Two new species from the Mexican Pacific Slope and new distributional records of Onthophagus Latreille, 1802 (Coleoptera,Scarabaeidae)

Two new species of Onthophagus Latreille, 1802 from the Pacific Slope of Mexico are described and illustrated: Onthophagus gonzaloi Moctezuma, Hernández & Sánchez-Huerta, sp. nov., and Onthophagus yescaensis Moctezuma, Hernández & Sánchez-Huerta, sp. nov. New records for Onthophagus browni Howden & Cartwright, 1963 from the Mexican states of Jalisco (the southernmost locality known to date) and Zacatecas are provided.urn:lsid:zoobank.org:pub:51AA52C6-41BF-4A8B-9BC9-D78600EDB32E.     

Effect of Density and Extra Dung on Brood Parasitism in the Dung Beetle, Onthophagus Taurus

Kleptoparasitism has not been well documented in insects and intraspecific brood parasitism is even less well known. This study examines the effect of extra resources and density on the probability of kleptoparasitism in the bull headed dung beetle Onthophagus taurus. A high level (>60 %) of kleptoparasitism was found across all treatments and suggest that although density may not affect the probability to kleptoparasitize, it may influence brood ball production. This study also documents for the first time that male O. taurus kleptoparasitize.     

Brood Ball-Mediated Transmission of Microbiome Members in the Dung Beetle,Onthophagus taurus (Coleoptera: Scarabaeidae)

Insects feeding on plant sap, blood, and other nutritionally incomplete diets are typically associated with mutualistic bacteria that supplement missing nutrients. Herbivorous mammal dung contains more than 86% cellulose and lacks amino acids essential for insect development and reproduction. Yet one of the most ecologically necessary and evolutionarily successful groups of beetles, the dung beetles (Scarabaeinae) feeds primarily, or exclusively, on dung. These associations suggest that dung beetles may benefit from mutualistic bacteria that provide nutrients missing from dung. The nesting behaviors of the female parent and the feeding behaviors of the larvae suggest that a microbiome could be vertically transmitted from the parental female to her offspring through the brood ball. Using sterile rearing and a combination of molecular and culture-based techniques, we examine transmission of the microbiome in the bull-headed dung beetle, Onthophagus taurus. Beetles were reared on autoclaved dung and the microbiome was characterized across development. A ~1425 bp region of the 16S rRNA identified Pseudomonadaceae, Enterobacteriaceae, and Comamonadaceae as the most common bacterial families across all life stages and populations, including cultured isolates from the 3^rd instar digestive system. Finer level phylotyping analyses based on lepA and gyrB amplicons of cultured isolates placed the isolates closest to Enterobacter cloacae, Providencia stuartii, Pusillimonas sp., Pedobacter heparinus, and Lysinibacillus sphaericus. Scanning electron micrographs of brood balls constructed from sterile dung reveals secretions and microbes only in the chamber the female prepares for the egg. The use of autoclaved dung for rearing, the presence of microbes in the brood ball and offspring, and identical 16S rRNA sequences in both parent and offspring suggests that the O. taurus female parent transmits specific microbiome members to her offspring through the brood chamber. The transmission of the dung beetle microbiome highlights the maintenance and likely importance of this newly-characterized bacterial community.     

A reappraisal of the 'fracticornis–opacicollis' taxonomic complex of the genus Onthophagus Latreille using allozymes (Coleoptera, Scarabaeoidea)

The present taxonomic status of the so called fracticornis–opacicollis complex of the genus Onthophagus , Onthophagus fracticornis (Preyssler, 1790), Onthophagus similis (Scriba, 1790) and Onthophagus opacicollis Reitter, 1892 is still controversial. Discrepancies mainly involve the status of O. similis and O. opacicollis . A genetic analysis of nine populations of this complex using eight loci is presented, indicating that: (i) O. fracticornis is a good species, and (ii) the genetic distances between O. opacicollis and O. similis populations as a function of the biogeographic scenery (allopatry versus sympatry), indicate that they are not completely reproductively isolated across their entire geographic range, thus suggesting a still unfinished speciation in different areas. The data demonstrate both the existence of some gene flow between O. opacicollis and O. similis in one place ('El Barraco'; Central Spain) and isolation in others ('S^a Nevada'; South-east Spain). Geographic areas hosting populations of both taxa with intermediate genetic distances ('Doñana'; South-west Spain) also exist in the Iberian Peninsula.     

