The role of resource imbalances in the evolutionary ecology of tropical arboreal ants

Biological Journal of the Linnean Society (1997), 61: 153–181. With 2 figures

The role of resource imbalances in the evolutionary ecology of tropical arboreal ants DIANE W. DAVIDSON Department of Biology, University of Utah, Salt Lake City, UT 84112, U.S.A. Received 26 July 1996; accepted for publication 13 December 1996

In numbers and biomass, ants (Hymenoptera, Formicidae) often dominate arthropod faunas of tropical rainforest canopies. Extraordinary ant abundance is due principally to one or a few species able to tap the high productivity of canopy foliage by feeding on plant and homopteran exudates. Prior studies of nitrogen isotopic ratios show that exudate-feeders derive much of their nitrogen (N) by processing large quantities of N-poor, but carbohydrate (CHO)-rich, exudates. CHOs in excess of those that can be coupled with protein for growth and reproduction (postulated as the colony’s first priorities) may be directed at little cost and some profit to functions that increase access to limiting protein. High dietary CHO:protein ratios for exudate-feeders appear to subsidize ‘high tempo’ foraging activity, defence of absolute (level III) territories, and production of N-free alarm/defence exocrine products that enhance ecological dominance in contests with other ants. Among organisms (e.g. plants and Lepidoptera) symbiotic with ants, CHO:protein ratios of ant rewards may control both the identities of ant associates and the quality of ant-rendered services. Dietary ratios of CHO:protein play an important and previously unrecognized role in the ecology and evolution of ants generally. Modifications of worker digestive systems in certain ant subfamilies and genera represent key innovations for handling and processing large volumes of liquid food. The supreme tropical dominants are species released from nest site limitation and able to place their nests in the vicinity of abundant exudate resources. Polydomy appears to be typical of these species and should produce energetic savings by taking colony fragments to the resource.  1997 The Linnean Society of London

ADDITIONAL KEY WORDS:—ant-plant interactions – canopy samples – exocrine chemistry – foraging tempo – Homoptera – lycaenoid butterflies – proventriculus – resource balance model – symbioses – territoriality.

CONTENTS

Introduction . . . . . . . . . . . . . Ant abundance in the tropical arboreal zone What kinds of ants are superabundant? . . Diets and dominance . . . . . . . . . . Key innovations for feeding . . . . . . Lessons from plant ecology . . . . . . Other considerations . . . . . . . . . . Nests near the fuel pump . . . . . . . 0024–4066/97/060153+29 $25.00/0/bj960128

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154 155 158 159 160 162 171 171

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Resource balance in relationships of ants Generalizing the resource balance model Acknowledgements . . . . . . . . References . . . . . . . . . . .

with . . . . . .

plants . . . . . .

and butterflies . . . . . . . . . . . . . . .

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173 175 175 176

INTRODUCTION

Ants are among the most numerous and readily observed arthropods of tropical forests. Indeed, based on their numbers, standing biomass, and frequency in fogging samples, and considering their many effects on other species, they are arguably the dominant arthropod family in the canopies of lowland tropical rain forests (Tobin, 1995; Davidson & Patrell-Kim, 1996). The exceptional abundance of ants in tropical forests led Tobin (1991, 1994) to question how ants, which have been presumed to feed mainly as predators and scavengers, can possibly be so abundant, often more abundant than their prey. The explanation given most credence by Tobin was that ants feed mainly as herbivores, and that this is especially true of members of the worker caste, whose activities are fuelled mainly by carbohydrates. Other hypotheses are explored briefly in Tobin (1991) and Davidson & Patrell-Kim (1996). Davidson & Patrell-Kim (1996) were initially skeptical of Tobin’s favoured hypothesis, because the protein building blocks needed for colony growth and reproduction are poorly represented in plant resources generally, and might not suffice for colony growth and reproduction. Nevertheless, they found credible evidence to support Tobin’s view. First, one or a very few ant species often account for most of the relative ‘excess’ of ants, and all of the abundant ants feed extensively on plant and homopteran exudates. Second, although amino acids and peptides are relatively minor components of exudates (Auclair, 1963; Baker, Opler & Baker, 1978; Harborne, 1982), stable isotope analyses revealed significantly lower d15N values in exudate-feeding ants than in predatory species. This result appears to indicate that exudate-feeders in at least some of the genera of very abundant canopy ants obtain their nitrogen at lower trophic levels than do more strictly predatory ants (see e.g. Miyake & Wada, 1967 and DeNiro & Epstein, 1981, for increasing d15N at successive trophic levels). Third, Davidson & Patrell-Kim found that % dry weight nitrogen content was lower in exudate-feeders than in more strictly predatory ants. One interpretation of this result (but see Maschwitz & Kloft, 1971) is that ants with relatively N-poor diets invest less nitrogen in costly protein-rich exoskeleton. Finally, Davidson and Patrell-Kim noted published evidence that homopteran exudates are often enriched relative to plant sap by the upgrading of non-essential to essential amino acids by intracellular bacterial symbionts of Homoptera (Gray, 1952; Salama & Rizk, 1969; Douglas, 1989; Prosser, Simpson & Douglas, 1992; Baumann et al., 1995), and they speculated that bacterial symbionts of some exudatefeeding ants might serve a similar function. This hypothesis is bolstered by the recent identification of bacterial symbionts of Camponotus ants as the sister group to endosymbionts of aphids and tsetse flies (Schro¨der et al., 1996). Ants that depend substantially on exudates for amino acids and peptides must process large volumes of exudates to meet their protein needs, and such species would be expected to have digestive systems adapted to gather, store and process large volumes of liquid food efficiently. Since exudates are rich in carbohydrates (CHOs), ‘excess’ carbohydrates, over and above quantities that can be paired with limiting protein for growth and reproduction, might be diverted at little cost and

