Phylogeny and biogeography of the dung beetle genus Phanaeus (Coleoptera: Scarabaeidae)

Abstract The dung beetle genus Phanaeus as currently recognized by Edmonds (1994) consists of 51 species placed in 13 species groups and two subgenera. Here, I examine the phylogeny and biogeography of this genus by analysing the mitochondrial cytochrome oxidase subunit I (530 bp), nuclear large subunit ribosomal RNA (28S, D2 region), and 67 morphological characters for 28 species of Phanaeus. Both maximum parsimony and Bayesian analyses from the combined data yielded well‐resolved trees, although low bootstrap and posterior probability support were found for basal nodes. The phylogenetic hypotheses presented here suggest that the subgenera Phanaeus s.str. and Notiophanaeus should each be elevated to the status of full genus. With the exception of the eucraniine outgroups, the paleano species group of the genus Phanaeus is recovered as sister to all other taxa, including the outgroups Oxysternon, Sulcophanaeus and Coprophanaeus. High bootstrap values and posterior probabilities supported the species groups endymion, tridens and vindex. Biogeographical analyses suggest an ancestral distribution for Phanaeus in the Andes in South America, although numerous dispersal events evidently have produced a complicated biogeographical history.     

A comparison of dung beetle (Coleoptera: Scarabaeidae) attraction to native and exotic mammal dung

Although the preference of dung beetles (Coleoptera: Scarabaeidae) for specific types and conditions of dung has been given substantial attention, little has been done to investigate the potential effects of exotic mammal introduction for game farms or rewilding projects. We used pitfall traps baited with various native and exotic herbivore, carnivore, and omnivore dung to evaluate dung beetle preference in the Great Plains of North America. Additionally, we analyzed of the nutrient quality of each dung type. In total, 9,089 dung beetles from 15 species were captured in 2 yr of sampling. We found significant differences (P < 0.05) in mean dung beetle capture among omnivore, herbivore, and carnivore dung, as well as differences in individual species preference for dung type. Omnivore dung was the most attractive with chimpanzee and human dung having the highest mean capture (291.1 ± 27.6 and 287.5 ± 28.5 respectively). Carrion also was highly attractive with a mean of 231.9 ± 20.6 beetles per trap (N = 8). Our results suggest definitive local preference of carrion in Phanaeus vindex Macleay and Onthophagus hecate (Panzer), while the congener, O. pennsylvanicus (Harold), was rarely captured in carrion and highly preferred omnivore dung. Preference for a specific bait type does not appear to be correlated with dung quality, mammalian diet, or origin of mammal. Results suggest niche segregation by dung type among dung beetle species.     

Between-group differences in the Iberian dung beetle species-area relationship (Coleoptera: Scarabaeidae)

Between-group α- and β-diversity differences were derived from species-area relationships fitted to field data. The accuracy of spatial richness variation predictions based on area size was also checked. The log-log model (log S = c + z log A) was found to be the best-fit linear model, with slopes (z) ranging from 0.089 to 0.142. Between-group comparisons of z (slope) and q (intercept) parameters, using the S = q + cA^z curvilinear regression model, corroborated early results, indicating a lower β-diversity (slope) for Scarabaeinae than for Geotrupinae and Aphodiinae. The latter group, probably more sensitive to environmental heterogeneity, should contribute more to species richness in large areas. α-Diversity is greater for Aphodiinae, more relevant to local diversity (1 km²), than for Scarabaeinae and considerably greater for these two groups than for Geotrupinae. As earlier results show that the richness of a single dung pat is rather more a function of the Scarabaeinae species pool, richness on dung pat scales is probably due more to the between-dropping mobile Scarabaeinae, while Aphodiinae contribute mainly to local and regional pool richness. Nearly 88 % of the total richness variance is explained by area size. This percentage decreases to 37 % when the spatial structure of area size and species number are extracted. The corresponding figures for Scarabaeinae, Aphodiinae and Geotrupinae are 44, 22 and 31 %, respectively.     

Suspected side effects of a herbicide on dung beetle populations (Coleoptera: Scarabaeidae).