Combination of geometric morphometric and genetic approaches applied to a debated taxonomical issue: the status of Onthophagus massai (Coleoptera, Scarabaeidae) as an endemic species vicarious to Onthophagus fracticornis in Sicily

The present study deals with the phenomenon of insular speciation and discusses, as a case study, the debated taxonomical issue of the status of Onthophagus massai (Coleoptera, Sarabaeidae) as an endemic species vicarious to Onthophagus fracticornis in Sicily. The authors investigated the differentiation patterns between an insular population belonging to the supposed species O. massai (collected in its locus typicus, Piano Battaglia) and three Italian O. fracticornis populations (collected along a N–S latitudinal gradient). These patterns are described and analysed using multiple approaches: the qualitative inspection of the microsculpture of elytral surfaces, considered a diagnostic character for O. massai identification; the comparison of horn static allometries, known to be a good indicator of divergence processes between closely related species or isolated populations of the same species; the comparison of the patterns of shape and size difference of the head, epipharynx and genitalia attained with a combination of traditional and geometric (landmark and semilandmark) morphometric methods; and, finally, the estimation of the genetic relationships between Sicilian and continental populations obtained by analysing cytochrome oxidase subunit 1 mitochondrial gene sequences. The integration of the results of these approaches indicates that there is not sufficient evidence to vindicate the species status for O. massai, which should more likely be considered a small-sized version of O. fracticornis (a possible case of insular dwarfism). However, the complex pattern of shape, size and genetic variation observed between the populations analysed hinted at the possibility that a diversification process is ongoing, but not only between insular and continental populations; each population showed a tendency to evolve as an evolutionarily independent unit.     

Sub-lethal effects of moxidectin on the Neotropical dung beetle Onthophagus landolti Harold (Coleoptera: Scarabaeinae)

Macrocyclic lactones can have adverse effects in dung beetles exposed to manure containing them. An assessment of the survival and fertility of adult Onthophagus landolti Harold fed with manure from cows treated with moxidectin was performed, as well as the emergence rate of the imagoes from the masses. Three cows (Bos indicus x B. taurus) were subcutaneously injected with 1% moxidectin (0.2 mg kg^?1 b.w.) and another three were injected with 10% moxidectin (1.0 mg/kg^?1 b.w.). Manure was collected from these animals one day prior to moxidectin administration, five days post-treatment in the 1% and 10% treatments, and fourteen days in the 10% treatment. Four bioassays were done: a control using manure without moxidectin; 1% moxidectin at five days post-treatment; 10% moxidectin at five days post-treatment; and 10% moxidectin at fourteen days post-treatment. In each replicate, for each pair of adult O. landolti was daily fed with 30 g manure according to the treatments. No lethal effects were observed in any of the four treatments. Sub-lethal effects (P < .05) were present in the 10% moxidectin treatments at five and fourteen days post-treatment. Fecundity was reduced by 78.2% at five days and 54.9% at fourteen days, and imago emergence was negatively affected at both times. Current moxidectin application methods may have negative effects on the environmental services provided by dung beetles, and therefore need to be modified to minimize any impacts they might have on these vital members of tropical livestock systems.     

Size and shape interspecific divergence patterns partly reflect phylogeny in an Onthophagus species‐complex (Coleoptera: Scarabaeidae)

Polyphenism has been suggested as an accelerator for morphological evolution and speciation. In the dung beetles of the genus Onthophagus, horn expression is polyphenic: large males develop horns whereas smaller males express greatly reduced or no horns. Horn static allometries seem to diverge rapidly amongst extant taxa, a process which might trigger changes in the male genital morphology, thus possibly promoting speciation as a by‐product. It can therefore be hypothesized that interspecific distances in allometries and, possibly, in other morphological traits mirror phylogenetic distances. In this study we first assessed the phylogenetic relationships amongst three closely related taxa belonging to the so‐called ‘Onthophagus fracticornis‐similis‐opacicollis’ species‐complex by sequencing the mitochondrial gene cytochrome oxidase subunit 1 (cox1). Biomolecular results indicated three independent lineages, the closest relationships being found between Onthophagus similis and Onthophagus opacicollis. Then we assessed the extent to which divergence pattern of horn static allometries and size and shape divergence patterns of one genital (paramere) and two nongenital (head and epipharynx) structures mirrored the phylogenetic relationships. Interspecific divergence patterns of horn static allometries, paramere, and head shape were found to be congruent with the evolutionary relationships inferred from biomolecular data. Nevertheless, paramere size and epipharynx shape showed patterns not consistent with the phylogeny. Furthermore, the relative size of nongenital structures showed little interspecific divergence compared to their shapes. Our results suggest that size and shape interspecific divergence mirror phylogeny only in part; they also indicate that distinct morphological traits may differ in their tendency to evolve in concert, and that size and shape of the same trait can evolve independently across species. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 162 , 482–498.     

