Hyperparasitoid defense strategies against spiders: the role of chemical and morphological protection

The aphid endohyperparasitoid Alloxysta brevis(Thomson) (Hymenoptera: Charipidae) applies defensive chemicals stored in mandibular gland reservoirs against attacking ants. Alloxystines can be divided into species capable of exploiting ant-attended resources and into species exclusively reared from unattended aphid-parasitoid systems. Mandibular secretions are found in species of both groups, with little variation in chemical composition. We show that the mandibular gland secretion does not only protect against ant attacks but acts as an overall defense agent against generalist predators like spiders. The protective success differed with the spider species. The web-building spider Agelena labyrinthica(Clerck) (Araneae: Agelinidae) killed 57% of attacked A. brevisfemales, but sucked out only 8%. The smaller free-hunting jumping spider Salticus scenicus(Clerck) (Araneae: Salticidae) failed in overwhelming or severely injuring A. brevis. The pattern of interactions showed striking similarities with interactions between A. brevisand the ant Lasius niger(Hymenoptera: Formicidae). Primary parasitoids which are lacking chemical defense and sufficient morphological protection suffered significantly higher mortality due to spider predation. Our results indicate that – additional to chemical defense- parasitoid survival depends on the specific morphological resistance against grip pressure during capture, and on the predator – prey size relationship.     

Ant assemblages in the taiga biome: testing the role of territorial wood ants

Summary Ants were collected with sets of pitfall traps in four coniferous-forest habitats in southern Finland. A three-level competition hierarchy concept was used to generate predictions on ant community structure. The levels of the hierarchy, and the respective predictions, from top to bottom were: (1) The dominant territorial wood ants (Formica rufa-group species), expected to exclude each other. (2) The other aggressive species, likely to be excluded by the F. rufa-group. (3) The submissive species, non-aggressive and defending only their nest, and thus likely to coexist with the dominants but in reduced numbers. As expected, the species of the F. rufa-group excluded each other, and the species number of the other aggressive ants was significantly cut down in the presence of the F. rufa-group. The aggressive species F. sanguinea and Camponotus herculeanus showed complementary occurrences with the F. rufa-group, and Lasius niger reduced occurrences. The number of the submissive species was not significantly affected by the F. rufa-group. However, pairwise correlation coefficients were significantly more often negative than positive between presence of the F. rufa-group and average proportion of pitfalls per set with a submissive species, each analyzed in turn. The result indicates that the F. rufa-group also reduced the colony densities of the submissive species. We conclude that in the taiga biome territorial wood ants are, after adjusting for physical vicissitudes of the environment, the major structuring force of ant species assemblages.     

Behavioral strategies of aphid hyperparasitoids to escape aggression by honeydew-collecting ants

We analyzed the behavioral interactions between two species of honeydew-collecting ants (Lasius niger, Myrmica laevinodis) and foraging females of four species of aphid hyperparasitoids (Aphidencyrtus aphidivorus, Dendrocerus carpenteri, Pachyneuron aphidis, Asaphes vulgaris) usingAphis fabae ssp.cirsiiacanthoidis andLysiphlebus cardui on thistles as aphid and primary parasitoid, respectively. The observed interaction patterns and foraging parameters varied within hyperparasitoid species and revealed different strategies based upon behavioral and morphological constraints.D. carpenteri generally tried to avoid ant encounters. This avoidance strategy was successful in interactions withM. laevinodis but failed when encountering the more aggressiveL. niger, which caused about 26% adult mortality. In contrast,A. aphidivorus, P. aphidis, andA. vulgaris possess jumping ability and were hardly exposed to mortality risks. The escape reaction jump off was used as soon as ants made physical contact with foraging females. While the flight strategy ofP. aphidis is connected with cryptic movement patterns without avoidance behavior,A. aphidivorus first avoided ants and jumped off only as a last resort. Similar patterns, but less expressive, are displayed byA. vulgaris. We suggest that these different strategies are responsible for different foraging success in ant-attended resources in field.     

