The hunter becomes the hunted: when cleptobiotic insects are captured by their target ants

Here we show that trying to rob prey (cleptobiosis) from a highly specialized predatory ant species is risky. To capture prey, Allomerus decemarticulatus workers build gallery-shaped traps on the stems of their associated myrmecophyte, Hirtella physophora. We wondered whether the frequent presence of immobilized prey on the trap attracted flying cleptoparasites. Nine social wasp species nest in the H. physophora foliage; of the six species studied, only Angiopolybia pallens rob prey from Allomerus colonies. For those H. physophora not sheltering wasps, we noted cleptobiosis by stingless bees (Trigona), social wasps (A. pallens and five Agelaia species), assassin bugs (Reduviidae), and flies. A relationship between the size of the robbers and their rate of capture by ambushing Allomerus workers was established for social wasps; small wasps were easily captured, while the largest never were. Reduviids, which are slow to extract their rostrum from prey, were always captured, while Trigona and flies often escaped. The balance sheet for the ants was positive vis-à-vis the reduviids and four out of the six social wasp species. For the latter, wasps began by cutting up parts of the prey’s abdomen and were captured (or abandoned the prey) before the entire abdomen was retrieved so that the total weight of the captured wasps exceeded that of the prey abdomens. For A. pallens, we show that the number of individuals captured during attempts at cleptobiosis increases with the size of the Allomerus’ prey.     

Male fighting and “territoriality” within colonies of the ant Cardiocondyla venustula

The ant genus Cardiocondyla is characterized by a bizarre male polymorphism with wingless fighter males and winged disperser males. Winged males have been lost convergently in several clades, and in at least one of them, wingless males have evolved mutual tolerance. To better understand the evolutionary pathways of reproductive tactics, we investigated Cardiocondyla venustula, a species, which in a phylogenetic analysis clusters with species with fighting and species with mutually tolerant, wingless males. Wingless males of C. venustula use their strong mandibles to kill freshly eclosed rival males and also engage in short fights with other adult males, but in addition show a novel behavior hitherto not reported from social insect males: they spread out in the natal nest and defend “territories” against other males. Ant males therefore show a much larger variety of reproductive tactics than previously assumed.     

The potential to encode sex,age, and individual identity in the alarm calls of three species of Marmotinae

In addition to encoding referential information and information about the sender’s motivation, mammalian alarm calls may encode information about other attributes of the sender, providing the potential for recognition among kin, mates, and neighbors. Here, we examined 96 speckled ground squirrels (Spermophilus suslicus), 100 yellow ground squirrels (Spermophilus fulvus) and 85 yellow-bellied marmots (Marmota flaviventris) to determine whether their alarm calls differed between species in their ability to encode information about the caller’s sex, age, and identity. Alarm calls were elicited by approaching individually identified animals in live-traps. We assume this experimental design modeled a naturally occurring predatory event, when receivers should acquire information about attributes of a caller from a single bout of alarm calls. In each species, variation that allows identification of the caller’s identity was greater than variation allowing identification of age or sex. We discuss these results in relation to each species’ biology and sociality.     

Queue up, please! Spermathecal filling in the rove beetle Drusilla canaliculata (Coleoptera, Staphylinidae)

Most studies on insect sperm motility have been conducted in vitro using artificial environments outside the animal’s body. Only little is known about the function of motile insect sperm at different sites within the male or female genital tracts. We dissected genital tracts of female rove beetles (Drusilla canaliculata) to show that spermatozoa use their own motility to migrate from the spermatophore into the spermatheca. Our dissection method allowed direct observation and filming of the spermathecal filling process inside the female’s genital tract. Spermatozoa were found to enter the spermatheca individually, sometimes in groups of two or three. Although exhibiting only weak motility and no progressive motion in buffer solution, the spermatozoa inside the female show vigorous lashing and reach an average velocity of 47.5 μm s⁻¹. To gain mobility and speed, the spermatozoa likely utilize the relatively small diameter of the spermathecal duct to push themselves off the duct walls, rather than swimming freely in seminal fluid. The spermatozoa (approximately 1,250 μm) are considerably longer than the distance they have to travel along the spermathecal duct (approximately 800 μm). Our study provides the first direct observation of active sperm migration within the female of an insect stressing the importance of the genital tract as a prerequisite for functional sperm motility.     

