A cuckoo-like parasitic moth leads African weaver ant colonies to their demise

Study sites and focal species

Field studies were conducted from 205 O. longinoda colonies in Gabon (Forêt des Abeilles; 0°40’S, 11°54’E; five colonies) and in several locations in Cameroon: in the city of Yaoundé (03°52’N, 11°31’E; 39 colonies) and the surrounding area, including Batchenga (03°51’N, 11°42’E; 21 colonies), Kala (03°50’N, 11°21’E; 46 colonies), Matomb (03°53’N, 11°14’E; 34 colonies), Mbalmayo (03°29’N, 11°30 ′E; 14 colonies) and Nkolbisson (03°59’N, 11°28’E; 32 colonies); and in areas close to Edea (3°47’N, 10°08’E; 11 colonies), Kribi (2°56’N, 9°54’E; seven colonies), Ebolowa (2°54’N, 11 °09’E; five colonies) and Buéa (4°09’N, 9°14’E; four colonies).

Oecophylla longinodaof the subfamily Formicinae, is a “territorially dominant arboreal ant species”1,25,26,27,28 characterized by large, polydomous (multiple nests) tree colonies; the workers build the nests by manipulating larvae to glue leaves together with the silk they produce. Unlike most ant ants, the larvae pupate without wrapping themselves in silk cocoons. Although this species is abundant in tree plantations where it is used as a biological control agent, in natural conditions this species occurs in relatively young or recently disturbed vegetation, whereas very old tropical rainforest trees are more likely to shelter trees, which nest in boxes. crematogaster spp.1,25,26,27,28.

As for most other ant species, oecophylla workers cannot mate due to lack of proper apparatus, but majors have fully functional ovaries and thus can lay trophic eggs which are generally given to the queen. They produce unfertilized eggs with chorion that can develop into fully functional males when the queen dies29. Because the colonies are very densely populated (more than 500,000 individuals)1), it is difficult to conduct experiments on it. Swarms occur all year round (AD, pers. obs.) allowing us to compare the production of winged sexes and moths.

In moths, the number of larval stages can vary intraspecifically. In the genus Eublemma (Noctuidae; Acontiinae), this number varies from eight to ten30.31 making it difficult to identify the different stages. Therefore, we distinguish only four “steps” in the larval life of E. albifascia (see Fig. 1 for the entire life cycle). Newly hatched caterpillars, or first instars, develop into 4 mm long second instars often found among the ant brood. The “intermediate” instars are caterpillars with a length of 8-20 mm that are able to attract trophallaxis from workers, the same applies to the last instars, up to 40 mm long, which then pupate.

Figure 1: Representation of the different phases in the life cycle of Eublemma albifascia.

(a) Egg cluster (N = 113). (b) Second stage caterpillar transported by a minor worker. (c) On the left, a trophallactic exchange between a caterpillar in the last instar and a large worker while another worker licks the caterpillar’s cuticle; to the right (see arrow), a worker bee takes in the anal secretion of another caterpillar in the last instar. (d) Late instar caterpillars in a highly parasitized colony with many males. (e) A group of agglutinated cocoons. (f) An adult moth. (g) A drawing representing the contracted gaster of a Oecophylla longinoda queen in certain parasitized colonies (I) and a “normal queen” in control colonies and other parasitized colonies (II).

Voucher specimens of ants, moths (identified by Dr. MR Honey) and parasitic wasps (identified by Dr. J. LaSalle) were deposited at the Museum of Natural History, London.

The search for parasitized Oecophylla longinoda colonies

To evaluate the degree of parasitism by: E. albifascia caterpillars, all 205 . nests O. longinoda colonies (N ≥ 20 to avoid colony initiation) on small trees (<6 m high) to allow easy access were first inspected externally to verify that clusters of Eublemma eggs had been laid on the leaves of the nests; if so, then we counted the number of eggs. The nests were then opened to verify their contents, including the presence of caterpillars (final instars were counted), treated queen(s), winged males and females as well as their pupae (plus large final instar female larvae). Although the ants were very alarmed, this process is not destructive (except for the colonies collected for specific studies, see below) and the workers restored the opened nests (see the opening of the nests and the observations in artificial nests32). In addition, ≈ 40 additional colonies were inspected during preliminary and additional studies.

Behavioral relationships between Eublemma albifascia caterpillars and Oecophylla longinoda workers

Laboratory tests were performed at 13 O. longinoda colonies that provide shelter Eublemma albifascia caterpillars would gather in Yaoundé or Nkolbisson to avoid transporting a high rate of caterpillar mortality over long distances. Nests were collected by chopping down the supporting branches with a clipping pole, placing them in plastic bags and taking them to the laboratory. They were installed in 40 × 20 × 5 cm plastic boxes with a transparent cover (which we covered with a screen outside the observation periods to prevent the workers from covering this surface with silk) that opened onto a table through holes of diameter of 0.8 cm, allowing the passage of emerging adult moths. The bases of the tables were placed in oil-filled boxes to prevent the workers from escaping. Extrafloral nectar-bearing pot plants (Alchonea chordifolia or Hibiscus spp.) were placed on the tables to allow the workers to forage for nectar and honeydew while observing scale insects on these plants. The workers wove new nests in the foliage of these plants. The colonies were also delivered ad libitum with water, honey and prey (usually cricket larvae and small mealworms).