Interactions between ants attendingAphis fabae ssp.cirsiiacanthoidis on thistles and foraging parasitoid wasps

We describe the behavioral interactions between honeydew-collecting workers of the ants Lasius nigerand Myrmica ruginodisand females of three species of aphidiid wasps (Lysiphlebus cardui, Lysiphlebus testaceipes, Trioxys angelicae)foraging for their aphid host, Aphis fabaessp. cirsiiacanthoidis,on thistles. Using field and laboratory experiments, we show that the ant-parasitoid interactions are species specific. Workers of both ant species generally attacked and killed females of T. angelicae,but they ignored those of L. cardui.This pattern was not altered when we anesthetized the wasps slightly with carbon dioxide to reduce their mobility. Prior contacts between L. carduiand either conspecific L. nigerfrom a different nest or workers of a different ant species (M. ruginodis)did not influence L. niger'snonaggressive behavior. The number of aphids parasitized by L. testaceipeswas significantly reduced in aphid colonies attended by L. niger,although this parasitoid was rarely attacked by ants. In encounters between these species of ants and wasps, ant aggression is consistent with differences in wasp behavior. We suggest that, in addition, chemical cues located in the cuticula may enable L. carduito avoid detection by honeydew-collecting ants.     

Density-dependent predation of the antLasius niger (Hymenoptera: Formicidae) on two attended aphidsLachnus tropicalis andMyzocallis kuricola (Homoptera: Aphididae)

The antLasius niger was observed collecting honeydew and preying on the two aphid speciesLachnus tropicalis andMyzocallis kuricola on the chestnut treesCastanea crenata. Observation determined how the antL. niger controlled their predation on the aphids in response to the density and honeydew-productivity of the aphids.Lachnus tropicalis was a better honeydew source thanM. kuricola forL. niger in terms of the amount of honeydew collected per unit time by the ants. The number of foraging workers on a tree increased with the number ofL. tropicalis on the tree, but not with the number ofM. kuricola. The density ofL. tropicalis perL. niger worker on a tree had a positive effect on the predation activity ofL. niger on both aphids, whereas the density ofM. kuricola per ant did not have any significant effect. The predation pressure by the ant which increased withL. tropicalis density, however, directed toM. kuricola rather than toL. tropicalis. These facts suggest (1) thatL. niger control their predation activities on aphids with regards to the densities of the attended aphids per worker, and (2) that the ants prey on the aphid species producing less honeydew. The effects of the ant predation on aphids and the importance of these predation effect in antaphids interactions were discussed.     

Diet and predators of Tenagomysis tasmaniae Fenton, Anisomysis mixta australis (Zimmer) and Paramesopodopsis rufa Fenton from south-eastern Tasmania (Crustacea:Mysidacea)

The diets of three mysid species Tenagomysis tasmaniae Fenton, Anisomysis mixta australis (Zimmer) and Paramesopodopsis rufa Fenton were investigated together with a number of potential fish predators by gut contents and stable isotope analysis. Gut content analysis of the three mysis species revealed that all have an omnivorous diet, although the stomachs of P. rufa contained a greater percentage of crustacean remains, whereas the stomach contents of T. tasmaniae were largely composed of fragments of macroalgae. The stomach contents of A. mixta australis were composed mainly of fine particulate matter. Diel feeding rhythms were examined from mysids collected during a 24-hour sampling session in October. P. rufa appeared to be primarily a day-time feeder while T. tasmaniae fed more intensively at night. The results for A. mixta australis were inconclusive. Gut contents analysis of fish collected at the study site revealed predation on mysids by Arripis trutta (juveniles), Aldrichetta forsteri, Vincentia conspersa and Pseudolabrus fucicola. The mysid species most frequently eaten was Tenagomysis australis Fenton. The mysid species most frequently eaten was Tenagomysis australis Fenton.     

Breeding biology of Tenagomysis tasmaniae Fenton,Anisomysis mixta australis (Zimmer) and Paramesopodopsis rufa Fenton from south-eastern Tasmania (Crustacea: Mysidacea)

The number, size and developmental stage of young in the brood pouch of female Tenagomysis tasmaniae, Anisomysis mixta australis and Paramesopodopsis rufa was recorded throughout the year. Breeding was intensive from spring till the end of autumn for the three species. Calculation of the egg ratio for each species showed that their major reproductive peaks occurred during spring and summer. A winter depression in the breeding cycle was observed for T. tasmaniae and P. rufa, but A. mixta australis ceased breeding during winter. Seasonal variation in the length of gravid females and number of young carried was evident for these three species. Females were longer in spring and summer and carried more young than in autumn and winter. A linear relationship between female length and brood size was demonstrated for each species; annual and seasonal equations were calculated for females carrying each developmental stage. The seasonal equations showed that for a female of given length fecundity was greater during spring than any other season. Natality was estimated to be highest during late spring, summer and early autumn for the three species. No seasonal variation in the size of eggs was evident for the three species. The reproduction pattern of T. tasmaniae, A. mixta australis and P. rufa appears to be very similar to that reported for the majority of iteroparous coastal temperate mysids throughout the world.     

