The alternative Pharaoh approach: stingless bees mummify beetle parasites alive

Workers from social insect colonies use different defence strategies to combat invaders. Nevertheless, some parasitic species are able to bypass colony defences. In particular, some beetle nest invaders cannot be killed or removed by workers of social bees, thus creating the need for alternative social defence strategies to ensure colony survival. Here we show, using diagnostic radioentomology, that stingless bee workers (Trigona carbonaria) immediately mummify invading adult small hive beetles (Aethina tumida) alive by coating them with a mixture of resin, wax and mud, thereby preventing severe damage to the colony. In sharp contrast to the responses of honeybee and bumblebee colonies, the rapid live mummification strategy of T. carbonaria effectively prevents beetle advancements and removes their ability to reproduce. The convergent evolution of mummification in stingless bees and encapsulation in honeybees is another striking example of co-evolution between insect societies and their parasites.     

Prison construction and guarding behaviour by European honeybees is dependent on inmate small hive beetle density

Increasing small hive beetle (Aethina tumida Murray) density changes prison construction and guarding behaviour in European honeybees (Apis mellifera L.). These changes include more guard bees per imprisoned beetle and the construction of more beetle prisons at the higher beetle density. Despite this, the number of beetles per prison (inmate density) did not change. Beetles solicited food more actively at the higher density and at night. In response, guard bees increased their aggressive behaviour towards beetle prisoners but did not feed beetles more at the higher density. Only 5% of all beetles were found among the combs at the low density but this percentage increased five-fold at the higher one. Successful comb infiltration (and thus reproduction) by beetles is a possible explanation for the significant damage beetles cause to European honeybee colonies in the USA.     

Oviposition by small hive beetles elicits hygienic responses from Cape honeybees

Two novel behaviours, both adaptations of small hive beetles (Aethina tumida Murray) and Cape honeybees (Apis mellifera capensis Esch.), are described. Beetles puncture the sides of empty cells and oviposit under the pupae in adjoining cells. However, bees detect this ruse and remove infested brood (hygienic behaviour), even under such well-disguised conditions. Indeed, bees removed 91% of treatment brood (brood cells with punctured walls caused by beetles) but only 2% of control brood (brood not exposed to beetles). Only 91% of treatment brood actually contained beetle eggs; the data therefore suggest that bees remove only that brood containing beetle eggs and leave uninfected brood alone, even if beetles have accessed (but not oviposited on) the brood. Although this unique oviposition strategy by beetles appears both elusive and adaptive, Cape honeybees are able to detect and remove virtually all of the infested brood.     

A review of myrmecophily in ant nest beetles (Coleoptera: Carabidae: Paussinae): linking early observations with recent findings

Myrmecophily provides various examples of how social structures can be overcome to exploit vast and well-protected resources. Ant nest beetles (Paussinae) are particularly well suited for ecological and evolutionary considerations in the context of association with ants because life habits within the subfamily range from free-living and predatory in basal taxa to obligatory myrmecophily in derived Paussini. Adult Paussini are accepted in the ant society, although parasitising the colony by preying on ant brood. Host species mainly belong to the ant families Myrmicinae and Formicinae, but at least several paussine genera are not host-specific. Morphological adaptations, such as special glands and associated tufts of hair (trichomes), characterise Paussini as typical myrmecophiles and lead to two different strategical types of body shape: while certain Paussini rely on the protective type with less exposed extremities, other genera access ant colonies using glandular secretions and trichomes (symphile type). We compare these adaptations with other taxonomic groups of insects by joining contemporary research and early sources and discuss the possibility of an attracting or appeasing effect of the secretion. Species that are ignored by their host ants might use chemical mimicry instead. Furthermore, vibrational signals may contribute to ant–beetle communication, and chemical signals have proven to play a role in host finding. The powerful defense chemistry of paussines as “bombardier beetles” is not used in contact with host ants. We attempt to trace the evolution of myrmecophily in paussines by reviewing important aspects of the association between paussine beetles and ants, i.e. morphological and potential chemical adaptations, life cycle, host specificity, alimentation, parasitism and sound production.

