colony of Amblyopone oregonensis
is perhaps the most paradoxical element of the North American myrmecofauna.
On one hand Amblyopone ants are regarded as being our most
primitive formicids, an idea not without merit- they are an
ancient lineage of simple-looking, sluggish ants with an exceptionally
basic social repetoire (Holldobler and Wilson 1990, Traniello 1982).
At the same time, we would be hard-pressed to find an ant with a more
apparently derived ecological niche. Most Amblyopone
species, to the extent they are known, are specialist predators. A.
oregonensis, the western North American species of the present
study, appears to prey exclusively on geophilomorph centipedes (Ward
collected a colony fragment of A. oregonensis on 25 June 2004
at Fern Glen, 8 km northwest of Quincy, Plumas Co., California (40º00'N
120º59'W, 1030m). The colony was nesting in a large rotting
Pseudotsuga log in an old growth Douglas fir forest (Fig.1).
This is a known population of A. oregonensis, Ward (1988) conducted
prey choice experiments with ants collected at the same site. At the
time of collection, the colony fragment contained 11 queens, 56 workers,
and hundreds of larvae of varying instars. No cocoons were seen in
the nest at the time of collection. A small number of geophilomorph
centipedes were also collected from the same log and maintained alive
for later feeding to the colony. The nest was then transported to
Creek field station near Truckee, California for observation.
Bringing down the beast:
provided the colony with 10 geophilomorph centipedes (Fig.
3), one per day for ten days. Four centipedes were captured
at Fern Glen when the colony was collected, and six were found under
stones at the Sagehen Creek field station. Geophilomorphs were
difficult to locate at Sagehen Creek, and after 10 days I was unsuccessful
in finding any additional prey items for the colony. The ants
went without food for the remainder of the observation period.
The ants can sense when a centipede has been paralyzed. Once the animal is subdued, the ants cease their stinging behavior and instead masticate the centipede with their mandibles (Fig. 7). To determine whether the ants’ change in behavior was a reaction to a cue from the centipede or a simple matter of elapsed time, I removed one centipede after it had been stung by a single Amblyopone worker and let it sit in a separate vial overnight before reintroduction to the ants. The centipede remained paralyzed during this time. When the ants were allowed to approach this centipede, they did not attempt to sting it again but rather bit and manipulated it with their mandibles, as they do for a more recently-stricken centipede. The cessation of stinging and initiation of mastication, then, seems to be due to a cue from the centipede.
Once in the brood nest, a centipede is not immediately fed to the larvae. Rather, the adult ants spend one to several hours masticating the centipede and licking the juices from the centipede’s wounds (Fig. 9). Ants masticate the centipede by grasping softer places on the centipede integument, often at the base of legs between the sclerites, with the tips of their mandibles and “chewing” by alternately crossing the left then the right mandible over each other several times in a scissoring-motion (Fig. 10). This process often releases droplets of hemolymph from the centipede, which the adult ants readily imbibe.
Larval numbers on a centipede increase over time as the centipede is ‘softened up’ by adult mastication. Within a few hours a centipede is covered in larvae, the larval heads and necks often buried deep within the body of the centipede (Fig 11). In all 10 centipede feedings, the prey was entirely consumed, save the head capsule and other hard sclerotized parts, within 24 hours.
Caught in the act of cannibalism:
was fortunate to observe several instances of larval hemolymph feeding
in A. oregonensis during the short period I kept the colony
in captivity. Four observations were from queens and two were
from workers. The adult ants engaging in LHF appear somewhat
agitated, they quickly grab and handle larvae in a haphazard manner,
squeezing the larvae with their mandibles with more force than is
ordinarily used in larval care and transport, and without apparent
regard to where on the larva they were squeezing (Fig
12). An individual larva is usually repositioned and squeezed
several times by an adult before either being successfully punctured
or passed over by the adult for another larva. Interestingly,
most of the squeezing fails to puncture the larval integument.
However, in all 6 instances where an adult ant succeeded in piercing
the larval integument, the ant had managed to sink the tips of its
mandibles in between the dorsal sclerites of larval abdominal segments
1 and 2, or between segments 2 and 3 (Fig 13), as
though those areas were more vulnerable than elsewhere on the body.
The behavior of the ants did not indicate that the ants were aiming
for these puncture points; rather, it appeared to be more a matter
of persistence and luck.
resulted in a droplet of hemolymph, which the adult ant would rush
forward to lap up with her mouthparts. The extent of the wound
is variable. In one instance, a queen was rewarded not just
with hemolymph but with a stream of fat bodies.
in the brood nest spent considerable time licking the larvae (Fig
16), especially after carrying larvae in their mandibles.
