Inverse dispersal patterns in a group of ant parasitoids (Hymenoptera: Eucharitidae: Oraseminae) and their ant hosts

When postulating evolutionary hypotheses for diverse groups of taxa using molecular data, there is a tradeoff between sampling large numbers of taxa with a few Sanger-sequenced genes or sampling fewer taxa with hundreds to thousands of next-generation-sequenced genes. High taxon sampling enables the testing of evolutionary hypotheses that are sensitive to sampling bias (i.e. dating, biogeography and diversification analyses), whereas high character sampling improves resolution of critical nodes. In a group of ant parasitoids (Hymenoptera: Eucharitidae: Oraseminae), we analyse both of these types of datasets independently (203 taxa with five Sanger loci, 92 taxa with 348 anchored hybrid enrichment loci) and in combination (229 taxa, 353 loci) to explore divergence dating, biogeography, host relationships and differential rates of diversification. Oraseminae specialize as parasitoids of the immature stages of ants in the subfamily Myrmicinae (Hymenoptera: Formicidae), with ants in the genus Pheidole being their most common and presumed ancestral host. A general assumption is that the distribution of the parasite must be limited by any range contraction or expansion of its host. Recent studies support a single New World to Old World dispersal pattern for Pheidole at c. 11–27 Ma. Using multiple phylogenetic inference methods (parsimony, maximum likelihood, dated Bayesian and coalescent analyses), we provide a robust phylogeny showing that Oraseminae dispersed in the opposite direction, from Old World to New World, c. 24–33 Ma, which implies that they existed in the Old World before their presumed ancestral hosts. Their dispersal into the New World appears to have promoted an increased diversification rate. Both the host and parasitoid show single unidirectional dispersals in accordance with the presence of the Beringian Land Bridge during the Oligocene, a time when the changing northern climate probably limited the dispersal ability of such tropically adapted groups.     

Ancient host shifts followed by host conservatism in a group of ant parasitoids

While ant colonies serve as host to a diverse array of myrmecophiles, few parasitoids are able to exploit this vast resource. A notable exception is the wasp family Eucharitidae, which is the only family of insects known to exclusively parasitize ants. Worldwide, approximately 700 Eucharitidae species attack five subfamilies across the ant phylogeny. Our goal is to uncover the pattern of eucharitid diversification, including timing of key evolutionary events, biogeographic patterns and potential cophylogeny with ant hosts. We present the most comprehensive molecular phylogeny of Eucharitidae to date, including 44 of the 53 genera and fossil-calibrated estimates of divergence dates. Eucharitidae arose approximately 50 Ma after their hosts, during the time when the major ant lineages were already established and diversifying. We incorporate host association data to test for congruence between eucharitid and ant phylogenies and find that their evolutionary histories are more similar than expected at random. After a series of initial host shifts, clades within Eucharitidae maintained their host affinity. Even after multiple dispersal events to the New World and extensive speciation within biogeographic regions, eucharitids remain parasitic on the same ant subfamilies as their Old World relatives, suggesting host conservatism despite access to a diverse novel ant fauna.     

Patterns of host use in solitary parasitoids (Hymenoptera, Ichneumonidae): field evidence from a homogeneous habitat

Teder, T., Tammaru, T. and Pedmanson, R. 1999. Patterns of host use in solitary parasitoids (Hymenoptera, Ichneumonidae): field evidence from a homogeneous habitat. - Ecography 22: 79-86.
We detected a significant inter- and intraspecific host preference on the level of individual host use in a system, in which three moth species (Lepidoptera: Noctuidae), feeding on a cattail Typha latifolia , are parasitized by three solitary parasitoid species (Hymenoptera: Ichneumonidae). The biology of the host species is similar but they exhibit remarkable inter- and intraspecific variance in body size. All the parasitoid species preferred the largest host species in this system whereas other host species were used only occasionally. We found that parasitoids which emerged from females of the preferred host species were larger than those which developed in males of the same species. Accordingly, two of the parasitoid species had a significant within-host-species preference: females of the largest moth species were used more often than males. No dependence of the preference pattern on host density was found. This pattern of host use is discussed in the light of the switching theory and the optimal host selection theory. Our results indicate that non-random host use by parasitoids may have significant effects on host populations and communities, and forms a potential selective factor against large body size in herbivorous insects. Unlike the majority of ichneumonid wasps, these three parasitoid species have no remarkable female-biased sexual size dimorphism, in accordance with the predictions of Charnov's sex allocation theory for this case, we did not observe any significant host quality dependent biases in sex allocation: there was no association between host sex and parasitoid sex, neither did parasitoid sex ratio differ between years with different host quality.     