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some profit to activities increasing rates of acquisition of nitrogenous resources, including perhaps essential amino acids that are relatively poorly represented in exudates. A resource balance model from plant biology (Bryant et al., 1985) provides a useful point of departure for considering the effects of CHO:protein imbalances on ant ecology, evolution and behaviour. Before investigating the utility of this approach, I briefly review the evidence for the remarkable abundance of ants in rainforest canopies of the lowland wet tropics, and examine the identities and characteristics of particularly abundant ant taxa. Ant abundance in the tropical arboreal zone Comprising between 9% and 70% of all arthropods sampled by insecticidal fogging (mainly) and other techniques, and from 17% to 50% of arthropod biomass (Tobin, 1995), tropical arboreal ants of lowland rain forests are more remarkable for their abundance in canopy samples than for their diversity (e.g. Erwin, 1983; Stork, 1988, 1991; Stork & Brendell, 1990; Tobin, 1991, 1994; Floren & Linsenmair, 1997; Davidson & Patrell-Kim, 1996). Thus, ants dominated both the numbers and biomass of arboreal arthropods in all ten samples from three forest types fogged by Erwin (1983) in central Amazonia. They were also numerically dominant in each of 19 first-time fogged samples from individual trees in Borneo, where they comprised a mean of 56% of all arthropod individuals in aggregate samples (Floren & Linsenmair, 1997). Calculations by Stork (1988) provide additional perspective on ant diversity and abundance. First, ants make up just a slightly greater percentage of arboreal arthropod diversity in tropical than in temperate samples, but they show much higher relative abundance in the former than the latter regions. Second, in Stork’s comparisons of arthropod samples from the ‘five principal biotopes’ of lowland rain forest in Seram, Indonesia, ants dominated the faunas to a much greater degree in the canopy than in the other four biotopes (tree trunks, ground vegetation, leaf litter and soil; see also Adis & Schubart, 1985). There, ants contributed approximately half of an estimated 12 million individual arthropods. Overall then, the remarkable numbers and biomass of ants are principally a phenomenon of the tropical arboreal zone. Ants sampled by insecticidal fogging and other techniques are not equally abundant; rather, one or a few ant species can be extraordinarily common. In Borneo, for example, the most common arthropod species in six of ten fogged trees was an ant, and ants comprised four of the five most common species in the combined samples (Stork, 1991). A single species, Myrmicaria sp. 1, ranked first in one sample and was among the three most common species in three other trees. Also in Borneo, Floren & Linsenmair (1997) encountered 192 ant species in canopy samples from 29 foggings of 19 trees, but classified only 2–3 species as numerically dominant in individual samples, and found a total of just 27 species to be represented by >1000 individuals in any sample. Together, two species of Dolichoderus were numerically dominant on a total of ten tree crowns. In Brazil and Peru, respectively, a member of the Crematogaster brevispinosa species group accounted for about 53% of ant numbers in each of two samples (Adis, Lubin & Montgomery, 1984), and Dolichoderus bispinosus Roger, for more than 70% of the biomass of the six most common ant species (Tobin, 1991). Wilson (1987) analysed canopy samples from a

a (fauna)Am-fr

 Crematogaster cf. limata var. parabioticaP,P

(tree)Am (tree)Am (tree)Am (tree)CA-b (tree)Am (tree)Am (tree)Am (tree)Am-b (tree)CA (ea of 2 trees)B (ea of 6 trees)B (tree)B (ea of 3 trees)B (fauna)NG

a a a a a a a a a a a a a a

a (tree)Am

 Azteca sp.P?,M?

Azteca sp.P?,M? Azteca sp.P?,M? Azteca sp.P?,M? Azteca sp.P?,M? Dolichoderus lutosus Smith?,? e Dolichoderus lutosus?,? Dolichoderus lutosus?,? Dolichoderus bispinosus?,? Dolichoderus sp.?,? Dolichoderus sp.?,? Dolichoderus sp.P,P f Dolichoderus sp.P,P f Technomyrmex sp.?,? Technomyrmex albipes?,?

b [b]

a (25m2 × 10m)Au-b a (tree)B

Oecophylla smaragdinaP,M Plagiolepis sp.?,?

b

(b) (b) (b) (b) (bc) (b) (b) b (b) (b) b b [b] b

(b)

b (b) (b) b

(fauna)SA-fr (tree)B (ea of 2 trees)B (fauna)Af-b

EFN’s &/or Homoptera

a a a a

Dominancec

 Camponotus femoratusP,P Camponotus?,? Camponotus?,? Oecophylla longinodaP,M

Ant taxab

b?

