340 Diane W. Davidson and Steven C. Cook
modelbehaviorsandinteractionsof antsas“black
boxes.” Within communities of arboreal exudate-
foragers, for example, we have just begun to
identify functional groups, correlated in some
cases with deep phylogenetic disparities in ant
digestive anatomy (Davidsonet al.2004). Here
we review structural and functional variation in
the ant proventriculus (gizzard) and then relate
thisvariationtotheactivitiesandrolesof arboreal
ants in rainforest ecosystems.
Form and function of the ant
proventriculus
The proventriculus controls food flow between
the worker crop (the colony’s “social stomach”)
and the midgut, where digestion occurs, and
it is remarkably diverse in form and function
(Hölldobler and Wilson 1990, p. 290 and figure 1
in Davidsonet al.2004). As early as the 1950s,
the biomechanics of the ant proventriculus were
inferred from histological sections, in elegant
studies by some of the foremost insect biolo-
gists of the past century (Eisner and Wilson
1952, Eisner 1957, Eisner and Brown 1958).This
early work tied anatomical structure of derived
proventriculi to both reliance on liquid foods
and capacity for trophalaxis (regurgitative food
sharing), hypothesized as key to colony social
integration. Proventricular anatomy came to play
a determining role in the designation of tribes
within subfamilies Formicinae and Dolichoderi-
nae (Baroni-Urbaniet al.1992, Shattuck 1992).
However, in recent work based on anatomical
characters, Bolton (2003) recognized no tribes
within Dolichoderinae, and by his proposed revi-
sion of formicines, the derived or “sepalous”
proventriculus is either homoplasious in various
tribes or has been lost repeatedly following a sin-
gle origin. Thus, although linkages likely exist
between derived proventriculi and liquid diets, the
case for such associations must be made anew
based on current phylogenetic hypotheses.
Formicines and dolichoderines are most promi-
nent among the exudate-foragers from which
canopy dominants are drawn. Other arbo-
real exudate-foragers include Ectatomminae
(EctatommaandGnamptogenys), the monotypic
Paraponerinae (Paraponera), some Ponerinae
(PachycondylaandDiacamma), and Myrmicinae
(especiallyCrematogaster,Myrmicaria,Cephalotes,
andCataulacus). Liquids are transported inter-
nally (in the crop) in all but the Ectatommi-
nae, Paraponerinae, and Ponerinae, which carry
food droplets in the mandibles. Early investiga-
tors (especially Eisner 1957) noted that several
independent lineages specializing in liquid foods,
and carrying them internally, exhibited “passive
damming” of crop fluids against posterior flow,
by virtue of sclerotization of the anterior proven-
triculus and/or evolution of an “occlusory tract.”
Simultaneous with each of these innovations,
loss of key muscle groups provided energetic sav-
ings and prevented dilution from compromising
enzyme function.The most highly derived proven-
triculi include the sepalous formicine organ and
the unique filtering shield associated with pollen-
feeding inCephalotes(Cephalotini, Myrmicinae;
see Baroni-Urbani and Andrade 1997, Roche
and Wheeler 1997, Andrade and Baroni-Urbani
1999). Additionally, several small-bodied genera
in one or more clades of the Dolichoderinae have
highly modified proventriculi that, in their most
derived state, appear functionally convergent with
the sepalous formicine proventriculus (Eisner and
Wilson 1952). In both cases, passive damming
is so complete as to require canals to pass liquid
foods posteriorly from the crop to the proventric-
ular bulb, which, in turn, delivers liquids to the
midgut.
Although early investigators mentioned only
intranidal functions of derived proventriculi in
liquid-feeding ants, novel approaches and tools
have recently raised new questions about how
proventricular anatomy has influenced foraging
behaviors. Recent field measures of liquid-feeding
performances in tropical and temperate ant taxa
reveal associations between passive damming
and two body size-adjusted measures of liquid-
feeding performance: relatively large maximum
load sizes in all such taxa, and rapid drinking
rates in formicines and dolichoderines with the
most derived proventriculi (Davidsonet al.2004).
In vivo biomechanical studies of feeding ants,
using synchrotron radiation, are currently defin-
ing determinants of feeding rates more precisely
(Cook 2008).