This paper addresses the association between use of a herbicide and anecdotal reports of reduced dung degradation and dung beetle populations. Dung beetles were monthly collected at two adjacent ranches in Mexico. Ranches were similar in area, elevation, exposition, soil, and vegetation, but differed in weed control. Ranch A controlled weeds manually, and ranch B controlled unwanted vegetation with applications of the herbicide Tordon 101M. The main species recovered on each ranch (Ataenius apicalis) was significantly more abundant at ranch A than at ranch B. Conversely, similar numbers of a second species, Ataenius sculptor, were recovered from both ranches. Three lines of evidence support the tentative conclusion that herbicide applications may be causing a decline in populations of A. apicalis on ranch B. First, the greatest reductions of A. apicalis were observed during periods of herbicide application. Second, A. sculptor, apparently little affected by these same herbicide applications, is active primarily during months without herbicide applications. Third, preliminary results of laboratory studies show that exposure to herbicide can impair reproductive function of the dung beetle Canthon cyanellus.     

Nesting of Afrotropical Oniticellus (Coleoptera, Scarabaeidae) and its evolutionary trend from soil to dung

Abstract. 1. Oniticellus egregius Klug constructs brood ovoids of dung in the soil immediately under the edge of animal droppings. Each successive brood ovoid is enveloped within a soil shell. After completion of brood construction, loose earth is cleared from around the broods to produce a brood chamber. The immatures are then abandoned as eggs or first instar larvae.
2. O.planatus Castelnau and O.formosus Chevrolat usually construct brood balls of dung within animal droppings. Each brood is progressively enlarged by the addition of further dung after egg-laying. This enlargement is slight in O.planatus and marked in O.formosus. Parental females of both species remain in the brood chambers during development of the immatures which are abandoned principally as pupae.
3. Under very moist experimental conditions, O.planatus buries dung and constructs broods shallowly in the soil. Such nests are frequently connected to the pad by a short tunnel.
4. From a consideration of behavioural patterns it is suggested that the specialized nesting habits of these species have been derived from those of dung-burying ancestors similar to the modern genus, Euoniticellus, through reduction and loss of tunnelling in the soil.     

Stenosternus Karsch,a possible link between Neotropical and Afrotropical Orphninae (Coleoptera,Scarabaeidae)

The monotypical orphnine genus Stenosternus Karsch is known from a single specimen of Stenosternus costatus collected on the São Tomé island (Gulf of Guinea). The holotype of Stenosternus costatus Karsch is re-examined and its characters are discussed and illustrated. Although the genus was implicitly placed by Paulian (1984) in the Old World tribe Orphnini Erichson, re-examination of the holotype of Stenosternus costatus shows that it has characters similar to those of the members of the New World tribe Aegidiini Paulian. Placement of Stenosternus in the Aegidiini is supported by the metepisternum widened posteriorly (forming posterior metepisternal lock for closed elytra) and a keel separating basal and anterolateral parts of propleurae. Relationships of Stenosternus with other orphnine taxa and possible ways of origin of São Toméan orphnine fauna are discussed.     

Duration and benefits of biparental brood care in the dung beetle Onthophagus vacca (Coleoptera: Scarabaeidae)

Abstract.

• 1 Single males, single females or pairs of dung beetles, Onthophagus vacca, were released on artificial small (100 g) or large (1000 g) dung pats in the laboratory. Emigrating beetles were trapped at 12 h intervals, and the number and size of the brood chambers were recorded after each replicate.
• 2 Emigration of males was delayed if females were present in the same dung pats, whereas emigration times of females were independent of the presence or absence of males.
• 3 A residency of 60 h proved to be a threshold value. Females emigrating before this time did not breed, whereas those emigrating later had built at least two brood chambers.
• 4 Females paired with males built more brood chambers than single females.
• 5 The reproductive success of pairs was not influenced by the size of the dung pats.

     

Horn polyphenism and related head shape variation in a single-horned dung beetle: Onthophagus (Palaeonthophagus) fracticornis (Coleoptera: Scarabaeidae)

Horns of Onthophagus beetles are typical examples of phenotypically plastic traits: they are expressed as a function of environmental (nutritional) stimuli, and their reaction norm (i.e. the full set of horn lengths expressed as a response to different degrees of nutritional states) can be either linear or threshold-dependent. Horned males of Onthophagus ( Palaeonthophagus ) fracticornis (Preyssler, 1790) bear a single triangular cephalic protrusion of vertex carina, which has received phylogenetic support as the most primitive horn shape in the genus. Inter- and intra-sexual patterns of horn expression were studied in O. fracticornis by means of static allometries while associated variations in head shape were assessed using geometric morphometric techniques. The relation between log-transformed measurements of body size and vertex carina supported an isometric scaling in females. On the contrary, a sigmoidal model described better the horn length-body size allometry in males, with a switch point between alternative morphs at a pronotum width of 3.88 mm. Sigmoidal static allometries of horns in Onthophagus populations arise from a threshold-dependent developmental process of horn growth. This process underlies the expression of both plesiomorphic and apomorphic horn shapes in the genus. Given that the single-horn model has been identified as primitive, we propose that such a developmental process giving rise to it may be evolutionarily ancient as well. Horn expression was accompanied by a deformation of the head which makes minor and major morphs appear even more different. Therefore, in this species both horn and head shape expression contribute to male dimorphism.     