Although the workers quickly became accustomed to being observed, most of the observations inside the nest were made at night with red light. Other observations were made between 8:00 AM and 12:00 PM to record the number of cases where a large worker bee delivered trophic eggs to the queen in control colonies and to four final instar caterpillars in parasitized colonies.

To verify whether E. albifascia caterpillars got the colony odor inside their host nests or, rather, have an intrinsic, calming odor to their host ants, we performed two series of confrontation experiments based on the idea of ​​colony partner recognition11. A control experiment was performed with 40 O. longinoda workers were transferred from one nest to another from the same colony and 40 others between two nests from two different colonies. We then transferred 20 caterpillars from one nest to another from a neighboring alien colony. Then 20 other caterpillars were transferred from one nest to another nest belonging to the same colony (two colonies used, one of which was raised in artificial nests).

The impact of caterpillar pressure on the sex ratio in Oecophylla longinoda colonies

All nests from each colony were collected, placed in large plastic bags and transported to the lab where they were placed in a refrigerator. We then counted the caterpillars in parasitized colonies, as well as the pupae and winged males and females in both types of colonies. While doing this, we noticed that parasitized colonies can have a queen that is morphologically similar to that in control colonies (hereinafter “normal queens”) or a queen with a “contracted gaster” (Fig. 1).

We first used a general linear model (GLM) (R v. 2.14.2 software; R Development Core Team used for all statistical comparisons) to test the hypothesis that colonies were highly parasitized (N = 8; they shelter 131 , 139, 144, 151, 177, 184, 201 and 214 caterpillars of the last instar, respectively; Table 1) contained more males than control colonies (N = 12; no caterpillar found regardless of stage; queens with a normal gaster). Since our response variable (i.e., the sex of the ants) was binary, we modeled it with a binomial error distribution and tested the effect of the presence of parasites on the probability of being male. These two batches of colonies consisted of a similar number of nests (mean ± SE: 28.75 ± 2.00 ‘nests’ per control colony vs. 29.50 ± 2.65 ‘nests’ per parasitized colony; t = 0.23; 18df; P = 0.82).

Table 1 Composition of the colonies studied.

Second, in the four parasitized colonies with a contracted gaster queen (i.e., with 206, 241, 260, and 274 final instar caterpillars, respectively; Table 1), the male pupae and adults were too numerous to count. So we counted the pupae and winged females in the field and checked for worker puppets.

Third, the same process was applied to six parasitized colonies that had lost their queen (ie with 55, 64, 69, 288, 235 and 359 caterpillars in the last instar, respectively); some nests belonging to the first three colonies were packed with agglutinated cocoons (Fig. 1 and Table 1). The number of pupae and winged males and females, corresponding to discrete, positive variables, was compared using a Poisson error distribution in a GLM.

After opening the nests of both the control colonies and the parasitized colonies, we recorded the number of eggs around the queen in each colony on an ordinal scale or collected them with a fine paintbrush, and placed them in a box for counting in the laboratory. . To test the effect of parasites on egg number, we used the nonparametric Wilcoxon rank test to account for the ordinal nature of the response variable (Table 1).

famine Oecophylla longinoda queens in parasitized colonies

For two O. longinoda control colonies and four parasitized colonies grown in the lab, we performed 54 series of 10-minute observations (9 hours), measuring the duration of the worker-queen trophallaxis in the first case and the worker-queen trophallaxis each time it occurred. caterpillar trophallaxis in the latter case (one caterpillar targeted in each colony during each observation session). The duration of the trophallaxis, an overdispersed positive variable, was compared using a GLM with a quasi Poisson error distribution. The number of trophallactic events, a discrete and positive but not overspread variable, was compared using a GLM with a Poisson error distribution.

For the same colonies, we also compared, using a GLM with a Poisson error distribution, the number of trophic eggs delivered by large workers to the queens in control colonies and to caterpillars in parasitized colonies (20 series of 10-minute observations per queen and per caterpillar) .

Using a microscale (Mettler® AE 260), we weighed small, medium and large workers, males, winged queens and mated queens (N = 10 in each case) taken from control colonies, as well as late instar caterpillars (N = 28). ) as “normal” queens (N = 5) and queens with a contracted gaster (N = 4) from parasitized colonies. The weight of 10 queens from control colonies and nine from parasitized colonies was compared with a classical GLM with a normal error distribution.

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