Patterns of host selection by four species of aphidiid (Hymenoptera) parasitoids: influence of host switching

Abstract.

• 1 We tested switching behaviour in four species of aphidiid parasitoids, using a two-aphid experimental system consisting of second-instar nymphs of pea aphid (Acyrthosiphon pisum (Harris)) and alfalfa aphid (Macrosiphum creelii Davis) feeding on broad beans in the laboratory.
• 2 Aphidius ervi Haliday, A.pisivorus Smith, A.smithi Sharma & Subba Rao, and Pram pequodorum Viereck showed an innate preference for pea aphid when both host species were provided in equal numbers.
• 3 Wasps encountered both aphid species equally but differed in their acceptance of alfalfa aphid. Females of A.pisivorus and P.pequodorum accepted alfalfa aphids when few pea aphids were available, but A. smithi always concentrated attacks on pea aphid. Aphidius ervi super-parasitized an increasing proportion of pea aphids as their availability declined.
• 4 Switching to the alfalfa aphid occurred in A.ervi and P.pequodorum (but not in A.pisivorus and A.smithi) under the condition of a 1:3 ratio of pea aphids:alfalfa aphids. Wasps did not switch when more pea aphids than alfalfa aphids were provided (3:1 ratio).
• 5 Alfalfa aphids were more likely than pea aphids to escape from parasitoid attack.
• 6 Switching to the most abundant host may not be adaptive in these four species of aphid parasitoids. A foraging wasp incurs a potentially higher cost in lost opportunity time when attacking (and failing to oviposit in) alfalfa aphids. In addition, alfalfa aphids may have lower host quality than pea aphids, a difference that could influence offspring fitness.

     

Jumping spiders (Salticidae) enhance the seed production of a plant with extrafloral nectaries

Many plants secrete nectar from extrafloral nectaries (EFNs), specialized structures that usually attract ants which can act as plant defenders. We examined the nectar-mediated interactions between Chamaecrista nictitans (Caesalpineaceae) and jumping spiders (Araneae, Salticidae) for 2 years in old fields in New Jersey, USA. Previous research suggests that spiders are entirely carnivorous, yet jumping spiders (Eris sp. and Metaphidippus sp.) on C. nictitans collected nectar in addition to feeding on herbivores, ants, bees, and other spiders. In a controlled-environment experiment, when given a choice between C. nictitans with or without active EFNs, foraging spiders spent 86% of their time on plants with nectar. C. nictitans with resident jumping spiders did set significantly more seed than plants with no spiders, indicating a beneficial effect from these predators. However, the presence of jumping spiders did not decrease numbers of Sennius cruentatus (Bruchidae), a specialist seed predator of C. nictitans. Jumping spiders may provide additional, unexpected defense to plants possessing EFNs. Plants with EFNs may therefore have beneficial interactions with other arthropod predators in addition to nectar-collecting ants. Received: 27 May 1998 / Accepted: 23 December 1998     

Bionomics of Orasema simplex (Hymenoptera: Eucharitidae), a parasitoid of Solenopsis fire ants (Hymenoptera: Formicidae) in Argentina

Biological characteristics of the parasitoid Orasema simplex Heraty (Hymenoptera: Eucharitidae), a potential candidate for the biological control of fire ants in the United States were investigated. Female survivorship, fertility and oviposition preferences were studied in the laboratory. Naturally parasitized colonies were examined to determine offspring sex ratio, development success and time, and to artificially parasitize healthy ant colonies. In addition, field studies were carried out to establish natural oviposition substrates and adult activity patterns. Orasema simplex female survivorship was 3.6 ± 1.5 days. Newly emerged females contained 613.5 ± 114.0 mature eggs. The adult development success in natural parasitized colonies was 22.2% with a female-biased sex ratio (4:1). The time required from planidia to adult was 29.5 ± 5.4 days. In the field, adults were mostly found around the ant nests at midday. A broad range of plant species was observed as oviposition substrates. The transfer of planidia to healthy ant colonies was achieved but the development success was very low. Orasema simplex appears to have a limited potential as a fire ant biocontrol agent because of cosmetic damage to a wide variety of plants used for oviposition. However, further studies are necessary to evaluate the real damage exerted by oviposition punctures.     