(c) (c) (c) (c) (c?) (c?) (c?) b? (c) [c] c? c? [b] a

(c?)(d)

bc ?

b? ? ? bc

Level III territoriesd

Tobin, 1991 and PC; (b) Leston, 1978 J. Tobin PC; (b) Oliveira & Brandao, 1991; (c) Leston, 1978 Floren & Linsenmair, 1997; (b) Way & Khoo, 1991; (c) Way & Khoo, 1989 Floren & Linsenmair, 1997; b. Maschwitz et al., 1988, 1991 Way & Khoo, 1991

(a) Wilson, 1987; b. Davidson, 1988

(b) Floren & Linsenmair, 1997 (a) Room, 1975

(a) (a) (a) (a)

(a) J. Tobin, PC (a) Adis et al., 1984; (b) Oliveira & Brando, 1991; (c) = Leston, 1978

continued

(a) Adis et al., 1984; (b) Adams, 1990a, Oliveira & Brandao, 1991; (c) = Leston, 1978; (d) Adams, 1990a, 1994

Wilson, 1987; (b) Davidson, 1988 Stork, 1991; (b) Dumpert et al., 1989; Maschwitz et al., 1992 Floren & Linsenmair, 1997 Majer, 1976a; (b) Way, 1954; (c) Majer, 1976c; Ho¨lldobler & Wilson, 1977 a & c, 1978; Jackson, 1984 (a) Majer, 1990; (b) Greenslade, 1971; Ho¨lldobler, 1983 (a) Floren & Linsenmair, 1997; (b) Wheeler, 1910, Oliveira & Brandao, 1991

(a) (a) (a) (a)

References

T 1. Primary dominants of individual canopy samples (or local faunas, where data not by sample), as calculated by numbers, biomass, or frequency in samplesa

156 D. W. DAVIDSON

brevispinosaP,? brevispinosaP,? striatulaP,? sp.?,?

b

(b)[c]

(b) (b) (b) (b) (b) (b)[c]

b b b (b)

EFN’s &/or Homoptera

c(I, II?)

(b)[c]

[c] [c] [c] [c] [c] (b)[c]

c c ac [c]

Level III territoriesd

(a) J. Tobin PC; (b) Young & Hermann 1980; Baird 1986; Oliveira & Brandao 1991; (c) Breed et al. 1991

(a) Stork, 1991; (b) Maschwitz et al., 1988, A. Weissflog & U. Maschwitz PC for M. arachnoides, var. lutea; (c) Dejean et al. 1994 for M. opaciventris

(a) Floren & Linsenmair, 1997

(a) Majer, 1976 a; (b) Strickland, 1951; (c) Dejean et al., 1994 (a) Stork, 1991; (b) Fiala & Maschwitz, 1991; (c) Majer, 1976b; Leston, 1978, Dejean et al., 1994; Adams, 1990a, 1994; Davidson, 1988

(a) Adis et al., 1984; (b) E. Adams, PC; (c) Adams, 1990a, 1994

References

a

Letters entered in columns and reference list identify the source of information (PC = pers. comm.) verifying dominance of canopy arthropod or ant samples (a), tending of Homoptera (b), and level III territoriality (unless levels I or II are indicated) (c); they index references from the same line or, if no reference appears on that line, the nearest previous line with a reference given after that letter. Letters in parentheses indicate that references are for species not necessarily but possibly identical to species in canopy samples [#], or for congeners definitely not identical to species in canopy samples [ ]. ‘Possibly identical’ is given wide latitude; e.g. although Weissflog & Maschwitz have found Myrmicaria arachnoides var. lutea in Peninsular Malaysia and not Borneo, there is some likelihood that the species occurs in Borneo and has not been reported from there yet. Some of the studies included here found secondary and tertiary dominants, but these were often considerably less common than the primary dominant, and I standardized the data by reporting only the latter. Two species were reported from the study by Wilson (1987); given the system of reporting (number of tray records, or frequency in trays), and wide discrepancy in body sizes of the two species, it was difficult to judge which would have been the primary dominant. I omitted Wilson’s Solenopsis (Diplorhoptrum) parabiotica, which parasitizes brood of ant-garden ants and has tiny workers. b Superscripts: P,P = polydomous, polygynous; M = monogynous; M? = probably monogamous; ? = unknown. Uncertainty for Myrmicaria species is based on whether or not Stork’s Bornean collections were M. arachnoides var. lutea, which has only been reported from Peninsular Malaysia. Many Azteca species are polydomous (e.g. Adams, 1990a and pers. obs.) and monogynous, but these traits cannot be assigned definitively to the unidentified Azteca species sampled. c Dominance of individual trees or local faunas. Superscripts: geographic regions (Af = Africa; Am = Amazonia; Au = Australia; B = Borneo; CA = Central America; NG = New Guinea), followed by ‘– type of sample’ (b = biomass; fr = frequency of records in samples, otherwise numbers). d ‘?’ denotes weak evidence not based on either experiments or statistical tests. e Classification of the Dolichoderinae follows Shattuck, 1992b. f Members of the Dolichoderus thoracicus group.

a (tree)CA-b

 Paraponera clavataP,M?