Visual targeting of components of floral colour patterns in flower-naïve bumblebees (Bombus terrestris; Apidae)

Floral colour patterns are contrasting colour patches on flowers, a part of the signalling apparatus that was considered to display shape and colour signals used by flower-visitors to detect flowers and locate the site of floral reward. Here, we show that flower-naïve bumblebees (Bombus terrestris) spontaneously direct their approach towards the outside margin of artificial flowers, which provides contrast between these dummy flowers and the background. If no floral guides are present, the bumblebees continue to approach the margin and finally touch the marginal area of the dummy flower with the tips of their antennae. Whilst approaching dummy flowers that also have a central floral guide, the bumblebees change their direction of flight: Initially, they approach the margin, later they switch to approaching the colour guide, and finally they precisely touch the floral guide with their antennae. Variation of the shape of equally sized dummy flowers did not alter the bumblebees’ preferential orientation towards the guide. Using reciprocal combinations of guide colour and surrounding colour, we showed that the approach from a distance towards the corolla and the antennal contact with the guide are elicited by the same colour parameter: spectral purity. As a consequence, the dummy flowers eliciting the greatest frequency of antennal reactions at the guide are those that combine a floral guide of high spectral purity with a corolla of less spectral purity. Our results support the hypothesis that floral guides direct bumblebees’ approaches to the site of first contact with the flower, which is achieved by the tips of the antennae.Electronic Supplementary Material  Supplementary material is available for this article at     

Is body size of the water frog Rana esculenta complex responding to climate change?

Recent studies on climate responses in ectothermic (cold-blooded) vertebrates have been few in number and focussed on phenology rather than morphology. According to Bergmann’s rule, endothermic (warm-blooded) vertebrates from cooler climates tend to be larger than congeners from warmer regions. Although amphibians are ectothermic vertebrates, weather and climatic conditions may also impact on their morphology, and thereby affect their survival rates and population dynamics. In this paper, we show, in a unique long-term study during the period 1963–2003 in an agricultural landscape in western Poland, that the body length of two water frog parental species (males of both Rana ridibunda and R. lessonae) increased significantly. However, their hybridogenetic hybrid R. esculenta did not show similar changes. A significant relationship with a large-scale climatic factor, the winter North Atlantic Oscillation index, was found positive for R. ridibunda males and R. lessonae females, and negative for R. esculenta females. Our findings, the first for amphibians, are consistent with other studies reporting that recent climate change has affected the morphology of animals. However, we also show that changes in amphibian phenotype linked to climate may vary independently between (even very similar) species.     

The Triassic dicynodont Kombuisia (Synapsida, Anomodontia) from Antarctica, a refuge from the terrestrial Permian-Triassic mass extinction

Fossils from the central Transantarctic Mountains in Antarctica are referred to a new species of the Triassic genus Kombuisia, one of four dicynodont lineages known to survive the end-Permian mass extinction. The specimens show a unique combination of characters only present in this genus, but the new species can be distinguished from the type species of the genus, Kombuisia frerensis, by the presence of a reduced but slit-like pineal foramen and the lack of contact between the postorbitals. Although incomplete, the Antarctic specimens are significant because Kombuisia was previously known only from the South African Karoo Basin and the new specimens extend the taxon’s biogeographic range to a wider portion of southern Pangaea. In addition, the new finds extend the known stratigraphic range of Kombuisia from the Middle Triassic subzone B of the Cynognathus Assemblage Zone into rocks that are equivalent in age to the Lower Triassic Lystrosaurus Assemblage Zone, shortening the proposed ghost lineage of this taxon. Most importantly, the occurrence of Kombuisia and Lystrosaurus mccaigi in the Lower Triassic of Antarctica suggests that this area served as a refuge from some of the effects of the end-Permian extinction. The composition of the lower Fremouw Formation fauna implies a community structure similar to that of the ecologically anomalous Lystrosaurus Assemblage Zone of South Africa, providing additional evidence for widespread ecological disturbance in the extinction’s aftermath.     