Effects of ant behaviour and presence of extrafloral nectaries on seed dispersal of the Neotropical myrmecochore Turnera ulmifolia L. (Turneraceae)

This paper describes the myrmecochory system of Turnera ulmifolia in a coastal sand dune matorral in Mexico. Turnera ulmifolia has elaiosome‐bearing seeds and extrafloral nectaries (EFNs). In ten quadrants (4 × 15 m) ant–seed interaction was monitored, and an interaction intensity index calculated and correlated with the number of seedlings. Seed removal rates by ants were surveyed every 2 h for 24 h, the ants being observed both on and beneath the plants. The role of the elaiosome in seed removal was evaluated by offering seeds with and without elaiosomes, and elaiosomes only. Finally, the effect of ant manipulation in seed germination was evaluated. There were 25 ant species associated with seeds and/or EFNs, the most frequently recorded being Monomorium cyaneum and Forelius analis. There was a positive correlation between the intensity index and seedling number per quadrant. There was significantly higher mean seed removal during the day than during the night (19.3% and 12.3%, respectively), and from beneath than on the plant (21.9% and 9.5%, respectively). The preference for elaiosomes only was also greater during the diurnal period, and when gathered on, rather than beneath, the plant. Seed manipulation by F. analis enhanced germination by T. ulmifolia. Seed removal, dispersal distances, seed predation and germination were largely determined by ant behaviour. The presence of EFNs may be influencing seed removal on the plant by attracting a specific assemblage of omnivorous ants. Among such assemblages associated with T. ulmifolia we encountered a variety of behaviours, with ant species either good at defending plants but bad at dispersing seeds, or vice versa. We discuss the way in which these two rewards, and the processes involved (defence and dispersion), could have interacted with each other and evolved. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 86 , 67–77.     

Developmental rates and host specificity for Pseudacteon parasitoids (Diptera: Phoridae) of fire ants (Hymenoptera: Formicidae) in Argentina

This study extends our comparative knowledge of Pseudacteon interactions with Solenopsis fire ant workers. Reported in this work are development times for seven Argentinean parasitoid species reared on two hosts, Solenopsis richteri Forel and Solenopsis invicta Buren, under laboratory temperature regimes comparable with those of the climatic zones occupied by these host species. Developmental times spanned 31-66 d across phorid species, and in general did not differ between genders or host species, but were longer at lower temperatures. The size distribution of flies reared was bimodal, with a group of large (Pseudacteon borgmeieri, Pseudacteon nocens, Pseudacteon obtusus and Pseudacteon tricuspis) and small (Pseudacteon cultellatus, Pseudacteon curvatus, and Pseudacteon nudicornis) species. P. borgmeieri was exceptional with respect to length of developmental time. Also reported are results of initial oviposition and developmental studies of some of these phorid species on other Argentinean Solenopsis ant species; P. curvatus was the only species able to complete its development on nonhost fire ants. These results support the concept of incorporating several complementary species of Pseudacteon in the biological control of pest fire ants.     

Insights into a novel three-partner interaction between ants,coreids (Hemiptera: Coreidae) and extrafloral nectaries: implications for the study of protective mutualisms