(tree)B (tree)B (tree)B (ea of 3 trees)B (tree)B (tree)B

(tree)Am (tree)Am (fauna)Af (tree)B

a (tree)B

a a a a a a

a a a a

Dominancec

Myrmicaria sp.P?,P?

Crematogaster sp.?,? Crematogaster sp.?,? Crematogaster sp.?,? Crematogaster sp.?,? Crematogaster sp.?,? Myrmicaria sp.P?,P?

Crematogaster Crematogaster Crematogaster Crematogaster

Ant taxab

T 1. continued

RESOURCE IMBALANCES IN TROPICAL ARBOREAL ANTS 157

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D. W. DAVIDSON

tropical moist forest in western Amazonia and noted that aggressive ant-garden ants (Camponotus femoratus Fabricius) occurred in 90% of all samples, and together with ‘parabiotic’ (cohabiting) species, comprised about a quarter of all species- and genuslevel records from the sample trays. What kinds of ants are superabundant? Table 1 (column 1) lists the single most common ant species as ranked by numbers, biomass or frequency of records in various canopy samples (column 2). Note that individual entries can refer to multiple independent fogging samples (range of 2–6), and that apparently repetitive entries in the table (e.g. various listings of Azteca in samples by Adis et al., 1984) represent unidentified but different species within the genera in question. Contributions of small-bodied species, e.g. Plagiolepis, Azteca, Technomyrmex and Crematogaster, might be somewhat inflated by relying on numerical abundance rather than biomass. Although there is no ready solution to this problem, the number of genera in Table 1 would have increased just slightly had second and third most abundant species been included. A surprisingly small number of genera contribute repeatedly to the list in Table 1. Species of Camponotus dominate canopy samples from both Peru (Wilson, 1987) and Borneo (Stork, 1991; Floren & Linsenmair, 1997). Also on the list are both of the extant Oecophylla species, one from Africa (Majer, 1976a) and the other from Australia (Majer, 1990). Species of the Neotropical genus Azteca dominate samples from Brazil (Adis et al., 1984) and Panama ( J. Tobin, pers. comm.), and those of Dolichoderus, samples from Brazil (Adis et al., 1984), Peru (Tobin, 1991), Panama ( J. Tobin, pers. comm.) and Borneo (Floren & Linsenmair, 1997). Technomyrmex species come from both Borneo (Floren & Linsenmair, 1997) and New Guinea (Room, 1975), and Crematogaster, from samples in Peru (Wilson, 1987), Brazil (Adis et al., 1984), Africa (Majer, 1976 a), and Borneo (Stork, 1991; Floren & Linsenmair, 1997). Only Plagiolepis, Myrmicaria and Paraponera (a New World endemic) are listed from a single region. What shared traits might help to explain the abundances of ants in these nine genera? The feature that most unites these genera is their strong reliance on plant and homopteran exudates (Table 1, column 3). Represented here are four of the five ant subfamilies in which at least some species depend directly and substantially on plant resources, and in which at least some obligate plant-ants have evolved (Davidson & McKey, 1993). Missing are only the Pseudomyrmecinae, comprised of just three ant genera, one recently discovered and monotypic (Ward, 1990). Although pseudomyrmecines might be missing from Table 1 simply because twig-nesters are undersampled by fogging, other explanations are also possible. Relative to the ants in Table 1, pseudomyrmecines tend to be timid and subordinate, occupying dead and live plant stems whose inside diameters (author’s unpub. data) or entrance holes (Klein, Maschwitz & Kovac, 1993) barely exceed the diameters of the highly streamlined workers. A substantial portion of pseudomyrmecine diets consists of pollen and fungal spores, dispersed resources that these ants are specially adapted to utilize (Wheeler & Bailey, 1920) and which may be unavailable to other ants. Tending homoptera (live stems only) and nesting inside these stems, pseudomyrmecines are relatively immune to interference from competitive dominants, but also perhaps relegated to comparatively low quality resource environments that may

