composition of germinants was similar among the five vegetation types. We estimated that the hog deer population in our study area could potentially disperse >130,000 viable seeds daily. Our study shows how an exotic mammal can disperse seeds from both native and invasive plants and highlights the need for endozoochory to be considered more widely in studies assessing the impacts of exotic mammals on plant communities.     

Effect of dung burial by the dung beetle Bubas bison on numbers and viability of Cryptosporidium oocysts in cattle dung

Cryptosporidium oocysts were inoculated into fresh dung (∼1.2 × 10⁴ oocysts per gram wet weight) and fed to dung beetles to assess the effect of dung burial by the dung beetle Bubas bison on the distribution of the oocysts in small cores of soil in the laboratory. The experiment consisted of five replicates of each of two treatments; controls (dung but no dung beetles) and the experimental treatment (inoculated dung and seven pairs of dung beetles). After 5 days, when approximately 90% of the dung was buried, the surface and buried dung was recovered and subsampled. The oocysts in the subsamples were recovered and enumerated using qPCR. Oocyst viability was evaluated using an assay based on the exclusion or inclusion of two fluorogenic vital dyes, 4′,6-diamidino-2-phenylindole (DAPI) and propidium iodide (PI). Results revealed that overall 13.7% of oocysts remained on the surface and 86.3% of oocysts were buried. The viability of oocysts in buried dung was only 10% compared to oocysts the surface dung (58%). Therefore, widespread dung burial by B. bison during the winter months could substantially reduce the numbers of Cryptosporidium oocysts available to be washed into waterways following winter rains.     

The phenology of Onitis alexis (Coleoptera: Scarabaeidae) in the Araluen Valley: Survival in a marginal environment

The introduced African dung beetle, Onitis alexis Klug, has become established in the warmer regions of Australia. The south-eastern limit of its current distribution is Moruya, NSW, and the Araluen Valley 50 km inland. At Araluen newly emerged beetles are present in dung in late spring, summer and autumn. Egg-laying starts 1-2 weeks after emergence and continues throughout the summer and autumn, as indicated by the presence of parous females in the population and of broods under experimental pads. Eggs laid in December/January produce adults in late summer and autumn, those laid from February to April produce adults in the following spring and summer. In the laboratory, mortality of larvae is high in cold (0–16°C), wet conditions and their development is delayed in warm (25°C and 27°C), dry conditions. This delay was confirmed in the field during the summer drought of 1982-83 when predicted times of emergence (based on day-degree summation in the soil) always preceded the observed emergence time of the local population, as well as preceding the emergence of beetles developing from eggs laid at known times. Follicle resorption in adult females was related directly to increasing age and to rainfall. Dung collected from hayed-off pasture did not affect fecundity, but caused larval mortality. Adults survived the winters at Araluen in some years, and immatures survived best during dry winters, being facilitated in this by a cold-induced larval diapause. Onitis alexis larvae can survive wet or dry summers, and cold dry winters (down to about 0°C) but not wet winters. This seems to be the major factor limiting the southern distribution of the species.