Extrafloral nectar of plants and honeydew of hemipterans are the common mediators of facultative interactions that involve ants as a mobile strategy of defence. The outcome of these interactions can vary from mutualistic to commensalistic or even antagonistic, depending on the ecological context and the interacting species. Here, we explore a novel, three-partner interaction involving ants, the coreid Dersagrena subfoveolata (Hemiptera) and the extrafloral nectaries (EFNs) bearing plant Senna aphylla (Fabaceae) in semi-arid Northwest Argentina. We surveyed natural areas and conducted ant exclusion experiments, to understand how each pairwise interaction influences the overall outcome among the three interacting parts. The outcome of the interactions was assessed for experimental plants as the reproductive output and herbivore abundances and for coreids as predator abundances. We found that the coreids occurred exclusively on S. aphylla plants and that at least nine ant species interacted with the EFNs as well as with the coreids. Coreid occurrence and abundance depended on ant densities, which in turn, was determined by the presence of actively secreting EFNs. Coreid and ant presence did not influence plant reproductive success, and ants provided to coreids some biotic defence, mainly against vespid wasp predators, but had no effect on non-coreid herbivores. We conclude that the interaction outcome is commensalistic between ants and plants (assuming that EF nectar is not costly for the plant), antagonistic between coreids and plants, and mutualistic between coreids and ants. The sum of all outcomes is net positive effect for ants and coreids, and net slightly negative to neutral for plants.     

How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew

Ant-plant interactions in the canopy of a lowland Amazonian rainforest of the upper Orinoco, Venezuela, were studied using a modified commercial crane on rails (Surumoni project). Our observations show a strong correlation between plant sap exudates and both abundance of ants and co-occurrence of ant species in tree canopies. Two types of plant sap sources were compared: extrafloral nectaries (EFNs) and honeydew secretions by homopterans. EFNs were a frequent food source for ants on epiphytes (Philodendron spp., Araceae) and lianas (Dioclea, Fabaceae), but rare on canopy trees in the study area, whereas the majority of trees were host to aggregations of homopterans tended by honeydew-seeking ants (on 62% of the trees examined). These aggregations rarely occurred on epiphytes. Baited ant traps were installed on plants with EFNs and in the crowns of trees from three common genera, including trees with and without ant-tended homopterans: Goupia glabra (Celastraceae), Vochysia spp. (Vochysiaceae), and Xylopia spp. (Annonaceae). The number of ant workers per trap was significantly higher on plants offering one of the two plant sap sources than on trees without such resources. Extrafloral nectaries were used by a much broader spectrum of ant species and genera than honeydew, and co-occurrence of ant species (in traps) was significantly higher on plants bearing EFNs than on trees. Homopteran honeydew (Coccidae and Membracidae), on the other hand, was mostly monopolised by a single ant colony per tree. Homopteran-tending ants were generally among the most dominant ants in the canopy. The most prominent genera were Azteca, Dolichoderus (both Dolichoderinae), Cephalotes, Pheidole, Crematogaster (all Myrmicinae), and Ectatomma (Ponerinae). Potential preferences were recorded between ant and homopteran species, and also between ant-homopteran associations and tree genera. We hypothesize that the high availability of homopteran honeydew provides a key resource for ant mosaics, where dominant ant colonies and species maintain mutually exclusive territories on trees. In turn, we propose that for nourishment of numerous ants of lower competitive capacity, Philodendron and other sources of EFNs might be particularly important.     

Observation of group recruitment to prey in a primitive ponerine ant,Amblyopone sp. (reclinata group) (Hymenoptera: Formicidae)

Summary Group recruitment during foraging was observed in a primitive ponerine ant,Amblyopone sp. (reclinata group) under laboratory condition. Workers searched for prey singly; however, if a item of prey was stung by a worker, other ants joined the attack. After the prey became immobile, one of the workers laid a trail directly toward the nest. This scout worker recruited additional workers (between 3 and 33). They formed a single file procession to the point of prey capture, and cooperatively transported the prey. A scout worker could stimulate nest workers to leave the nest without direct contact, and the recruited workers could trace the trail without guidance by the scout worker. This is the first report of recruitment behavior during foraging in the primitive antAmblyopone.     

Lophomyrmex terraceensis,a new ant species (Hymenoptera: Formicidae) in the bedoti group with a revised key

Lophomyrmex terraceensis sp. nov. is described from India. This species belongs to the bedoti group of the genus Lophomyrmex, which is characterized by a pronotum with lateral irregular marginations. The new species can be separated from other species within this group by the presence of sub-parallel, blunt and thick propodeal spines of almost uniform diameter and by an obliquely truncate petiolar node.     

