The capacity of a Myrmica ant nest to support a predacious species of Maculinea butterfly

Abstract

Caterpillars of Maculinea arion are obligate predators of the brood of Myrmica sabuleti ants. In the aboratory, caterpillars eat the largest available ant larvae, although eggs, small larvae and prepupae are also palatable. This is an efficient way to predate. It ensures that newly-adopted caterpillars consume the final part of the first cohort of ant brood in a nest, before this pupates in early autumn and becomes unavailable as prey. At the same time, the fixed number of larvae in the second cohort is left to grow larger before being killed in late autumn and spring. Caterpillars also improve their feeding efficiency by hibernating for longer than ants in spring, losing just 6% of their weight while the biomass of ant larvae increases by 27%. Final instar caterpillars acquire more than 99% of their ultimate biomass in Myrmica nests, growing from 1.3 mg to an estimated 173 mg. A close correlation was found between the weights of caterpillars throughout autumn and the number of large ant larvae they had eaten. This was used to calculate the number of larvae eaten in spring, allowing both for the loss of caterpillar weight during winter and the increase in the size of their prey in spring. It is estimated that 230 of the largest available larvae, and a minimum nest size of 354 M. sabuleti workers, is needed to support one butterfly. Few wild M. sabuleti nests are this large: on one site, it was estimated that 85% of nests were too small to produce a butterfly, and only 5% could support two or more. This prediction was confirmed by the mortalities of 376 caterpillars in 151 wild M. sabuleti nests there. Mortalities were particularly high in nests that adopted more than two caterpillars, apparently due to scramble competition and starvation in autumn. Survival was higher than predicted in wild nests that adopted one caterpillar. These caterpillars seldom exhaust their food before spring, when there is intense competition among Myrmica for nest sites. Ants often desert their nests in the absence of brood, leaving the caterpillar behind. Vacant nests are frequently repopulated by a neighbouring colony, carrying in a fresh supply of brood. Maculinea arion caterpillars have an exceptional ability to withstand starvation, and sometimes survive to parasitize more than one Myrmica colony. Despite these adaptations, predation is an inefficient way to exploit the resources of a Myrmica nest. By contrast, Maculinea rebeli feeds mainly at a lower trophic level, on the regurgitations of worker ants. Published data show that Myrmica nests can support 6 times more caterpillars of Maculinea rebeli than of M. arion in the laboratory. This is confirmed by field data.

Polymorphic growth rates in myrmecophilous insects

“…It is known that Myrmica colonies frequently disperse after M. arion has destroyed their brood because their normal social focus has been lost and the M. arion caterpillar (unlike those of cuckoo-feeding Maculinea species) is not treated as a substitute (Thomas & Wardlaw 1992). Under these circumstances, the caterpillar is left behind in the empty nest where it awaits the arrival of an o¡shoot of a neighbouring host ant colony.…”

“…With two exceptions, these were kept singly either in small boxes or using the`walnut method' with their obligate host Myrmica sabuleti Meinert. All were provided with surplus food, but in four di¡erent diets/treatments: large ant larvae only (nˆ6), ant pre-pupae only (nˆ6) and under walnuts containing mixed ant brood and M. arion from France (nˆ5) or Sweden (nˆ9) (see Thomas & Wardlaw 1992). Since M. arion caterpillars are very sensitive to disturbance and because it is virtually impossible to rear them to pupation, all were weighed only once after eight weeks with ants, towards the end of the autumn growth period.…”

“…The mean weight of Microdon biomass per ant Myrmica scabrinodis nest in May was 561.6 § 66.0 mg (nˆ18). Assuming the same feeding e¤ciency (Thomas & Wardlaw 1992) as of M. arion larvae which take one year to develop and that Microdon is an obligate predator of ant brood, this biomass is equivalent to a mean colony size for Myrmica scabrinodis of 1148 workers to support the predators. In fact, the average colony size for this species in the UK is 462 workers (Wardlaw & Elmes 1996).…”

Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism

“…Equally widespread are species that exploit these partnerships: rhizobia that use plant sugars but fail to fix nitrogen (3), cleaner fish that consume tissue but ignore ectoparasites (4), and caterpillars eat the broods of their ant defenders (5). Because natural selection should favor such freeloaders if they can reap benefits without reciprocating, the persistence of mutualisms is a central puzzle in biology (6).…”

Development of parasitic Maculinea teleius (Lepidoptera, Lycaenidae) larvae in laboratory nests of four Myrmica ant host species

“…The growth pattern of M. teleius larvae inside colonies of M. scabrinodis, M. ruginodis and M. rubra was similar although larvae reared by nests of the latter two species were slightly heavier 18 weeks after adoption. The general larval growth pattern observed in cuckoo Maculinea comprises an increase of body mass at the beginning of the larval development during the first week of adoption and again shortly before pupation, as well as a slight decline of body mass during winter (Thomas and Wardlaw, 1992;Elmes et al, 1991b;Sielezniew and Stankiewicz, 2007;Schönrogge et al, 2000;Sielezniew and Stankiewicz, 2007;Nash et al, 2011). In contrast to cuckoo Maculinea butterflies, M. teleius larvae seem to grow very slowly during the early larval development and the mean body mass reached at the beginning of the winter diapause was 14.6 mg (Fig.…”