Genetic and morphological differentiation patterns between sister species: the case of Onthophagus taurus and Onthophagus illyricus (Coleoptera, Scarabaeidae)

The present study investigated the morphological and genetic differentiation pattern between two sympatric dung beetle sister species, Onthophagus taurus and Onthophagus illyricus . The geometric morphometric approach coupled with the use of molecular markers allowed examination of the nature of interspecific relationships and an outline of the evolutionary and geographical processes that might have led to interspecific differentiation and the present-day partial sympatric and syntopic pattern of distribution. Geometric morphometrics failed to discrimininate the two species on the ground of external morphological traits, but revealed interspecific differences when the shape of the primary sexual traits was taken into account. The use of two different molecular markers (cytochrome oxidase subunit I gene and amplified fragment-length polymorphism) demonstrates that the two species are genetically well differentiated, forming two distinguishable lineages probably diverged during the Pliocene by allopatric speciation. No evidence of past or recent introgression and no support for hybridization were found, suggesting that sympatry was established subsequently, when speciation was accomplished. Both molecular markers and genital shape indicate that phenotypically intermediate individuals, despite their ambiguous appearance, are members of O. illyricus species rather than hybrids.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 197–211.     

Taxonomy of new relatives of Onthophagus?catenatus Lansberge, 1883 from New Guinea (Coleoptera,?Scarabaeidae,Scarabaeinae)

Four new taxa from New Guinea are proposed in the dung beetle genus Onthophagus Latreille, 1802, all in the operational group of Onthophagus catenatus Lansberge, 1883. The group is discussed, defined, and the five taxa included are listed, keyed, and diagnosed. Three new species are described: Onthophagus abmisibilus (from West New Guinea, Indonesia), Onthophagus kokodanus, Onthophagus kokosquamatus (both from Papua New Guinea). One new species comprises a lowland and an upland subspecies: Onthophagus kokodanus kokodanus and kokodanus hagenaltus (both in Papua New Guinea).     

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.

     

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.

     

Revised classification and phylogeny of an Afrotropical species group based on molecular and morphological data,with the description of a new genus (Coleoptera: Scarabaeidae: Onthophagini)

The worldwide distributed Onthophagus genus comprises at present more than 2000 species, that often show a complicated and uncertain systematic history. In particular, the many Afrotropical species included in this genus have never been entirely reviewed after the division into 32 species groups proposed by d’Orbigny in 1913, although subsequent researches focusing on some of these species suggested that Onthophagus constituted a nonmonophyletic taxon. In order to highlight their phylogenetic relationships, the various Afrotropical species groups of d’Orbigny must thus be examined, and it would be advisable to study them separately to avoid misunderstanding. In this framework, the taxonomic position of the three species currently included in the 21st d’Orbigny group was examined. Both morphological and biomolecular analyses contributed in confirming that these species (i.e., Onthophagus caffrarius d’Orbigny, 1902; Onthophagus quadraticeps Harold, 1867; and Onthophagus signatus Fåhraeus, 1857) constituted a well-defined monophyletic group that cannot be maintained within the genus Onthophagus. Therefore, the Kurtops gen.n. is here described to accommodate these Afrotropical species, that are nevertheless always included within the Onthophagini tribe. On the basis of the phylogenetic relationships here elucidated, it was also emphasized that the new genus is strictly related to Digitonthophagus and Phalops; thus, it was proposed to include the three genera into a single clade of suprageneric rank naming it as Phalops complex.     

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.     

Adjustment of Parental Investment in the Dung Beetle Onthophagus atripennis (Col., Scarabaeidae)

If parents can invest resources optimally per offspring, they should adjust the amount of investment in an offspring according to environmental heterogeneity. Many studies have demonstrated changes in egg size or the amount of resource supplied in response to environmental heterogeneity. However, it remains unclear whether parents simply know the resource type a priori or can assess resource quality and adjust the quantity of investment accordingly. We examined the parental capability to adjust the amount of investment per offspring by providing Onthophagus atripennis dung beetle parents with one of three dung types of different quality: monkey dung (high quality), cow dung (low quality), or a mixture of monkey and cow dung (medium quality). The beetle parents cooperatively produce dung brood masses each with one egg under the ground. The size of a brood mass, on which a larva can only feed until adult, represents a large part of the amount of investment. Parents produced a greater number of smaller brood masses given high‐quality resource, while they compensated for low quality of the resource by providing a larger amount of the resource, at the cost of offspring number. However, despite this compensation in the amount of food, offspring raised on low‐quality food was still smaller than offspring raised on high‐quality food. Thus, O. atripennis parents assessed resource quality partly and adjusted the amount of resource provided for their offspring.     