Fire ant venom alkaloids act as key attractants for the parasitic phorid fly, Pseudacteon tricuspis (Diptera: Phoridae)

The phorid fly, Pseudacteon tricuspis Borgmeier, is an introduced parasitoid of imported fire ants, Solenopsis spp., in the USA. Although the assumption that phorid flies use fire ant alarm pheromones for host location is probably true, we demonstrated in a previous study the possible involvement of other ant semiochemicals in the response of P. tricuspis to fire ants. This study was conducted to determine the glandular sources and identity of the semiochemicals mediating this interaction. First, we tested the electroantennogram response of P. tricuspis to extracts of key body parts and glands of workers of the red imported fire ant, S. invicta Buren. The results confirm that the poison (venom) gland/sac is the key source of compounds which elicited strong antennal activity in P. tricuspis. Follow-up studies were conducted by using a combination of bioassay-guided fractionation and behavioral bioassays to test the hypothesis that attraction of this parasitoid to fire ants is mediated by venom alkaloids. The results confirm the response of P. tricuspis to physiologically relevant amounts of the two venom alkaloid fractions (cis and trans alkaloid fractions) of S. invicta. Further analysis by coupled gas chromatography–electroantennogram detection revealed nine venom alkaloid components including two novel 2,6-dialkylpiperideines that elicited significant antennal activity in P. tricuspis. This is the first demonstration of the role of venom alkaloids of ants as attractants for their natural enemies. We propose a semiochemical-mediated host location mechanism for P. tricuspis involving both alarm pheromones and venom alkaloids. The ecological significance of these findings, including the attraction of male P. tricuspis to fire ant venom alkaloids, possibly for mate location, is discussed.     

Dancing to different tunes: heterospecific deciphering of the honeybee waggle dance

Although the structure of the dance language is very similar among species of honeybees, communication of the distance component of the message varies both intraspecifically and interspecifically. However, it is not known whether different honeybee species would attend interspecific waggle dances and, if so, whether they can decipher such dances. Using mixed-species colonies of Apis cerana and Apis mellifera, we show that, despite internal differences in the structure of the waggle dances of foragers, both species attend, and act on the information encoded in each other’s waggle dances but with limited accuracy. These observations indicate that direction and distance communication pre-date speciation in honeybees.     

Eunuchs as better fighters?

Male–male competition for females can significantly affect a male’s reproductive success and hence his fitness. Game theory predicts that an individual should avoid fighting when its future reproductive potential is high, but should fight forcefully when its future reproductive potential is insignificant. When mates are scarce, extreme competition and fatal fighting is expected. We recently showed that Nephilengys malabarensis eunuchs, i.e. sterile spider males that lost their genitals during copulation, become more aggressive during male–male contests. Here, we add crucial comparative data by exploring eunuch fighting behaviour in Nephilengys livida from Madagascar, specifically by testing the ‘better fighter hypotheses’ in a laboratory setting. Similar to N. malabarensis, N. livida copulations resulted in total male castration with the severed palp plugging the female genitals in 70.83% cases, which mostly (63.63%) prevented subsequent copulations. Unexpectedly, however, N. livida eunuchs exhibited lower aggressiveness than virgin males. We interpret these results in the light of different mating biology between the so far studied species known for the eunuch phenomenon, which might reflect differing plug effectiveness due to variation in genital anatomy in N. livida, N. malabarensis and Herennia multipuncta. However, detected differences in aggressive behaviour of N. livida versus N. malabarensis eunuchs might also be explained by the species’ ecology, with lower population densities resulting in a relaxed male–male competition making excessive aggression and mate guarding redundant. This study thus questions the generality of overt aggressiveness in mated males with no reproductive value, and highlights the importance of understanding the natural history of species in the question.     