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preclude them from dominating canopy samples. Cephalotines (Myrmicinae) are another group of pollen-foraging arboreal ants (C. Baroni-Urbani, pers. comm.) that may feed on exudates in less than optimal circumstances (e.g. Adams, 1990b). With the exception of Cephalotes atratus Linnaeus ( J. Tobin, pers. comm.), which relies on pollen to a lesser degree than do other cephalotines (C. Baroni-Urbani, pers. comm.), they do not appear to be superabundant in the canopy. Finally, Table 1 also lists no specialized predators, for example, legionary ants. The Ponerinae, which include many specialized predators, are poorly represented here as well, as they are among obligate plant-ants (Davidson & McKey, 1993). The list includes only Paraponera clavata Fabricius, an atypical ponerine characterized by obligate arboreal foraging and strong reliance on plant exudates and even fruit (Young & Hermann, 1980). Among the ants listed in Table 1, P. clavata workers are distinctive for transporting large nectar droplets between their mandibles. In summary then, this survey of arboreal dominants and their traits supports Tobin’s (1991) claim that the extraordinary abundances of ants in canopy arthropod samples may be subsidized by plant resources, mostly in the form of plant and homopteran exudates. In addition to being outstanding homopteran tenders, many of the dominants are polydomous (have multiple nests per colony), and several are polygynous (Table 1, column 1). Polydomous species, those with multiple nests, are thought to achieve energetic savings by taking portions of the colony nearer to the resource (Ho¨lldobler & Lumsden, 1980). Moreover (and especially important for populous colonies), overlap in the foraging paths of individual workers may be reduced, since all are not foraging from a single central place. Polygyny, or the presence of multiple egglaying queens per colony, tends to be correlated with large colony sizes and with abundant resources that permit rapid growth (Ho¨lldobler & Wilson, 1977b). It may enable species to benefit from productive resource environments in ways unavailable to monogynous species. Although polydomy and polygyny often occur together, perhaps due to their mutual relationship to large colony size, polydomy can exist without polygyny, as in Oecophylla species and many Azteca species (Table 1). Workers can simply transport young brood from a single egg-laying queen to various secondary nests.

DIETS AND DOMINANCE

How might CHO-rich plant and homopteran exudates contribute to the disproportionate abundances of one or a few ant species in canopy samples from lowland tropical rainforests? I will argue that the numerical dominants of these samples benefit from key innovations for gathering and processing the large exudate volumes required to obtain significant amounts of nitrogen (Eisner, 1957; Davidson & Patrell-Kim, 1996) from liquids containing very low concentrations of nitrogenous compounds (Auclair, 1963; Baker et al., 1978; Harborne, 1982). In addition, carbohydrates in excess of those which can be paired with nitrogen for growth and reproduction (postulated here as the colony’s first priorities) may serve to fuel especially large and active worker populations that not only compete successfully against other ant species, but perhaps also reduce populations of other canopy arthropods to unusually low levels (Way, 1953; Leston, 1973; Majer 1976b).

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D. W. DAVIDSON

Key innovations for feeding As pointed out by others (Wilson, 1987; Tobin, 1994; Floren & Linsenmair, 1997), the subfamilies Formicinae and Dolichoderinae are particularly well represented among ant taxa that are abundant in rainforest canopies (see also Table 1). A possible explanation for this finding comes from the work of Eisner (1957), who showed that formicines and some dolichoderines are uniquely adapted to benefit from the ready availability of liquid foods. Eisner studied the functional morphology of the proventriculus, a digestive organ that regulates flow of food among three components (crop, proventriculus, midgut) of the ant digestive system. Situated just posteriorly to the crop, the proventricular bulb alternately pumps liquid food from the crop to the midgut, and then dams its posterior flow. In this manner, it controls the movement of food from the crop, a ‘social stomach’ whose contents are shared with nestmates, to the midgut, where food is digested by the individual worker. In workers of the subfamilies Myrmeciinae, Pseudomyrmecinae and Aneuretinae, Eisner found the proventriculus to be little modified from that of the ancestors of ants, aculeate Hymenoptera (Ho¨lldobler & Wilson, 1990a), in that sustained muscular contractions are required to dam the flow of liquids. In contrast, in many dolichoderines and all formicines studied, ‘passive damming’ by a sclerotized proventriculus occurs without continuous and energetically expensive muscular contractions, and the associated musculature is reduced. Such adaptations should lead to considerable energetic savings in ants that forage extensively for exudates and store them in great quantities for long time-periods. In groups with passive damming, much of the liquid diet remains in the crop to be shared with nestmates through oral trophalaxis (regurgitation), but small amounts regularly pass into the worker midgut for digestion and use. Eisner (1957) suggested that a constraint imposed by passive damming is that only liquids and the tiniest solid particles can pass through a pilose, cruciform slit in the cupola, a barrier between the crop and proventriculus. A corollary should be that workers of these taxa are fuelled disproportionately (relative to ants in other subfamilies) by liquid foods. One might posit also that any worker-synthesized exocrine products that are regularly used and replaced would likely be constituted from the mainly carbohydrate elements of the liquid diet (see below). Noting the ‘radically different’ structures of the proventriculus in formicines and dolichoderines, Eisner (1957) considered these specializations to have arisen independently in the two groups (Fig. 1). (In contrast, Baroni-Urbani, Bolton & Ward [1992] view the rigid, pumping proventriculi of Formicinae and Dolichoderinae as a character that could have evolved just once.) Within the Dolichoderinae, passive damming was found to be most ‘advanced’ (read ‘apomorphic’) in the tribe Tapinomini, including Azteca and Technomyrmex from Table 1, though the tribe may be an artificial grouping (Shattuck, 1992a). Although Dolichoderus is well represented in Table 1, the proventriculus of the single species examined (Hypoclinea pustulatus = Dolichoderus pustulatus Mayr, see Shattuck, 1992a) was structurally similar to the plesiomorphic form of more predatory ants. Nevertheless, the bulb’s plicae or pleats are sclerotized posteriorly, and the muscles which expand the bulb have been lost. Ingress of fluids from the crop is a passive process, occurring automatically with the relaxation of the bulb’s circular muscles. With the exception of passive uptake of fluids by the bulb, Eisner considered the proventriculus of D. pustulatus to function much like the plesiomorphic form. However, it seems equally plausible that structural