Hormonal control of male horn length dimorphism in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae)

Male dung beetles (Onthophagus taurus) facultatively produce a pair of horns that extend from the base of the head: males growing larger than a threshold body size develop long horns, whereas males that do not achieve this size grow only rudimentary horns or no horns at all. Here we characterize the postembryonic development of these beetles, and begin to explore the hormonal regulation of horn growth. Using radioimmune assays to compare the ecdysteroid titers of horned males, hornless males, and females, we identify a small pulse of ecdysteroid which is present in both hornless males and females, but not in horned males. In addition, we identify a brief period near the end of the final (third) larval instar when topical applications of the juvenile hormone analog methoprene can switch the morphology of developing males. Small, normally hornless, males receiving methoprene during this sensitive period were induced to produce horns in 80% of the cases. We summarize this information in two models for the hormonal control of male dimorphism in horn length.     

SPLAT-OrB reveals competitive attraction as a mechanism of mating disruption in oriental beetle (Coleoptera: Scarabaeidae)

This study compared the efficacy of SPLAT-OrB, a new pheromone formulation for oriental beetle mating disruption that can be mechanically applied, with hand-applied plastic dispensers in commercial blueberry fields. Both formulations were tested at 2.5 and 5 g of the major sex pheromone component (Z)-7-tetradecen-2-one per hectare, and evaluated by measuring trap shut-down, mating success of caged females, and the number of grubs in sentinel blueberry pots baited with tethered females. All pheromone-treated plots had fewer male captures in traps and lower mating success of caged females compared with untreated plots. SPLAT-OrB, and plastic dispensers at the higher rate, also reduced the number of grubs in sentinel pots. To understand the mechanism of mating disruption in oriental beetle, males were observed approaching the pheromone sources in disrupted plots. In addition, male oriental beetle captures were quantified in plots treated with varying SPLAT-OrB dollop densities per ha. Consistent with predictions for competitive attraction, field observations revealed males approaching the pheromone source and male captures decreasing concavely with increasing dollop density. In a mark-release-recapture study, male oriental beetles responded to SPLAT-OrB dollops and plastic dispensers at least 60 m from the source. Additionally, SPLAT-OrB emitted pheromone that was attractive to male oriental beetles for >5 wk; however, emission rates and attraction dropped rapidly during the first 3-4 wk. This study demonstrates the feasibility of using SPLAT-OrB for oriental beetle mating disruption as an alternative to hand-applied plastic dispensers, and conclusively reveals that a principal mechanism is the competitive attraction of males.     

Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae)

In nature, larvae of the dung beetle Onthophagus taurus (Schreber 1759) are confronted with significant variation in the availability of food without the option of locating new resources. Here we explore how variation in feeding conditions during the final larval instar affects larval growth and the timing of pupation. We found that larvae respond to food deprivation with a reduction in the length of the instar and premature pupation, leading to the early eclosion of a small adult. To achieve pupation, larvae required access to food for at least the first 5 days of the final instar (= 30% of mean third‐instar duration in control individuals), and had to exceed a weight of 0.08 g (= 58% of mean peak weight in control individuals). Larvae that were allowed to feed longer exhibited higher pupation success, but increased larval weight at the time of food deprivation did not result in increased pupation success except for larvae weighing > 0.14 g. Larvae responded to food deprivation by initiating and undergoing the same sequence of developmental events, requiring the same amount of time, as ad libitum‐fed larvae once those had reached their natural peak weight. Our results reveal a striking degree of flexibility in the dynamics and timing of larval development in O. taurus. They also suggest that premature exhaustion of a larva's food supply can serve as a cue for the initiation of metamorphosis. Premature metamorphosis in response to food deprivation has been documented in amphibians, but this is, to the best of our knowledge, the first time such a behaviour has been documented for a holometabolous insect. We discuss our findings in the context of the natural history and behavioural ecology of onthophagine beetles.     