Mortality of pollen beetle (Meligethes spp.) larvae due to predators and parasitoids in rape fields and the effect of conservation strips

In 1996–1999, different mortality factors of pollen beetle larvae were investigated in twenty six rape fields in the northern part of Switzerland which had either a wild flower strip or an extensively managed meadow adjacent to the long side of the field. At 3 and 30 m into the crop from the conservation strip, total mortality, mortality from predators, parasitoids and unspecified factors were measured. Total pollen beetle larval mortality was 66–96%. Mortality caused by predators was 16–27% and there was no significant difference between mortality at 3 m and that 30 m from the extensively managed meadows. However, in fields with wild flower strips adjacent to them, the percentage mortality from predators was significantly greater at 30 m than at 3 m. The range of parasitism of pollen beetle larvae was 0–54% and was on average greater at 3 m than at 30 m. In fields with wild flower strips, the percentage parasitism with Tersilochus heterocerus was significantly higher than in fields with extensively managed meadows. However, mortality from all parasitoids was only 1–2% and there was no significant difference between 3 and 30 m. The effect of parasitoids on pollen beetle mortality was masked by the high unspecified mortality and the mortality from predators. The unspecified mortality was 46–72% and was significantly greater in 1998 and 1999 than in 1996 and 1997. These differences are probably because of meteorological factors (wet in 1999 and dry in 1998). The possible influences of the two types of conservation strips on pollen beetle larval density were investigated. The results show that in fields with adjacent wild flower strips, the pollen beetle larvae were more evenly distributed (but not significantly so) than in fields with extensively managed meadows where larval density decreases faster from the edge into the rape field.     

Social encapsulation of beetle parasites by Cape honeybee colonies (Apis mellifera capensis Esch.)

Worker honeybees (Apis mellifera capensis) encapsulate the small hive beetle (Aethina tumida), a nest parasite, in propolis (tree resin collected by the bees). The encapsulation process lasts 1-4 days and the bees have a sophisticated guarding strategy for limiting the escape of beetles during encapsulation. Some encapsulated beetles died (4.9%) and a few escaped (1.6%). Encapsulation has probably evolved because the small hive beetle cannot easily be killed by the bees due to its hard exoskeleton and defensive behaviour.     

Molecular evidence of facultative intraguild predation by Monochamus titillator larvae (Coleoptera: Cerambycidae) on members of the southern pine beetle guild

The southern pine bark beetle guild (SPBG) is arguably the most destructive group of forest insects in the southeastern USA. This guild contains five species of bark beetles (Coleoptera: Curculionidae: Scolytinae): Dendroctonus frontalis, Dendroctonus terebrans, Ips avulsus, Ips calligraphus, and Ips grandicollis. A diverse community of illicit receivers is attracted to pheromones emitted by the SPBG, including the woodborers Monochamus carolinensis and Monochamus titillator (Coleoptera: Cerambycidae). These woodborers have been traditionally classified as resource competitors; however, laboratory assays suggest that larval M. carolinensis may be facultative intraguild predators of SPBG larvae. This study used polymerase chain reaction (PCR)-based molecular gut content analyses to characterize subcortical interactions between M. titillator and members of the SPBG. The half-lives of SPBG DNA were estimated in the laboratory prior to examining these interactions in the field. A total of 271 field-collected M. titillator larvae were analyzed and 26 (9.6?%) tested positive for DNA of members of the SPBG. Of these larvae, 25 (96.2?%) tested positive for I. grandicollis and one (3.8?%) for I. calligraphus. Failure to detect D. terebrans and D. frontalis was likely due to their absence in the field. I. avulsus was present, but primers developed using adult tissues failed to amplify larval tissue. Results from this study support the hypothesis that larval Monochamus spp. are facultative intraguild predators of bark beetle larvae. Additionally, this study demonstrates the capabilities of PCR in elucidating the interactions of cryptic forest insects and provides a tool to better understand mechanisms driving southern pine beetle guild population fluctuations.     