RESOURCE IMBALANCES IN TROPICAL ARBOREAL ANTS

161

Iridomyrmex Conomyrma Dorymyrmex Forelius

Technomyrmex

?

Cladomyrma Camponotus

Tapinoma Azteca Acropyga

Notoncus

Leptomyrmex Amblyopone Pogonomyrmex Liometopum

Dolichoderus Pseudomyrmex

Odontomachus

MYRMICINAE

Aneuretus

DORYLINAE

Phyracages

Myrmecia

FORMICINAE DOLICHODERINAE PONERINAE ANEURETINAE PSEUDOMYRMECINAE MYRMECIINAE MYRMECIOID COMPLEX

Eciton

CERAPACHYNAE

PONEROID COMPLEX

Figure 1. After Eisner (1957). Mapping of proventricular structures onto a (then current) phylogenetic hypothesis for relationships among the ants. See text for details.

modifications in this species may allow the bulb to act as a secondary storage organ, ancillary to the crop, and therefore to increase (though not greatly, T. Eisner, pers. comm.) the potential liquid food loads of foraging workers. Such a slight selective advantage at this early stage could have figured importantly in later evolutionary modifications of the dolichoderine proventriculus. Further studies might focus profitably on Dolichoderus species that are either obligate homopteran tenders (Maschwitz & Ha¨nel, 1985) or included among the tropical dominants, in order to determine if the proventriculus has been modified further in these species. What of the myrmicines in Table 1? Nothing is known of the proventriculus of Myrmicaria. Although the proventriculus of most myrmicines is much reduced, with active daming of fluids (Eisner, 1957), that of Crematogaster is ‘radically different’ in morphology and perhaps in action as well (DeMoss, 1973: 93–94). The portal between the crop and proventriculus is unusually narrow for a myrmicine and reduced to a slit. DeMoss considers it to resemble “the cupola portal of the formicines and dolichoderine proventriculus.” Crematogaster is also unusual among myrmicines for exhibiting oral trophallaxis (regurgitation of food among nestmates), and this observation by Wilson & Eisner (1957) suggests unusual dependence on liquid food. Finally, it is notable that ants of the myrmicine tribe Cephalotini have independently acquired a rigid proventricular cupola (Forel, 1878; Emery, 1888; DeMoss 1973), whose functional significance is only now being studied by C. Baroni-Urbani (pers. comm.). Cephalotes atratus both tends Homoptera (Leston, 1978) and can be among the secondary dominants of some canopy arthropod samples ( J. Tobin, pers. comm.). At least some other Cephalotines (e.g. Zacryptocerus, subgenus Harnedia, Adams, 1990b) parasitize the food-finding abilities of exudate-feeding ants, and may rely to some degree on liquid foods.

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To recapitulate, modifications of the proventriculus in formicines, some dolichoderines, and possibly other genera (e.g. Crematogaster and some cephalotines), might be regarded as key innovations, enabling these ants to benefit differentially from plant and homopteran exudates. In turn, these disproportionate benefits may translate in some way into the very high abundances recorded for these ants in rainforest canopy samples.

Lessons from plant ecology Models borrowed from plant ecology suggest several ways in which the differential CHO-enrichment of the diets of certain ant taxa may enhance the absolute and contested protein carrying capacities for these species. Surprisingly, despite the many differences that separate ants and plants, the two groups have much in common. Anderson (1991) recently summarized many similarities of ants and plants, and his list might easily be expanded. One potentially profitable area in which parallels have yet to be drawn concerns the defences of individual leaves (in plants) or workers (in ants). A virtual explosion of recent work on antiherbivore defences in plants has produced several well-accepted generalizations. These generalizations are unlikely to transfer to ants and other social insects in unaltered form, because the two groups differ in some important ways. Clearly, one very important distinction is that ants can regulate the expression of their defences behaviorally. Like inducible plant defenses (e.g. Karban & Myers, 1989), but forming a larger component of the defensive arsenal, a variety of ant behaviours ranging from flight responses, to the release of chemicals like formic acid, and even the deterence of phorid flies by hitch-hiking leaf-cutter minors (Feener & Moss, 1990), are deployed only when needed. Inducibility should make such defences relatively cost-effective as evolutionary options. A second difference is that ants have offensive as well as defensive weaponry. A single chemical or a shield of exoskeleton might have both offensive and defensive functions, even simultaneously. In the discussion which follows, I ignore the need for virtually all ants to defend against other (principally vertebrate) enemies, and define defence more narrowly than have others (e.g. Buschinger & Maschwitz, 1984) as mechanisms favouring ants in competition and aggressive interactions with other ants. (See Ho¨lldobler & Wilson, 1990a and Anderson, 1991, for reviews of the preeminence of ant-ant competition in ant ecology.) Furthermore, I consider only defences of individual workers and not those of the colony as a whole, so as to maintain the analogy with foliar defences of plants, and to avoid the complexities of how the effectiveness of colony-level defences might vary with colony size. Finally, I use Table 1 to focus attention on the suite of extraordinarily abundant tropical canopy ants, and only at the end, broaden the discussion to ants in other environments. The ‘resource balance model’ in plants and ants Theories of plant defensive investment generally assume that defence is costly, and that the types of defences used by plants should help to minimize costs. Using such an approach, Bryant et al. (1985) have shown that interspecific variation in plant defensive investment is well described by a resource balance model. Plants rely on