A reassessment of the mating system characteristics of the army ant Eciton burchellii

In a recent study, Denny et al. (2004a) showed that queens of the army ant, Eciton burchellii, mate with multiple males and presented estimates suggesting that they mate with more males than queens of any other ant species so far investigated. They also inferred that data were consistent with queens being inseminated repeatedly throughout their life, which would be exceptional among the social Hymenoptera and contradictory to predictions from kin selection theory. In the present study, we reanalyze these data using new software and supplement them with similar microsatellite data from other colonies of the same species. Mating frequencies in E. burchellii are indeed very high (mean observed and effective queen-mating frequencies of 12.9 each) but considerably lower than the previous estimates. We show that the number of patrilines represented in the first worker offspring of a young queen is lower than in older queens but suggest that this may be due to initial sperm clumping in the queen’s sperm storage organ, rather than to repeated inseminations. Moreover, we found no evidence for repeated mating by genotyping sequential worker generations produced by a single old queen, showing that she did not obtain new inseminations despite ample opportunities for mating.     

Scale-dependent analysis of an otter–crustacean system in Argentinean Patagonia

The Southern river otter or ‘huillin’, Lontra provocax, is an endangered species endemic of the Andean Patagonian region of Argentina and Chile. It feeds almost exclusively on the genera of macro-crustacea: Aegla and Sammastacus. The aim of this study was to analyse the role of food availability on the huillin’s distribution using a scale-dependent analysis of crustacean and otter distributions. We compared the distributions of otters and macro-crustaceans along a north–south regional gradient, between river basins of northern Patagonia, in an altitudinal gradient within a river basin, and between habitat types within a lake. We investigated the distribution of otters by sign surveys along lake shores, river banks and marine coasts, and of crustaceans using surveys in the water, undigested remains in mink (Mustela vison) scats, presence of external skeletons at the waterside and through interviews with local people. Our results show that there were heterogeneities in the distributions of macro-crustaceans at four scales and these were generally reflected in the distributions of freshwater otters. We conclude that the main factor limiting the distributions of L. provocax in freshwater environments is the availability of macro-crustaceans. This paper shows how scale-dependent type analyses of population distribution serves as a method for identifying key environmental factors for species for which the use of long-term demographies is unfeasible.     

Winged queens replaced by reproductives smaller than workers in <Emphasis Type="Italic">Mystrium</Emphasis> ants

In ants, winged queens that are specialized for independent colony foundation can be replaced by wingless reproductives better adapted for colony fission. We studied this shift in reproductive strategy by comparing two Mystrium species from Madagascar using morphometry, allometry and dissections. Mystrium rogeri has a single dealate queen in each colony with a larger thorax than workers and similar mandibles that allow these queens to hunt during non-claustral foundation. In contrast, Mystrium ‘red’ lacks winged queens and half of the female adults belong to a wingless ‘intermorph’ caste smaller and allometrically distinct from the workers. Intermorphs have functional ovaries and spermatheca while those of workers are degenerate. Intermorphs care for brood and a few mate and reproduce making them an all-purpose caste that takes charge of both work and reproduction. However, their mandibles are reduced and inappropriate for hunting centipedes, unlike the workers’ mandibles. This together with their small thorax disallow them to perform independent colony foundation, and colonies reproduce by fission. M. rogeri workers have mandibles polymorphic in size and shape, which allow for all tasks from brood care to hunting. In M. ‘red’, colonial investment in reproduction has shifted from producing expensive winged queens to more numerous helpers. M. ‘red’ intermorphs are the first case of reproductives smaller than workers in ants and illustrate their potential to diversify their caste system for better colonial economy.     

Measuring the order in ordered porous arrays: can bees outperform humans?