Role of post-dispersal seed and seedling predation in establishment of dandelion (Taraxacum agg.) plants

Dandelion Taraxacum agg. (formerly Taraxacum officinale G.H. Weber ex Wiggers) is a common weed species associated with pastures, grasslands and no-tillage cropping systems throughout its native range in Europe, and more recently introduced into North America, Australasia and elsewhere. Following wind-dispersal from the parent plant, its seeds are subject to predation from a host of invertebrate predators. Similarly, seedling predation may also significantly limit dandelion recruitment. Although such post-dispersal mortality is central to our understanding of dandelion population dynamics and therefore weed control, the precise spatio-temporal role played by different putative seed and seedling predators is poorly understood. Here we studied how seed viability, and seed and seedling predation influenced dandelion recruitment at two contrasting sites in central Europe. The abundance in the field and seed and seedling consumption in the laboratory were determined for the main groups of predators—ground beetles (Coleoptera: Carabiade), terrestrial isopods (Isopoda: Oniscidea) and molluscs (Gastopoda: Pulmonata). At particular sites, seed viability and seedling predation were negatively correlated while the percentage of seeds that succumbed to seed predation was similar. Combined factors accounted for the death of 98% and 87% of exposed seeds. Ground beetles (particularly Amara spp.) and terrestrial isopods (Armadillidium vulgare) were efficient and dominant seed predators, while slugs (Arion lusitanicus) and isopods were important predators of seedlings. While there was no seasonal trend in the intensity of seed predation it decreased towards autumn in parallel with the feeding activity of the declining population of A. lusitanicus. The mortality factors thus varied in their importance, largely between sites and less with the course of the season. Although seed inviability, seed and seedling predation did not stop the recruitment of dandelion seedlings they are crucial factors limiting dandelion populations. Methods of increasing the efficiency of predation of seed as a means of managing weeds are worthy of further study, particularly in areas where dandelion is an invasive species.     

Ecophysiology of dorsal versus ventral cuticle in flattened sawfly larvae

Platycampus larvae are highly cryptic leaf feeders characterised by a dorso-ventrally flattened body, the dorsal integument resembling a shield. Dorsal and ventral cuticles from Platycampus luridiventris were compared by histology and gel electrophoresis. By Azan-staining, a red and a blue layer were distinguished in the dorsal cuticle, while the ventral cuticle showed one, almost uniform blue layer, as in both cuticles of control species. The two cuticles from P. luridiventris had similar amounts and sodium dodecyl sulphate-polyacrylamide gel electrophoresis profiles of soluble proteins, but not insoluble proteins. One insoluble protein (MW ≈ 41 kDa) was visible as a large band in the ventral cuticle only. It is likely that this protein renders the cuticle elastic, and that the dorsal, red layer is the exocuticle, mainly composed of insoluble proteins. We discuss eco-physiological implications of the exocuticle in insects. Further, data from the literature indicate that the defence strategy in P. luridiventris larvae relies on being visually cryptic towards avian predators and tactically cryptic towards arthropod predators and parasitoids. Crypsis in both senses is favoured by the shield effect, itself based on an abnormally thick dorsal exocuticle. Although the larvae are external feeders, they may be considered as hidden from an ecological perspective.     