Production and biomass of Tenagomysis tasmaniae Fenton, Anisomysis mixta australis (Zimmer) and Paramesopodopsis rufa Fenton from south-eastern Tasmania (Crustacea: Mysidacea)

Annual production estimates were calculated for Tenagomysis tasmaniae, Anisomysis mixta australis and Paramedopodopsis rufa using the size-frequency and Petrovich methods. Annual production for T. tasmaniae was more than twice that for P. rufa and A. mixta australis. The P:B ratio was however , higher for a. mixta australis than T. tasmaniae and P. rufa. The P:B values for the three species are among the highest ratios reported for mysids.     

Effects of ants on plant diversity in semi-natural grasslands

Ants (L. niger and L. flavus) build conspicuous mounds that are covered with vegetation. The aim of this study was to investigate whether the vegetation on ant mounds in semi-natural grasslands differed from that around the mounds. Another aim was to investigate whether the changes in the vegetation on ant mounds were influenced by grazing management or by habitat characteristics, semi-dry versus moist. Here, the total number of plant species and total plant cover were lower on ant mounds than in patches off-mound. The plant cover of perennials that form rosettes was twice as high on mounds inhabited by L. niger than on those inhabited by L. flavus. Only a few plant species were restricted to either ant mounds or adjacent field and the effects of ants on the plant diversity in semi-natural grasslands seemed to be low. Grazing management did not affect the differences in the vegetation on ant mounds and in equal-sized patches off-mound, whereas habitat characteristics affected ant-induced changes in vegetation cover of some plant species.     

Biology of Tetrastichus howardi (Olliff) (Hymenoptera: Eulophidae): A facultative Hyperparasitoid of stem borers

The biology of the parasitoid Tetrastichus howardi, which was introduced from the Philippines into South Africa for the biological control of the stem borer Chilo partellus, was studied in the laboratory. On average, a T. howardi female produced 101 progeny (92% females) which developed in 4.3 hosts. The upper threshold temperature for development was around 33°C, the minimum threshold was calculated as 12.8°C and the thermal constant as 239.8 day‐degrees. With hosts, females lived 23.6 and males 16.7 days. T. howardi was found to be a facultative hyperparasitoid with a very wide host range. As a primary parasitoid, it developed in pupae of various Lepidoptera as well as Coleoptera and Hymenoptera and as a hyperparasitoid in dipteran and hymenopteran parasitoids. A linear relation was found between the number of emergent parasitoids and the volume of the host from which they emerged. Preference tests indicated that T. howardi preferred to parasitize the phytophagous insects C. partellus and Heliothis armigera, over their parasitoids Xanthopimpla stemmator and Palexorista laxa. The host selection of inexperienced T. howardi females was different from the experienced parasitoids. When given a choice, females showed preference for the host species they were allowed to parasitize previously and the host species from which they had been reared. The use of facultative hyperparasitoids in biological control in general and against stem borers in South Africa in particular is discussed.     

Immune priming and pathogen resistance in ant queens

Growing empirical evidence indicates that invertebrates become more resistant to a pathogen following initial exposure to a nonlethal dose; yet the generality, mechanisms, and adaptive value of such immune priming are still under debate. Because life‐history theory predicts that immune priming and large investment in immunity should be more frequent in long‐lived species, we here tested for immune priming and pathogen resistance in ant queens, which have extraordinarily long life span. We exposed virgin and mated queens of Lasius niger and Formica selysi to a low dose of the entomopathogenic fungus Beauveria bassiana, before challenging them with a high dose of the same pathogen. We found evidence for immune priming in naturally mated queens of L. niger. In contrast, we found no sign of priming in virgin queens of L. niger, nor in virgin or experimentally mated queens of F. selysi, which indicates that immune priming in ant queens varies according to mating status and mating conditions or species. In both ant species, mated queens showed higher pathogen resistance than virgin queens, which suggests that mating triggers an up‐regulation of the immune system. Overall, mated ant queens combine high reproductive output, very long life span, and elevated investment in immune defense. Hence, ant queens are able to invest heavily in both reproduction and maintenance, which can be explained by the fact that mature queens will be protected and nourished by their worker offspring.     