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several essential, i.e. not substitutable, resources (sensu Tilman, 1982). Some resources are usually present in excess, while one or a few resources limit growth. For example, plant growth requires both light (for carbon fixation) and nutrients, and having abundant light does not obviate the need for nutrients. Carbon (or light) can therefore be present in excess of amounts needed for plant growth, assumed to be the first priority. Whichever resource is present in excess can presumably be shunted toward defensive function, perhaps at minor cost. In environments where plants are mainly limited by nutrients (often nitrogen), rather than by light, the predominant plant species are predicted to have nitrogen-free (so-called ‘carbon-based’) defences such as terpenes, tannins, fibre and lignin. In contrast, where nitrogen is less limiting than light, nitrogen-based toxins are frequently used in plant defense (Mattson, 1980). Within any single species, levels of carbon-based or nitrogen-based defences may be higher in environments where light or nitrogen, respectively, are more abundant (but see Baldwin et al., 1994). Coupled with other models of plant defence, this model has much explanatory power in accounting for the amount, type and distribution of plant defences. Might the resource balance model also apply to ants and other social insects? The resources of ants, like those of plants, are not perfectly substitutable. Carbohydrates are necessary but not sufficient for brood production, which depends substantially on the availability of protein (reviewed in Ho¨lldobler & Wilson, 1990a, and Tobin, 1995). On their own, however, CHOs can fund a variety of defensive functions. If available in excess of amounts that can be paired with protein for colony growth or reproduction, CHOs might be directed toward greater rates of protein acquisition as mediated by elevated activity rates, territoriality and mainly carbon-based or nitrogen-free exocrine products. These topics are treated in sequence below. CHOs and ‘high tempo’ activity Oster & Wilson (1978) first called attention to the remarkable range of variability in worker activity levels represented among social insects. They referred to these levels as ‘tempos’ and distinguished between ‘high tempo’ and ‘low tempo’ ants. In an effort to understand the determinants of tempo, Oster & Wilson (1978) noted associations between high tempo activity and both large colony size and caste polymorphism. From these correlates, and an assumed greater riskiness of high tempo foraging, they inferred that species with small colony sizes should adopt less risky, low tempo foraging strategies, since resource scarcity is associated with slow colony growth and worker replacement rates. They also suggested that, if high tempo activity leads to an average increase in worker turnover rates, then workers might be less likely to have active ovaries. The lack of evolutionary opposition by workers might then enable the queen to produce polymorphic workers (but see Frumhoff & Ward, 1992). The resource balance model offers an alternative explanation for interspecific disparities in the tempos of ant activities. Excess CHOs can serve as a sort of ‘gasoline’ to fuel high worker activity rates, alertness, and vehement defense of anttended organisms (e.g. Fiedler & Maschwitz, 1989) at little or no cost to colony growth. A number of tropical dominants (Table 1), e.g. Camponotus femoratus, Oecophylla spp., Azteca spp., and at least some Dolichoderus spp. (bidens Linnaeus, bispinosus Olivier, and debilis Emery) exhibit rapid or even frenzied activity. Ho¨lldobler & Wilson (1990a) list Crematogaster as high tempo and Dolichoderus as low tempo. (Presumably