Strategies of a bark beetle, Pityogenes bidentatus, in an olfactory landscape

 Volatiles from leaves or bark of nonhost birch (Betula pendula) and Norway spruce (Picea abies) dramatically reduced the attraction of the bark beetle, Pityogenes bidentatus (Coleoptera: Scolytidae), to their aggregation pheromone components (cis-verbenol and grandisol) in the field. In addition, odors from both the needles and bark of the host Scots pine (Pinus sylvestris) similarly inhibited attraction. Monoterpenes of pine and spruce (α-pinene, β-pinene, terpinolene, and 3-carene) as well as ethanol, chalcogran and some nonhost green leaf alcohols [(Z)-3-hexen-1-ol, (E)-2-hexen-1-ol, and 1-hexanol], also reduced catches. Collections of volatiles from the field-tested plant tissues indicated they released monoterpenes in amounts similar to the synthetics that inhibited responses. The various plant and insect sources of these inhibitory compounds indicate that P. bidentatus bark beetles have evolved several strategies to increase their fitness by avoiding nonhost and unsuitable host trees in a complex olfactory landscape. Received: 6 June 2000 / Accepted in revised form: 25 September 2000     

Small hive beetles survive in honeybee prisons by behavioural mimicry

We report the results of a simple experiment to determine whether honeybees feed their small hive beetle nest parasites. Honeybees incarcerate the beetles in cells constructed of plant resins and continually guard them. The longevity of incarcerated beetles greatly exceeds their metabolic reserves. We show that survival of small hive beetles derives from behavioural mimicry by which the beetles induce the bees to feed them trophallactically. Electronic supplementary material to this paper can be obtained by using the Springer LINK server located at htpp://dx.doi.org/10.1007/s00114-002-0326-y.     

Post-dispersal weed seed predation by avian and non-avian predators

Seed predation by avian and non-avian predators was quantified in the boundaries and cropped areas of cereal fields by presenting known quantities of seed with and without exclusion cages. Predator encounter-rates with the dishes exceeded 99%. Birds removed on average 6.7% seed from the dishes during the seven-day trials compared to 51% by non-avian predators. A comparison was made of the causal factors responsible for predation of Avena fatua, Chenopodium album and Cirsium arvense seeds. A. fatua seeds were preyed most heavily by both avian and non-avian predators. Seed removal by birds was greater in the cropped area than in the field boundary, non-avian predators being generally more active in the field boundary. Seed predation by birds was greater in spring than in any other season, whilst losses to other animals were greater during autumn and winter. Although, birds were not the main seed predators in cereal fields, they may contribute to weed seed depletion, of relevance to reduced-input farming systems where herbicides use is restricted.     

Prey-rolling behavior of coatis (Nasua spp.) is elicited by benzoquinones from millipedes

Coatis (Nasua spp.), gregarious, omnivorous carnivores that range in forests from the southwestern USA to south America, dispatch millipedes by rolling them on the ground using rapid, alternating movements of their forepaws. Prey rolling of millipedes is thought to stimulate the depletion of their defensive secretions and to wipe off secretions before millipedes are consumed. We report that prey-rolling behavior in Nasua spp. is elicited by 1,4-benzoquinone; 2-methyl-1,4-benzoquinone; and 2-methoxy-3-methyl-1,4-benzoquinone, the chief components of the defensive secretions of julidan, spirobolidan, and spirostreptidan millipedes. Chemicals elaborated for defense sometimes evolutionarily “backfire,” providing cues to predators on the presence or identity of prey. The elicitation of prey-rolling behavior in Nasua spp. by benzoquinones illustrates this effect for millipedes (and possibly other arthropods) that defensively discharge these compounds.     

Avoidance of nonhost plants by a bark beetle, Pityogenes bidentatus, in a forest of odors