Conservation strategies for poorly surveyed taxa: a dung beetle (Coleoptera, Scarabaeidae) case study from southern Africa

Despite being the focus of an international research effort spanning decades, the spatial distribution of southern African scarab beetles remains poorly documented. As well as reinforcing the magnitude of the challenge facing biodiversity scientists, this raises real concerns about best practice conservation strategies in the absence of detailed distribution information. However, dung beetles appear to be well represented in established conservation areas. This apparent contradiction could be ascribed to anthropogenic transformation, successful conservation efforts, the presence of dung generalists and reserve-biased or mesic-biased dung beetle collection efforts. It is suggested that all of the above contribute to the observed pattern to varying degrees. The implications of selecting areas that are either rich in species, contain rare species or contain taxonomically distinct species from a group whose taxonomy is well known but for which inadequate distribution data exist are explored. Best practice, in the face of inadequate data, appears to revolve around a subtle interplay between advantages and disadvantages associated with data interpolation techniques, reserve selection algorithms that use criteria more robust than database rarity (such as taxonomic distinctiveness) and the long-term economic costs of proceeding with the data at hand versus investing in biological surveys.     

Nest construction, fighting, and larval behaviour in a geotrupine dung beetle, Ceratophyus hoffmannseggi (Coleoptera: Scarabaeidae)

A pair of beetles worked together to make a series of horizontal brood masses by packing dung into underground chambers. An egg was laid in the soil just beyond the tip of each mass. Resident beetles used their horns to resist intruders of either sex. During head-to-head pushing contests in the nest entrance-tunnel, a stable position was adopted where the horns of each opponent thrust harmlessly against the pronotum of the other. The larva prevented collapse of its chamber by building a rigid tube from accurately positioned faecal pellets. Defects in the larval chamber released no obvious repair behaviour and the larva was, therefore, not able to survive in a free-standing brood ball or in the presence of another larva in the same chamber.
It is a pleasure to thank Sr J. de Ferrer (8 Av. F. Franco, Algeciras) for his help and advice.     

Population genetic characterization of the endangered dung beetle Copris tripartitus (Coleoptera: Scarabaeidae) using novel microsatellite markers

The dung beetle Copris tripartitus (Coleoptera: Scarabaeidae) has long been considered an endangered insect in South Korea; the detection of recent population increases leaves its endangered status uncertain. Population genetic analysis subsequent to development of molecular markers is essential for establishing proper conservation strategies. In this study, we developed ten microsatellite markers specifically for C. tripartitus. Sixty-eight individuals of C. tripartitus collected from six South Korean localities were genotyped to validate these markers and preliminarily assess population genetic characteristics. Per-locus observed number of alleles, observed heterozygosity (H_O), and expected heterozygosity (H_E) ranged from 5–12, 0.499–0.958, and 0.54–0.743, respectively. All populations showed higher H_O than H_E, negative values of inbreeding coefficient, and, overall, no sign of recent population bottlenecks (excluding one population, Seosan). This suggests that C. tripartitus did not suffer from genetic drift and inbreeding, which are typically severe in small, isolated populations. Nevertheless, detection of only one of the two gene pools in some populations and resultant genetic subdivision into two population groups may suggest that the population size is not enough to cover both gene pools. Thus, a more extended period of protection may be required to ensure higher genetic diversity of widespread populations and achieve the long-term conservation goal.     

Thermoregulation in endothermic dung beetles (Coleoptera: Scarabaeidae): effect of body size and ecophysiological constraints in flight

We explore the physiological constraints of body temperature as related to body mass and ambient temperature during flight in endothermic dung beetles showing a mass-related breakpoint where species show strong vs. weak endothermy. We found two different strategies in the dung beetles prior to flight; larger beetles (>1.9 g) elevate and maintain their body temperature (T(b)) at levels well above ambient temperature (T(a)) whereas smaller beetles' (<1.9 g) T(b) tends to conform with T(a). Physiological constraints analysis revealed a constant maximum tolerated temperature (in flight) of 42 degrees C and a minimum temperature for flight of around 25 degrees C. These, with body mass, may play a role in thermal niche partitioning and geographical distribution patterns.     

