Larval Hemolymph Feeding

Larval hemolymph feeding occurs when adult ants, both queens and workers or queens alone, feed on hemolymph from larvae within their colonies. In these species the workers and queens (or queens only) are incapable of trophallaxis, the direct transfer of food between individuals within the colony, and instead consume the hemolymph of their larvae. Adult ants feed on drops of hemolymph from either punctures in the larval skin or through specialised organs found on the larvae. The larvae themselves survive this feeding with little apparent long-term harm. It is believed that this behaviour has evolved in response to limited and highly variable prey availability or as a mechanism to syncronise brood production, depending on the ants involved.

Larval hemolymph feeding is found primarily in the subfamily Amblyoponinae, where it occurs in all genera, but is also known in a limited number of species scattered across another four subfamilies. Among amblyoponine ants, the occurrence of larval hemolymph feeding has been reported in Adetomyrma sp., Myopopone castanea, Mystrium camillae, Onychomyrmex, Prionopelta kraepelini and Stigmatomma spp. (Ito & Billen 1998; Masuko 2003; Saux et al. 2004; F. Ito, unpubl. data, 1989, 2002, 2010). Larval hemolymph feeding has also been found in a handful of ant species outside of Amblyoponinae, including a few species of Proceratium (Proceratiinae), a few species of Gnamptogenys (Ectatomminae), Leptanilla japonica and Leptanilla clypeata (Leptanillinae), and Calyptomyrmex sp. (Myrmicinae) (Masuko 1986, 1989, 2019; Ito 2001; Ito & Gobin 2008; F. Ito, unpubl. data, 2001, 2010). Larval hemolymph feeding is known from only a small minority (11 genera from five subfamilies) of ant lineages, suggesting that it is a not a particularly successful evolutionary experiment, certainly less adaptive than other modes of food transfer, for example, trophic eggs offered to queens (Peeters, 2020, unpublished).

The better studied taxa showing larval hemolymph feeding include the following:

Leptanilla
The larvae of the migratory Japanese ant Leptanilla japonica have a specialized duct organ on each side of the 4th abdominal segment, the larval hemolymph tap (Masuko, 1989). Workers and queens are able to imbibe hemolymph directly from the larval body cavity through these taps, without the need to pierce the cuticle as occurs in Stigmatomma. While both workers and queens undertake larval hemolymph feeding, this is the sole source of nutrient for the queens.

Leptanilla japonica is cyclical in its brood production with all larvae in a colony developing in concert. When mature larvae are present, the queen significantly increases her level of larval hemolymph feeding. Nourished in this way, she achieves full physogastry within a few days and then lays a batch of 100-200 eggs. It is believed that larval hemolymph feeding facilitates synchronization of brood maturation and concentrated production of eggs by the queen. The larval hemolymph tap has probably evolved de novo in Leptanilla, in relation to cyclical brood production by species with small colony populations.

Myopopone
In Myopopone castanea workers have been observed performing larval hemolymph feeding (Ito, 2010). Workers kept with larvae in the laboratory frequently showed larval hemolymph feeding. This behavior is very similar to that of queens of Stigmatomma silvestrii as reported by Masuko (1986). Workers pinched the larvae with their mandibles and licked hemolymph from the wounds. Workers most often pinched the dorsal integument of the upper abdomen of larvae. Many large larvae had scars which seem to be made during larval hemolymph feeding. During 14 hours of observations of an orphan colony with 25 workers, larval hemolymph feeding was observed 38 times. Twelve of the 25 workers performed larval hemolymph feeding. One worker monopolized more than 50% of larval hemolymph feeding (21 times) and the others only showed the behavior one to three times. Among workers, we never observed aggressive behavior. The relationship between larval hemolymph feeding and ovarian development could not be examined, because colony condition was unfortunately poor at the end of the observation. Additionally, queens have yet to be studied and it is unknown if they also partake in larval hemolymph feeding.

Proceratium
Larval hemolymph feeding similar to that in Stigmatomma has been found to occur in several Proceratium species, including Proceratium itoi (confirmed with behavioral observations, Masuko (1986), Masuko (2019)), Proceratium japonicum and Proceratium watasei. However, only Proceratium itoi has been studied in detail (Masuko, 2019). In this species, the queen feeds exclusively on the older final instar larvae by breaking open a specialized dorsal area. While workers are predatory on spider eggs, it is intriguing that the queen does not feed directly on this easy prey. It is possible that the larvae function as a filter, affording protection against toxins or parasites.

Stigmatomma
Larval hemolymph feeding is best documented within the genus Stigmatomma. These ants have earned the name Dracula Ants because they "drink the blood" of their larvae. Feeding has been directly observed in three species, Stigmatomma oregonense, Stigmatomma pallipes and Stigmatomma silvestrii but likely occurs in many more. In colonies of S. silvestrii (Masuko, 1986) queens pierce the dorsal integument of the upper abdomen of older (5th instar) larvae by pinching with their sharpened mandibular tips, and then feed upon hemolymph leaking from the puncture. In general, queens (inseminated females) perform hemolymph feeding; except when the colony is starved, it is seldom seen in workers and dealate, uninseminated females. The latter castes instead feed directly on prey, the cuticle of which has been opened either by larvae or adults.

Larval hemolymph feeding is not only performed solely by queens, but it is the queen's only way of obtaining nutrients, even when captured prey items (centipedes or mealworms) are available in the brood chamber. However, it is interesting that while larval hemolymph feeding is seen in some colony founding queens, these queens show a strong preference for prey feeding and many do not undertake larval hemolymph feeding at all. It is believed that this low rate of larval hemolymph feeding compared to queens in developed colonies, allows these new colonies to rear the first workers as quickly as possible, thus increasing the likelihood of the colony becoming established.

It is thought that the evolution of larval hemolymph feeding has been driven by the specialised feeding habits of these ants (Masuko, 1986). When prey becomes scarce, Stigmatomma queens, in the absence of regurgitation by the workers, are able to obtain nutrient only from immatures. In such cases irrevocable loss of brood by destructive cannibalism would be selected against, as long as the possibility remained of obtaining prey within a short time. This would favor the evolution of nondestructive cannibalism, such as larval hemolymph feeding. The nondestructive nature of larval hemolymph feeding would be equally or more important in the colony-founding stage when there are few larvae as in the later stages with many. Furthermore, the productivity of A. silvestrii queens is very low: they lay on average only one or two eggs per day, and 5th-instar larvae are present in the nest year round. Therefore, larval hemolymph feeding is accessible to queens all the time, and could sustain their low fecundity despite unstable food conditions. In a literal sense, the larvae serve as "food reservoirs" for colonies. The larval hemolymph is also probably assimilated by queens more efficiently than prey flesh, which might explain why queens of developed colonies persist with larval hemolymph feeding even when prey is available.