The bark beetle, Pityogenes bidentatus (Coleoptera: Scolytidae), searches in mixed conifer and deciduous forests of northern Europe for suitable branches of its host, Scots pine (Pinus sylvestris). We tested whether odors from several diverse nonhost trees and plants common in the habitat (e.g., mountain ash, Sorbus aucuparia; oak, Quercus robur; alder buckthorn, Frangula alnus; blueberry, Vaccinium myrtillus; raspberry, Rubus idaeus; and grass, Deschampsia flexuosa) would reduce the attraction of the bark beetle to traps releasing its aggregation pheromone components in the field. Volatiles from the leaves or bark of each of these plants significantly reduced the attraction of the beetles to their pheromone. Odors collected from these nonhosts and analyzed by GC/MS contained monoterpenes, sesquiterpenes, and green-leaf alcohols, several of which (e.g., 1-octene-3-ol and -caryophyllene) reduced the attraction to pheromone in the field and elicited electroantennographic responses. In the laboratory, reproduction by the beetle was marginal in nonhost Norway spruce, Picea abies, and was absent in the other nonhost trees. Olfactory avoidance of unsuitable nonhosts may have evolved due to advantages in avoiding mistakes during host selection.     

A behavioral study of the beetle Tenebrio molitor infected with cysticercoids of the rat tapeworm Hymenolepis diminuta

The host–parasite relationship, Tenebrio molitor–Hymenolepis diminuta, was analyzed. The learning behavior of infected and uninfected (control) beetles in a T-maze was compared. The infected beetles moved much slower in the T-maze than the controls. The infected beetles reached the same level of learning as the controls. However, they needed more trials than the controls. The effect of the infection was already distinct after the first week and even higher after the second week. This indicates that the initial phase of infection caused stress in the beetles. Longer infection did not worsen their ability to learn. Thus, the parasites clearly changed the behavior of their intermediate host and probably made them more susceptible to their final host, the rat.     

Is naïveté forever? Alien predator and aggressor recognition by two endemic island reptiles

The disproportionate impacts of invasive predators are often attributed to the naïveté (i.e., inefficient or non-existing anti-predator behavior) of island native species having evolved without such predators. Naïveté has long been regarded as a fixed characteristic, but a few recent studies indicate a capacity for behavioral adaptation in native species in contact with alien predators. Here, we tested whether two reptiles endemic to New Caledonia, a skink, Caledoniscincus austrocaledonicus, and a gecko, Bavayia septuiclavis, recognized and responded to the odor of six introduced species (two rodents, the feral cat, and three species of ants). We used an experimental design in which reptiles had a choice of retreat sites with or without the odor of predators or aggressors. Skinks avoided two or three of the predators, whereas geckos avoided at most one. These results suggest that diurnal skinks are more responsive than nocturnal geckos to the odor of introduced predators. Neither skinks nor geckos avoided the three species of ants. Thus, the odors of alien predators are shown to influence retreat site selection by two native island reptiles. Moreover, the study suggests that this loss of naïveté varies among native species, probably as a consequence of the intensity of the threat and of time since introduction. These findings argue for re-thinking the behavioral flexibility of ectothermic reptiles in terms of their responses to biological invasion.     

A male gift to its partner? Cyanogenic glycosides in the spermatophore of longwing butterflies (<Emphasis Type="Italic">Heliconius</Emphasis>)

Males of several insect species transfer nuptial gifts to females during mating, typically in the form of a protein-rich spermatophore. In chemically defended species, males could potentially enhance such a gift with chemicals that help protect the female, her eggs, or both. This was shown for lepidopteran species that accumulate pyrrolizidine alkaloids. Most Heliconius butterflies are presumably protected from predators by virtue of de novo synthesized and/or sequestered cyanogenic glycosides. Males of Heliconius species are known to transfer nutritional gifts to the females but whether defensive chemicals could also be transferred is not known. To ascertain whether transfer of cyanogens occurs, we dissected freshly mated females from nine different Heliconius species and analyzed spermatophores for cyanogenic glycosides. We found cyanogens in the spermatophores of all nine species. This is the first time cyanogenic glycosides are reported in the spermatophores of arthropods. We discuss the implications of these findings for Heliconius biology and for other cyanogenic insects as well. We suggest that chemically defended species commonly lace their nuptial gifts with defensive chemicals to improve gift quality.     

Do mites phoretic on elm bark beetles contribute to the transmission of Dutch elm disease?