Potential resistance of crape myrtle cultivars to flea beetle (Coleoptera: Chrysomelidae) and Japanese beetle (Coleoptera: Scarabaeidae) damage

Field and laboratory studies were conducted to identify potential resistance among crape myrtles, Lagerstroemia spp., to Japanese beetle, Popillia japonica Newman and to flea beetles, Altica spp. Damage ratings revealed variation among cultivars in susceptibility to beetle feeding. Cultivars with Lagerstroemia fauriei Koehne in their parentage exhibited the least amount of damage in choice and no-choice experiments, with few exceptions. The data indicate that both beetle species cause more feeding damage on certain cultivars of Lagerstroemia indica L., such as 'Country Red', 'Twilight', and 'Carolina Beauty' than interspecific cultivars with L. fauriei in their parentage, such as 'Natchez', 'Tonto', and 'Muskogee'. When comparing the effect of parentage on all of the major pests of crape myrtle, L. faurei confers resistance to all pests except crape myrtle aphid. No correlation was found between leaf toughness, leaf color, and leaf nutrients in estimating flea beetle cultivar preference. With this information, growers can more effectively target scouting measures to the most susceptible cultivars. and breeders can select plants that will require the fewest chemical inputs.     

Interactions between dung beetles (Coleoptera: Scarabaeidae) and the arbovirus vector Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae)

Abstract  The potential for dung beetles to reduce populations of the biting midge and arbovirus vector Culicoides brevitarsis in bovine dung was studied in the Hunter Valley, New South Wales (NSW) between 1999 and 2003 using natural populations of insects. Preliminary work to develop experimental procedures showed that: a few C. brevitarsis could survive in buried dung; dung beetles and C. brevitarsis coming to dung were unaffected by a background of shade-cloth used experimentally to prevent dung burial; the most abundant dung beetle, Onthophagus gazella L. and C. brevitarsis oviposition occurred concurrently in the first 2 d after dung deposition, and the potential for interaction between dung beetles and C. brevitarsis was greatest in open pasture adjacent to trees where cattle congregate at night. Laboratory experiments on dung burial showed that C. brevitarsis numbers decreased as numbers of dung beetles increased or as the dry weight of dung decreased due to burial. This was seldom reflected in the field where, although significant burial occurred experimentally in 9 of 20 trials over 3 years, a significant decline in C. brevitarsis numbers attributable to burial only occurred once. C. brevitarsis numbers in the field were lower in unburied dung in 70% of trials. Differences were significant twice and were considered the result of dung disturbance. In the laboratory, decreasing numbers of C. brevitarsis were related to three characteristics of disturbance: the flattening, spreading and reduction in wet weight of the dung. Evidence of C. brevitarsis activity throughout coastal NSW suggests that, while C. brevitarsis numbers may be modified by dung beetles, the interaction is insufficient to prevent their increase, spread and ability to transmit viruses to livestock.     

Genetic diversity of the dung beetle,Copris tripartitus (Coleoptera: Scarabaeidae), that is endangered in Korea

The dung beetle, Copris tripartitus (Coleoptera: Scarabaeidae), is an endangered insect in Korea. In order to establish a conservation strategy, a preliminary investigation on the genetic diversity of Korean populations was performed using mitochondrial COI (658 bp), CytB (433 bp), and nuclear ITS2 (411 nucleotide positions). Sequencing of 69 individuals collected from five localities showed substantially higher variability (5.02% for COI, 4.62% for CytB, and 8.03% for ITS2). The resulting networks for mitochondrial DNA (mtDNA) haplotypes exhibited two star‐like phylogenies, which might indicate that Korean populations have recently expended from two small populations. The ITS2 network, which was presented in the form of a star‐like phylogeny, confirmed that a recent population expansion occurred. Considering the high genetic diversity and gene flow in C. tripartitus populations, one issue regarding conservation seems to be the recovery of previous habitats.     

Structure and function of the mandibles of adult dung beetles (Coleoptera : Scarabaeidae)

The mouthparts of adult dung beetles (Coleoptera : Scarabaeidae) are adapted for manipulation of soft, pasty food—usually the excrement of vertebrates. Nutrients are derived primarily from micro-organisms contained in the food and these must be broken up before ingestion. The mandibles, particularly the molar lobes, are designed to finely grind these particulates; the molae function as a mortar-pestle system, which mills the organic “grist” contained in the food by a combination of squeezing and grinding actions. The ability of the molae to finely grind food particles resides primarily in the structure of the molar surface, which consists of a series of ridges bearing rows of submicroscopic scrapers (“tritors”). The incisor lobes of the mandibles scrape food from the surfaces of the galeae and lacinae, which bring food into the preoral cavity. The structure of the mouthparts of Canthon pilularius (L.), which is described in detail, is basically the same as that of 10 other species examined. Those of Aphodius and Geotrupes are similar in some respects to those of scarabaeines but are obviously less well specialized for microphagy.