Interactions between extrafloral nectaries, ants (Hymenoptera: Formicidae), and other natural enemies affect biological control of Grapholita molesta (Lepidoptera: Tortricidae) on peach (Rosales: Rosaceae)

Extrafloral nectaries (EFNs) are reported to benefit some plants when ants (Hymenoptera: Formicidae) use their secretions and fend off herbivores, but in some cases resulting competitive interactions may reduce biological control of specific herbivores. This research examined the interactions between ants and other natural enemies associated with the EFNs of peach [Prunus persica (L.) Batcsh] and the implications for biological control of a key pest, the oriental fruit moth [Grapholita molesta (Busck)]. Studies using sentinel G. molesta placed on peach trees ('Lovell' cultivar) with EFNs present and absent revealed that several natural enemy groups associated with the EFNs contribute to reductions in G. molesta eggs, larvae, and pupae in peach orchards. Ants on trees with EFNs antagonized the G. molesta egg parasitoid Trichogramma minutum (Riley), but the ants were crucial in reducing G. molesta in both the larval and pupal stages. Overall, individual trees with EFNs experienced higher ant and other (nonant) natural enemy densities and subsequent pest reductions, as compared with trees without EFNs. However, the implications of EFN-natural enemy-pest interactions to orchard-level biological control will likely depend on local G. molesta population dynamics.     

Ant visitation of extrafloral nectaries of Passiflora: the effects of nectary attributes and ant behavior on patterns in facultative ant-plant mutualisms

Extrafloral nectary (EFN) plants are widespread and can be quite species-rich in some communities. Thus, ants that utilize extrafloral nectar may have the opportunity to discriminate among a wide variety of nectar sources, resulting in variation in the ant attention EFN plants receive. In this study, we compare ant visitation rates of three Passiflora species that coexist in an early successional neotropical forest. These three vine species (Passiflora auriculata, P. biflora, and P. oerstedii) differ in their extrafloral nectary structure and placement, and thus may attract different numbers or species of ants. Through censuses of ants tending extrafloral nectaries, we found that P. auriculata received significantly higher numbers of ant visitors than P. oerstedii, but did not differ significantly from P. biflora in its attractiveness to ants. We also found that termite worker baits (simulating herbivores) placed on P. auriculata and P. biflora were discovered by ants significantly more quickly than baits placed on P. oerstedii. In both ant visitation censuses and in termite bait trials, we found no significant associations between Passiflora species and the species of ant visitors. We also performed experimental manipulations of several characteristics of P. auriculata, which resulted in changes in levels of ant visitation. When petiolar nectaries of P. auriculata were experimentally blocked, visitation by the common ant Ectatomma ruidum declined, even though nectaries on the leaf surfaces were still functional. Connections with other vegetation also had an effect on ant visitation. Though experimental creation of connections between growing P. auriculata shoots and other vegetation did not enhance ant visitation, eliminating connections resulted in a significant decline in the number of ant visitors. The results of this study suggest factors that may contribute to variation in ant visitation of extrafloral nectary plants. In addition, this study demonstrates that extrafloral nectary plants co-occurring in a habitat and available to the same ants may differ in patterns of visitation by ants and perhaps in the quality of protection from herbivores that they receive.     

Adoption of lycaenid Niphanda fusca (Lepidoptera: Lycaenidae) caterpillars by the host ant Camponotus japonicus (Hymenoptera: Formicidae)

Caterpillars of the parasitic lycaenid butterfly are often adopted by host ants. It has been proposed that this adoption occurs because the caterpillars mimic the cuticular hydrocarbons of the host ant. This study aimed to examine whether caterpillars of the Japanese lycaenid butterfly Niphanda fusca induce adoption by mimicking their host ant Camponotus japonicus. Behavioral observations conducted in the laboratory showed that most second‐instar caterpillars were not adopted, whereas most third‐instar caterpillars were successfully adopted by host workers. A chemical comparison detected no characteristic differences in the cuticular hydrocarbon profiles between second‐ and third‐instar caterpillars. However, morphological features of the caterpillars differed between the second and third instars; third‐instar caterpillars developed exocrine glands (ant organs) such as tentacle organs and a dorsal nectary organ. These results suggest that multiple chemical signatures, not only cuticular hydrocarbons, may be important for invasion of the host ant nest.