Such grooming behavior may be related to LHF, as the ants tend to
concentrate on the part of the larval body touched by the mandibles
even though the amount of force used by the ants is noticeably less
than in instances where ants succeeding in producing visible drops
of hemolymph from puncture points.
prevalence of LHF may be related to the availability of prey centipedes
in the nest. LHF was not observed in workers until after I ran
out of prey centipedes to feed the colony, although admittedly I only
recorded two observations of worker LHF. In other Amblyopone
species, LHF is only known from queens (Masuko 1986)
Differential vulnerability of larval integuments to puncture
by the observation that LHF did not appear successful until the feeding
ant focused on particular parts of the larval body, I decided to explore
the relative susceptibility of different parts of the larval integument
some parts of the larvae are much more vulnerable than others raises
the question of why adult ants do not appear to be able to target
those sites for LHF, instead of hitting them by what appears to be
an inefficient process of trial and error. It may be that the
larvae are adapted to avoid being fed upon too readily by making it
difficult to find the sites. But this possibility raises the
issue of why the larvae are vulnerable at all, if there is pressure
on them to evolve defensive mechanisms. There may well be an
evolutionary tension between selection on individuals and between
selection on colonies.
the study colony contained 11 queens, only three queens had enlarged
abdomens indicating ovary development (visible distension between
abdominal segments 4 and 5). Two of these were observed laying
eggs in the nest. Interestingly, these three queens also showed
signs of damage beyond anything seen in workers or non-laying queens.
All three were missing parts of their legs in a manner that suggests
past fighting (Fig. 20), even though no aggression
was observed during the course of the study. It may be that
dominance-related conflict and fighting only takes places at particular
times of year, or at particular points in the brood cycle.
Cocoon-spinning behavior is essentially as has been reported in other species with enclosed pupae (Holldobler and Wilson 1990). Adult ants place debris in a bank around larvae of the right age, and the larvae use the debris as scaffolding to produce a network of silk (Fig 22). Once the cocoon is completed, worker ants remove the debris from the silken casing.
recent paper by Saux et al (2004) detailing a molecular phylogeny
of Amblyoponine ants could have some rather bizarre implications for
the ancestral state of all ants, if the specialized predation and
larval cannibalism habits reported here and elsewhere in the ants
are mapped to Saux et al's inferred maximum parsimony and maximum
likelihood phylogenies. The taxon sampling in that study is
complete enough to suggest that the assemblage of taxa that engage
in LHF- Leptanilla, Proceratium, and various Amblyoponines-
spans the root node of all extant ants. These taxa are all specialized
predators on other arthropods, and interestingly, Leptanilla
and many Amblyoponines are restricted to geophilomorph centipedes.
The most parsimonius reconstruction of the common ant ancestor, if
Saux et al's phylogeny is correct, shows an ant with behavior much
like that of Amblyopone. Having a centipede predator
that feeds from larval hemolymph as the archetypal ant is highly speculative,
of course, but still food for a myrmecologist's thoughts.
Holldobler, B. and E. O.Wilson. 1990. The Ants. Harvard University Press, Cambridge (USA).
Masuko, K. 1986. Larval hemolymph feeding: a nondestructive parental cannibalism in the primitive ant Amblyopone silvestrii Wheeler (Hymenoptera: Formicidae). Behav. Ecol. Sociobiol. 19: 249-255.
Masuko, K. 1989. Larval hemolymph feeding in the ant Leptanilla japonica by use of a specialized duct organ, the "larval hemolymph tap" (Hymenoptera: Formicidae). Behav. Ecol. Sociobiol. 24: 127-132.
Saux, C., B. L. Fisher and G. L. Spicer. 2004. Dracula ant phylogeny as inferred by nuclear 28s rDNA sequences and implications for ant systematics (Hymenoptera: Formicidae: Amblyoponinae). Molecular Phylogenetics and Evolution 33: 457-468.
Traniello, J. F. A. 1982. Population structure and social organization in the primitive ant Amblyopone pallipes (Hymenoptera: Formicidae). Psyche 89: 65-80.
Ward, P. S. 1988. Mesic elements in the western Nearctic ant fauna: taxonomic and biological notes on Amblyopone, Proceratium and Smithistruma (Hymenoptera: Formicidae). J. Kans. Entomol. Soc. 61: 102-124.
thanks to Jo-Anne Holley and Phil Ward for commenting on the manuscript