Male dimorphism in three sympatric species of Onthophagus (Coleoptera: Scarabaeidae)

Onthophagus trituber, O. taurinus, and O. proletarius, three sympatric dung beetle species native to southern Taiwan, exhibit normally distributed body size (pronotum width) but non-normally distributed horn length due to the presence of horned and hornless morphs. The scaling relationships between horn length and body size were established by using sigmoidal and segmented linear estimation, and the horned/hornless ratio in each of the species was estimated. The ratios estimated by sigmoidal curves showed that all three species were biased toward the hornless morph, whereas the ratios from segmented lines showed that only one species (O. taurinus) was biased toward the hornless morph. Nevertheless, the results of the two methods of estimation were concordant in ranking the horned morph proportions among the three species; O. proletarius had the largest proportion of horned morphs, whereas O. taurinus had the smallest, suggesting that the fewer horned morph in O. taurinus likely resulted from both intra- and inter-specific competition.     

Male morph predicts investment in larval immune function in the dung beetle, Onthophagus taurus

Investment in immunity is costly, so that resource-based trade-offsbetween immunity and sexually selected ornaments might be expected.The amount of resources that an individual can invest in eachtrait will be limited by the total resources available to them.It would therefore be informative to investigate how investmentin immune function changes during growth or production of thesexual trait as resources are diverted to it. Using the dungbeetle, Onthophagus taurus, which displays both sexual and maledimorphism in horn size, we examined changes in one measureof immune function, phenoloxidase (PO) activity, in the hemolymphof larvae prior to and during horn growth. We found that POlevels differed between small- and large-horned males throughoutthe final instar prior to the point where investment in horngrowth was taking place. PO levels in females were intermediateto the 2 male morphs. These differences could not be accountedfor by differences in condition, measured as hemolymph proteinlevels and weight. We suggest that the observed differencesmight be associated with sex- and morph-specific variation injuvenile hormone levels.     

Game theoretic model of brood parasitism in a dung beetle Onthophagus taurus

We present a game theoretic model of brood parasitism in the dung beetle Onthophagus taurus. Female O. taurus engage in brood parasitism when they attack a brood ball made by another female, destroy the existing egg and place one of their own eggs to develop within the existing dung ball. Brood parasitism is more costly than other forms of kleptoparasitism because an individual loses the total investment in an offspring. In this paper, we outline the behaviors involved in brood ball production and provide time estimates of those behaviors. The model is then used to predict when it is beneficial to steal the brood ball created by another female and when it is beneficial for a female to create her own. We also investigate how long a female should guard her eggs.     

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.     

Male differentiation patterns in two polyphenic sister species of the genus Onthophagus Latreille, 1802 (Coleoptera: Scarabaeidae): a geometric morphometric approach

This paper focuses on morphological (both shape and size ) differences that quite similar polyphenic sister species evolve during divergence processes. Traits were analysed using a geometrical morphometric approach, which has the ability to evidence also very subtle differences in shape. As a case study, we considered males of the dung beetle sister species pair Onthophagus taurus and Onthophagus illyricus (Coleoptera, Scarabaeidae); these species represent a typical example of polyphenic trait expression concerning the facultative development of horns and considerable body size differences. External shape morphology failed to discriminate O. taurus from O. illyricus , whereas the reproductive system shape showed significant interspecific discrimination power. However, the head of O. taurus was significantly larger than that of O. illyricus and the reverse was true for the elytra. The two species also showed different allometric values of the head with respect to body size. This complex pattern of interspecific morphological divergence is discussed in the light of the differential trait divergence rate hypothesis. In both species, differences between major and minor forms concern the overall shape of head and pronotum: we suggest that such different forms, which likely reflect morphological readjustment to accommodate horns of considerable bulk and disproportionate length, may be nevertheless advantageously used by the two male morphs in their alternative reproductive tactics. Male genitalia sizes were virtually constant with respect to body size; however, the ratio between phallotheca and body size was significantly higher in minor males, in keeping with the hypothesis of a higher investment in genitalia borne by this morph.