Interference competition,not predation,explains the negative association between wood ants (Formica rufa) and abundance of ground beetles (Coleoptera: Carabidae)

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Fire ant myrmecophiles: feeding relationships ofMartinezia dutertrei andEuparia castanea (Coleoptera: Scarabaeidae) with their host ants,Solenopsis spp. (Hymenoptera: Formicidae)

Summary Feeding relationships of adultEuparia castanea Serville andMartinezia dutertrei Chalumeau with their ant hosts were studied in the laboratory using the radioactive tracer³²P.Euparia castanea was tested withSolenopsis geminata (F.),Martinezia dutertrei Chalumeau was tested withS. invicta Buren,S. richteri Forel, andS. geminata. Unlabeled beetles were exposed to various radioisotope labeled conditions for 24 hr and then checked for acquired radioactivity. In whole colony tests, both species of beetles acquired radioactivity.M. dutertrei obtained food from live ants, butE. castanea did not. Both species of beetles ate ant larvae.E. castanea also obtained food from ant larvae by strigilation. Neither species of beetle fed on ant feces or other secretions on the substrate. Both species of beetles obtained food by strigilation from fresh and decomposed worker ant cadavers.M. dutertrei also ate both kinds of ant cadavers. Both species of beetles also ate dead house flies, indicative of scavenging or feeding on ant booty.Martinezia dutertrei showed no preference for any particular ant species. Ants did not obtain food by trophallaxis or glandular secretion from either species of beetle. Martinezia dutertrei Chalumeau, 1983 (=Myrmecaphodius excavaticollis Auct.,nec Blanchard 1843).This article reports the results of research only. Mention of a proprietary product does not constitute an endorsement or a recommendation for its use by the U.S. Department of Agriculture.     

An aphidiine parasitoid Monoctonia vesicarii (Hymenoptera: Braconidae) and three chalcidoid hyperparasitoids of Pemphigus matsumurai (Homoptera: Aphididae) forming leaf galls on Populus maximowiczii in Japan

More than 300 unopened leaf galls formed by the pemphigine aphid Pemphigus matsumurai on Populus maximowiczii were collected at Nakasatsunai, Hokkaido, Japan, in July and September 2007 and kept in cold conditions during winter. From mummified fundatrices in the galls an aphidiine parasitoid Monoctonia vesicarii and three species of hyperparasitoids belonging to Pteromalidae, Eupelmidae and Eulophidae emerged from March to May 2008. Monoctonia vesicarii, which is new to Japan, is redescribed. The eulophid hyperparasitoid is described as a new species, Aprostocetus (Aprostocetus) doronokianus, and the pteromalid and eupelmid hyperparasitoids are identified as Pachyneuron sp. and Eupelmus sp., respectively. Approximately 180 unopened mummies of P. matsumurai were dissected in August and November 2008 and a living larva of M. vesicarii was found in each of 17 of them. These observations suggest that some individuals of M. vesicarii pass through two‐year cycles. The implications of the three species of hyperparasitoids to P. matsumurai galls are discussed.     

Population dynamics of Tenagomysis tasmaniae Fenton,Anisomysis mixta australis (Zimmer) and Paramesopodopsis rufa Fenton from south-eastern Tasmania (Crustacea:Mysidacea)

The population dynamics of a coastal mysid community was examined at One Tree Point in southern Tasmania over a 12-month period, including three 24-hour sampling sessions. Fourteen mysid species were recorded. Zonation patterns, life-history and diel activity of the three most abundant species, Tenagomysis tasmaniae, Anisomysis mixta australis and Paramesopodopsis rufa were examined. These three species were found in large numbers throughout the year associated with the macroalgal fringe on either side of the bay. Habitat partitioning within this zone of occurrence was evident. T. tasmaniae was the most abundant species (annual mean density 32.4 m^–3), followed by A. mixta australis (annual mean density 20.5 m^–3 ) and P. rufa (annual mean density 11.3 m^–3). The major peaks of abundance of these three species were temporally separate. Breeding was intensive for the three species from spring till late autumn. A cessation of breeding in winter was evident for A. mixta australis and to a lesser extent for P. rufa but T. tasmaniae bred throughout the year although at a reduced rate during winter. Examination of the diel behaviour identified peaks of abundance at sunrise and sunset for T. tasmaniae; P. rufa was caught in greater numbers at night, but no consistent pattern was observed for A. mixta australis.     