Dutch elm disease (DED) is a destructive vascular wilt disease of elm (Ulmus) trees caused by the introduced Ascomycete fungus Ophiostoma novo-ulmi. In Europe, this DED pathogen is transmitted by elm bark beetles in the genus Scolytus. These insects carry phoretic mites to new, suitable habitats. The aim of this study was to record and quantify conidia and ascospores of O. novo-ulmi on phoretic mites on the three elm bark beetle species Scolytus multistriatus, Scolytus pygmaeus, and Scolytus scolytus. Spores of O. novo-ulmi were found on four of the ten mite species phoretic on Scolytus spp. These included Elattoma fraxini, Proctolaelaps scolyti, Pseudotarsonemoides eccoptogasteri, and Tarsonemus crassus. All four species had spores attached externally to their body surfaces. However, T. crassus carried most spores within its sporothecae, two paired pocket-like structures adapted for fungal transmission. Individuals of Pr. scolyti also had O. novo-ulmi conidia and ascospores frequently in their digestive system, where they may remain viable. While E. fraxini and P. eccoptogasteri rarely had spores attached to their bodies, large portions of Pr. scolyti and T. crassus carried significant numbers of conidia and/or ascospores of O. novo-ulmi. P. scolyti and T. crassus, which likely are fungivores, may thus contribute to the transmission of O. novo-ulmi, by increasing the spore loads of individual Scolytus beetles during their maturation feeding on twigs of healthy elm trees, enhancing the chance for successful infection with the pathogen. Only S. scolytus, which is the most efficient vector of O. novo-ulmi in Europe, carried high numbers of Pr. scolyti and T. crassus, in contrast to S. multistriatus and S. pygmaeus, which are known as less efficient vectors. The high efficiency of S. scolytus in spreading Dutch elm disease may be partly due to its association with these two mites and the hyperphoretic spores of O. novo-ulmi they carry.     

Irresistible bouquet of death—how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses

Chemical composition of volatiles emitted from fresh mouse carcasses (laboratory mice, Mus musculus) was studied using solid sample injection technique (solid-phase micro-extraction), two-dimensional gas chromatography with time of flight mass spectrometric detection and gas chromatography with electroantennographic detection. Electroantennography (EAG) and laboratory olfactometric behavioural observations were used to study the antennal sensitivity to identified infochemicals and their attractiveness for burying beetles Nicrophorus vespillo and Nicrophorus vespilloides (Silphidae: Nicrophorinae). Chemical analysis showed that immediately after death, emitted volatiles did not differ from those emitted by a living organism. However, in the course of time, sulphur-containing chemicals, specifically methanethiol, methyl thiolacetate, dimethyl sulphide, dimethyl disulphide and dimethyl trisulphide appear. EAG measurements revealed antennal sensitivity to these compounds. Behavioural tests in laboratory olfactometer showed that dimethyl sulphide, dimethyl disulphide and dimethyl trisulphide are highly attractive to both studied species. The data suggest that sulphur-containing chemicals are involved in mediating the fresh carcass attractiveness for N. vespillo and N. vespilloides.     

A new type of infrared organ in the Australian "fire-beetle" Merimna atrata (Coleoptera: Buprestidae)

 The Australian buprestid beetle Merimna atrata (Coleoptera: Buprestidae) approaches forest fires because its larvae develop in freshly burnt wood. So far nothing is known about possible sensory systems enabling the beetles to detect fires and to cope with the thermal environment close to the flames. We found that M. atrata has two pairs of infrared (IR) organs on the ventrolateral sides of the abdomen. Each IR organ consists of a specialized IR-absorbing area which is innervated by one thermosensitive multipolar neuron. The primary dendritic branches ramify into more than 800 closely packed terminal endings which contain a large number of mitochondria. We called the special morphology of the dendritic region a terminal dendritic mass. The type of IR receptor found in M. atrata is unique in insects and can best be compared with the IR organs of boid snakes. Received: 14 August 2000 / Accepted in revised form: 18 October 2000