A method that explains how to quantify the amount of order in “ordered” and “highly ordered” porous arrays is derived. Ordered arrays from bee honeycomb and several from the general field of nanoscience are compared. Accurate measures of the order in porous arrays are made using the discrete radial distribution function (RDF). Nanoporous anodized aluminum oxide (AAO), hexagonal arrays from functional materials, hexagonal arrays from nanosphere lithography, and square arrays defined by interference lithography (all taken from the literature) are compared to two-dimensional model systems. These arrays have a range of pore diameters from ∼60 to 180 nm. An order parameter, OP ₃ , is defined to evaluate the total order in a given array such that an ideal network has the value of 1. When we compare RDFs of man-made arrays with that of our honeycomb (pore diameter ∼5.89 mm), a locally grown version made by Apis mellifera without the use of foundation comb, we find OP ₃ =0.399 for the honeycomb and OP ₃ =0.572 for man’s best hexagonal array. The nearest neighbor peaks range from 4.65 for the honeycomb to 5.77 for man’s best hexagonal array, while the ideal hexagonal array has an average of 5.93 nearest neighbors. Ordered arrays are now becoming quite common in nanostructured science, while bee honeycombs were studied for millennia. This paper describes the first method to quantify the order found in these arrays with a simple yet elegant procedure that provides a precise measurement of the order in one array compared to other arrays.     

Regional,seasonal and interspecific variation in <Superscript>15</Superscript>N and <Superscript>13</Superscript>C in sympatric mouse lemurs

Madagascar provides some of the rare examples where two or more primate species of the same genus and with seemingly identical niche requirements occur in sympatry. If congeneric primate species co-occur in other parts of the world, they differ in size in a way that is consistent with Hutchinson’s rule for coexisting species, or they occupy different ecological niches. In some areas of Madagascar, mouse lemurs do not follow these “rules” and thus seem to violate one of the principles of community ecology. In order to understand the mechanisms that allow coexistence of sympatric congeneric species without obvious niche differentiation, we studied food composition of two identical sized omnivorous mouse lemur species, Microcebus griseorufus and M. murinus with the help of stable isotope analyses (δ ¹⁵N and δ ¹³C). The two species are closely related sister species. During the rich season, when food seems abundant, the two species do not differ in their nitrogen isotope composition, indicating that the two species occupy the same trophic level. But they differ in their δ ¹³C values, indicating that M. griseorufus feeds more on C₄ and CAM (Crassulacean-acid-metabolism) plants than M. murinus. During the lean season, M. murinus has lower δ ¹⁵N values, indicating that the two species feed at different trophic levels during times of food shortage. Hybrids between the two species showed intermediate food composition. The results reflect subtle differences in foraging or metabolic adaptations that are difficult to quantify by traditional observations but that represent possibilities to allow coexistence of species.     

Macroglomeruli for fruit odors change blend preference in Drosophila

The olfactory circuitry of Drosophila melanogaster is becoming increasingly clear. However, how olfactory processing translates into appropriate behavioral responses is still poorly understood. Using a sibling species approach, we tested how a perturbation in the olfactory circuitry affects odor preference. In a previous study, we found that the sibling species of D. melanogaster, the specialist D. sechellia, overrepresents a sensillum, ab3, the A neuron of which is sensitive to hexanoate esters, characteristic of the species’ sole host, the Morinda citrifolia fruit. Concordantly, the corresponding glomerulus, DM2, is enlarged. In this study, we found that the ab3B neuron, the expansion of which was previously assumed to be pleiotropic and of no ecological significance, is in fact tuned to another morinda fruit volatile, 2-heptanone (HP). Axons of this neuron type arborize in a second enlarged glomerulus. In behavioral experiments we tested how this has affected the fly’s odor preference. We demonstrate that D. sechellia has a reversed preference for the key ligands of these macroglomeruli, especially at high concentrations. Whereas D. melanogaster was repelled by high concentrations of these odors, D. sechellia was highly attracted. This was the case for odors presented singly, but more notably for blends thereof. Our study indicates that relatively simple changes, such as a shift in sensillar abundance, and concordant shifts in glomerular size, can distort the resulting olfactory code, and can lead to saltatory shifts in odor preference. D. sechellia has exploited this to align its olfactory preference with its ecological niche.     

