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

Écologie des Forêts de Guyane (UMR-CNRS 8172), CNRS, Campus Agronomique, Kourou cedex, France.
The Science of Nature (Impact Factor: 2.1). 02/2012; 99(4):265-73. DOI: 10.1007/s00114-012-0895-3
Source: PubMed


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.

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    • "Because the preys are very attractive to predatory social wasps and stingless bees (Dejean et al. 2012), the faster the siblings arrive, the less chance there is that a successful nymph will have its prey stolen or even be killed in turn. Moreover, arriving siblings can capture these cleptobionts (see Table 2) as do Allomerus ants (Dejean et al. 2012). "
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    ABSTRACT: Zelus annulosus is an assassin bug species mostly 28 noted on Hirtella physophora, a myrmecophyte specifically associated with the ant Allomerus decemarticulatus known to build traps on host tree twigs to ambush insect prey. The females lay egg clutches protected by a sticky substance. To avoid being trapped, the first three instars of Z. annulosus nymphs remain grouped in a clutch beneath the leaves where they hatched, yet from time to time they climb onto the upper side to group ambush prey. Long-distance prey detection permits these bugs to capture flying or jumping insects that alight on their leaves. Like for some other Zelus species, the sticky substance of the sundew setae of their forelegs aids in prey capture. Group ambushing permits early instars to capture insects that they then share or not depending on prey size and the hunger of the successful nymphs. Fourth and fifth instars, with greater needs, rather ambush solitarily on different host tree leaves, but attract siblings to share large prey. Communal feeding permits faster prey consumption, enabling small nymphs to return sooner to the shelter of their leaves. By improving the regularity of feeding for each nymph, it likely regulates nymphal development, synchronizing molting and subsequently limiting cannibalism.
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    • "This provides the ants with more housing, in turn providing accommodation for the additional winged females produced and enabling the ants to build longer gallery-traps to capture more prey. In addition to this self-sustaining process, the prey carcasses incorporated into the trap to feed the fungus attract necrophagous insects that are then frequently captured [25], while the trapped prey attract cleptobionts that are also captured (Fig. 1a; [34]). "
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    ABSTRACT: Mutualisms, or interactions between species that lead to net fitness benefits for each species involved, are stable and ubiquitous in nature mostly due to "byproduct benefits" stemming from the intrinsic traits of one partner that generate an indirect and positive outcome for the other. Here we verify if myrmecotrophy (where plants obtain nutrients from the refuse of their associated ants) can explain the stability of the tripartite association between the myrmecophyte Hirtella physophora, the ant Allomerus decemarticulatus and an Ascomycota fungus. The plant shelters and provides the ants with extrafloral nectar. The ants protect the plant from herbivores and integrate the fungus into the construction of a trap that they use to capture prey; they also provide the fungus and their host plant with nutrients. During a 9-month field study, we over-provisioned experimental ant colonies with insects, enhancing colony fitness (i.e., more winged females were produced). The rate of partial castration of the host plant, previously demonstrated, was not influenced by the experiment. Experimental plants showed higher δ(15)N values (confirming myrmecotrophy), plus enhanced vegetative growth (e.g., more leaves produced increased the possibility of lodging ants in leaf pouches) and fitness (i.e., more fruits produced and more flowers that matured into fruit). This study highlights the importance of myrmecotrophy on host plant fitness and the stability of ant-myrmecophyte mutualisms.
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    • "155.5±0.7 7/7 100.0 % – – – Coprophaenaeus sp. 353.2±1.9 5/5 100.0 % – – – Reduviidae 45.1±1.4 9/9 100.0 % 6/6 100.0 % NS Total 276/268 97.1 % 562/147 26.1 % – a See Dejean et al. (2012) "
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    ABSTRACT: 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.
    Full-text · Article · Jun 2012 · The Science of Nature
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