Quarantining behaviour of ants towards infected aphids as an antifungal mechanism in ant–aphid interactions

The ecological success of social insects, including ants, is tightly connected with their ability to protect themselves and their food resources. In exchange for energy‐rich honeydew, ants protect myrmecophilous aphids from various natural enemies. Fungal infection can have disastrous consequences for both mutualist partners, wherein aphids can be disease vectors. Behavioural responses towards fungus‐infected aphids of ant species in nature have scarcely been studied. Here, we studied the behaviour of honeydew foragers of four ant species – Formica polyctena Foerster, Formica rufa L., Formica pratensis Retzius (Hymenoptera: Formicidae, Formicini), and Lasius niger (L.) (Formicidae, Lasiini) – towards Symydobius oblongus (von Heyden) aphids contaminated with the generalist fungal pathogen Beauveria bassiana (Balsamo‐Crivelli) Vuillemin in the field. Aphid milkers from Formica spp. quickly detected and removed infected aphids from the host plant (Betula pendula Roth., Betulaceae). Neither ant species, the degree of aphid‐milker specialization (medium or high), nor the number of honeydew foragers had significant effects on the behaviour of Formica milkers towards infected aphids. Unlike Formica ants, L. niger usually displayed non‐aggressive behaviour (tolerance, antennation, honeydew collection, grooming). By the immediate removal of infected insects, Formica ants seem to minimize the probability of infection of symbionts as well as themselves. Quarantining behaviour may play an important role in ant–aphid interactions as a preventive antifungal mechanism formed under parasite pressure and thus contributing to the ecological success of ants.     

Cascading effects of herbivore protective symbionts on hyperparasitoids

1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity. 2. This study investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids). 3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species. 4. It was found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid–parasitoid–hyperparasitoid interactions we studied. 5. It is concluded that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.     

Disruption of parasitism of the California red scale (Homoptera: Diaspididae) by three ant species (Hymenoptera: Formicidae)

The relative influence of the southern fire ant, Solenopsis xyloni McCook, Argentine ant, Linepithema humile (Mayr), and native gray ant, Formica aerata (Francoeur), on parasitism of California red scale, Aonidiella aurantii Maskell, was studied in the laboratory for two parasitoids, Comperiella bifasciata Howard and Aphytis melinus DeBach. All three ant species reduced percentage parasitism by C. bifasciata and both percentage parasitism and host mutilation by A. melinus. Southern fire ant was the least disruptive and native gray ant the most disruptive. Southern fire ant removed 12% of scale from the lemons, presumably to feed on them, while the other ant species did not exhibit significant removal of scale compared to the controls. Percentage parasitism of California red scale exhibited by C. bifasciata was more than 2-fold the level exhibited by A. melinus. Percentage mutilation of California red scale, including probing and host feeding, was nearly 5-fold higher for A. melinus than C. bifasciata. Because A. melinus required a longer total host examination + oviposition period in the absence of ants than C. bifasciata and because oviposition occurs as the last act in a sequence of behaviors, disruption by the ants had a more significant negative effect on oviposition by A. melinus.     

Aphanogmus sp. (Hymenoptera: Ceraphronidae): a hyperparasitoid of the coffee berry borer parasitoid Prorops nasuta (Hymenoptera: Bethylidae) in Kenya

This is the first report of a hyperparasitoid of Prorops nasuta, a primary parasitoid of the coffee berry borer. Aphanogmus sp. is a gregarious ectoparasitoid of larval and pupal stages of P. nasuta, which was found in coffee berry samples collected on the ground of an organic coffee plantation in Western Kenya. The hyperparasitoid shows a clear pattern of emergence from year to year, following its host. Aphanogmus sp. parasitizes around 10% of P. nasuta immature stages under field conditions.     

Mycelial carton galleries of Azteca brevis (Formicidae) as a multi-species network

Apart from growing fungi for nutrition, as seen in the New World Attini, ants cultivate fungi for reinforcement of the walls of their nests or tunnel-shaped runway galleries. These fungi are grown on organic material such as bark, epiphylls or trichomes, and form stable ‘carton structures’. In this study, the carton of the runway galleries built by Azteca brevis (Formicidae, Dolichoderinae) on branches of Tetrathylacium macrophyllum (Flacourtiaceae) is investigated. For the first time, molecular tools are used to address the biodiversity and phylogenetic affinities of fungi involved in tropical ant carton architecture, a previously neglected ant–fungus mutualism.The A. brevis carton involves a complex association of several fungi. All the isolated fungi were unequivocally placed within the Chaetothyriales by DNA sequence data. Whereas five types of fungal hyphae were morphologically distinguishable, our DNA data showed that more species are involved, applying a phylogenetic species concept based on DNA phylogenies and hyphal morphology. In contrast to the New World Attini with their many-to-one (different ant species—one fungal cultivar) pattern, and temperate Lasius with a one-to-two (one ant species—two mutualists) or many-to-one (different ant species share the same mutualist) system, the A. brevis–fungi association is a one-to-many multi-species network. Vertical fungus transmission has not yet been found, indicating that the A. brevis–fungi interaction is rather generalized.