The European land leech: biology and DNA-based taxonomy of a rare species that is threatened by climate warming

The European land leech Xerobdella lecomtei was discovered in 1868 and is one of the rarest animals on Earth. During the 1960s, several individuals of these approx. 40 mm long, cold-adapted terrestrial annelids that inhabit the moist soils of birch forests around Graz, Austria, were investigated. Only one original research paper has been published on the biology of this species. Between 2001 and 2005, we re-investigated the morphology of preserved specimens and searched for living individuals in their natural habitat that appeared to be intact. We found only one juvenile individual (length approx. 10 mm), indicating that this local leech population became largely extinct over the past four decades. The feeding behaviour of our ‘lonesome George of the annelids’ was studied and is described here in detail. After its death, the Xerobdella individual was used for chemical extraction and molecular studies (deoxyribonucleic acid [DNA] barcoding, based on one gene, the mitochondrial cytochrome c oxidase subunit I). In addition, novel DNA barcodes for a land leech from Madagascar and a recently discovered species from Europe were obtained. Our phylogenetic tree shows that X. lecomtei is not a member of the tropical land leeches (family Haemadipsidae), as previously thought, but represents a separate line of descent (family Xerobdellidae). The decline of the local leech population around Graz correlates with a rise in average summer temperatures of +3°C between 1961 and 2004. This warming led to a drastic reduction in the moisture content of the soil where X. lecomtei lives. We suggest that human-induced climate change without apparent habitat destruction can lead to the extinction of populations of cold-adapted species that have a low colonization ability.     

When attempts at robbing prey turn fatal

Because group-hunting arboreal ants spread-eagle insect prey for a long time before retrieving them, these prey can be coveted by predatory flying insects. Yet, attempting to rob these prey is risky if the ant species is also an effective predator. Here, we show that trying to rob prey from Azteca andreae workers is a fatal error as 268 out of 276 potential cleptobionts (97.1?%) were captured in turn. The ant workers hunt in a group and use the “Velcro?” principle to cling firmly to the leaves of their host tree, permitting them to capture very large prey. Exceptions were one social wasp, plus some Trigona spp. workers and flies that landed directly on the prey and were able to take off immediately when attacked. We conclude that in this situation, previously captured prey attract potential cleptobionts that are captured in turn in most of the cases.     

Spectral characteristics of plant communities from salt marshes:A case study from Chongming Dongtan,Yangtzeestuary,China

The spectral reflectance of recently formed salt marshes at the mouth of the Yangtze River, which are undergoing invasion by Spartina alterniflora, were assessed to determine the potential utility of remotely sensed data in assessing future invasion and changes in species composition. Following a review of published research on remote sensing of salt marshes, 53 locations along three transects were sampled for paired data on plant species composition and spectral reflectance using a FieldSpec™ Pro JR Field Portable Spectroradiometer. Spectral data were processed concerning reflectance, and the averaged reflectance values for each sample were reanalysed to correspond to a 12-waveband bandset of the Compact Airborne Spectral Imager. The spectral data were summarised using principal components analysis (PCA) and the relationships between the vegetation composition, and the PCA axes of spectral data were examined. The first PCA axis of the reflectance data showed a strong correlation with variability in near infrared reflectance and ‘brightness’, while the second axis was correlated with visible reflectance and ‘greenness’. Total vegetation cover, vegetation height, and mudflat cover were all significantly related to the first axis. The implications of this in terms of the ability of remote sensing to distinguish the various salt marsh species and in particular the invasive species S. alterniflora were discussed. Major differences in species with various physiognomies could be recognised but problems occurred in separating early colonising S. alterniflora from other species at that stage. Further work using multi-seasonal hyperspectral data might assist in solving these problems.