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they referred to Dolichoderus [as in Oster & Wilson, 1978] not including Hypoclinea, which has now been lumped under Dolichoderus, see Shattuck, 1992a.) However, a great deal of variation exists within each of these genera, as well as within Camponotus and even Azteca. For example, some Azteca living symbiotically with Triplaris are timid and slow-moving (Davidson, Snelling & Longino, 1989). Though there would be much agreement among myrmecologists as to the tempos of particular ant species, agreement would not be perfect, and evaluations will remain speculative until comparative measurements are actually made. Rapid foraging velocities might convey any of a number of benefits. They should both increase rates of resource discovery, since higher ‘dynamic densities’ (individuals/m2/min, Savolainen & Vepsa¨la¨inen, 1988) would be positively correlated with area searched per unit of time, and also speed recruitment to contested resources once these are discovered. Thus, Wilson (1962) has argued that the seemingly frenetic pace of worker activity in large colonies of some high tempo ants may permit these ants to follow and capture moving prey more efficiently than do more ‘precise’ recruitment strategies. This putative reliance of high tempo ants on moving prey may be most important in visually-orienting species with relatively large body sizes (Ho¨lldobler, 1979), for Oecophylla, and pers. obs. for Camponotus femoratus and some Dolichoderus species). Second, large colonies of high tempo ants may also succeed in uncovering hidden or cryptic prey by stirring them into motion. An example is provided by army ants, whose high pace of activity may be subsidized by energy from arthropod hemolymph, rather than by exudates. As in army ants, flushing of prey might effectively increase the carrying capacity for ants, as well as deplete arthropod populations to lower levels than in adjacent habitats lacking dominant ants (Way, 1953; Leston, 1973, Majer, 1976b). A rich supply of CHO energy sources may also be crucial to the abilities of some of these ants to patrol and forage from the treetops all the way to the ground below (e.g. Room, 1975 for Oecophylla, Davidson, 1988, for ant-garden ants). Oster & Wilson (1978) predicted that homopteran-tending ants would exhibit low tempo foraging activity, since their resources are spatially predictable, and because perpetual discovery of new resources (maximized by high tempo activity) is unnecessary. The resource balance hypothesis makes exactly the opposite prediction and appears to be more compatible with observed variation in ant tempos. CHOs and territoriality Excess carbohydrate might also be used for territorial defence. By Vepsa¨la¨inen & Pisarski’s (1982) three-tiered framework for classifying dominance hierarchies in ants, species listed in Table 1 (columns 1 and 4) tend often to defend ‘level III’ territories consisting not just of nest sites alone (level I territoriality), or just nests and spatiotemporal resource patches (level II), but three-dimensional absolute territories that are patrolled regularly. As is common among ants (Ho¨lldobler & Wilson, 1990a), territories are defended interspecifically as well as intraspecifically, but typically only against a particular subset of interspecific competitors (e.g. Ho¨lldobler, 1979, for Oecophylla longinoda Latreille). Although level III territoriality is relatively rare among ant species as a whole, it definitely or probably occurs in 11 of 12 species for which data are available in Table 1. Since traits linking the species in Table 1 are often not common among their congeners (see below), most of these data points might turn out to be statistically independent. However, the two Oecophylla species likely share territorial traits through common ancestry.

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The quality of evidence for level III territoriality is variable. Evidence is most convincing, indeed incontrovertible, for weaver ants, Oecophylla longinoda in Africa, and O. smaragdina Fabricius in Australasia (Ho¨lldobler & Wilson, 1977a, c; 1978; Ho¨lldobler, 1979, 1983). Workers chase and attack intruding ants, capture and kill potential competitors, use recruitment pheromones and ‘vehement’ jerking displays to attract help from nestmates, maintain outposts of older ants to deter invaders at the territory edge, scent mark their home ranges with colony-specific pheromones from rectal bladders, and quickly explore and mark any open space or new objects placed within existing territories. Intraspecific territoriality is so strong that ‘no-ants lands’ often separate individual territories from one another (Ho¨lldobler, 1979, 1983). Interspecific territorial defence is selective, sometimes reciprocal, and a good predictor of a lack of interspecific spatial overlap (Greenslade, 1971; Majer, 1976 a; Ho¨lldobler, 1979). Camponotus femoratus, an ant-garden ant, may be the ecological equivalent of Oecophylla in the Neotropics (author’s obs.). Colony-level recruitment and defense systems have not been studied carefully, but workers parallel those of Oecophylla in quickly occupying vacant space or new objects, using a violent, jerking display to alert and summon nestmates to possible dangers, and exhibiting aggression against conspecifics from different colonies (Davidson, 1988). Bait censuses show that either the abundances, or the activities of other arboreal ants are lower in forests occupied by ‘archipelagos’ of ant-garden nests than in nearby areas lacking ant gardens (Davidson, 1988). This observation suggests interspecific territorial defence but does not indicate which of the parabiotic (cohabiting) ant-garden ants (C. femoratus, Crematogaster limata var. parabiotica Smith, or both) may be responsible for the pattern. In contrast, available evidence suggests that Paraponera clavata lacks level III territoriality (Table 1). Although these ants defend the nest vicinity and relatively long-lived food finds against conspecifics (Breed et al., 1991, see also Baird, 1986), there is no evidence that they patrol either intraspecific or interspecific absolute territories. Indeed, the extremely large workers of this species can be pushed around by even tiny Crematogaster ants (author’s obs.). Distinctive in many ways from other tropical dominants, this species may be a relatively new arrival in the arboreal zone (see below). Nevertheless, by comparison with Dinoponera gigantea Perty (= D. grandis, see Bolton, 1995), another large-bodied ponerine, P. clavata is much more aggressive in nest defense (Hermann et al., 1984). Although both P. clavata and D. gigantea nest terrestrially, workers of the former species forage mainly arboreally, whereas those of the latter species forage terrestrially (Hermann et al., 1984) and almost certainly have diets less rich in CHOs. Evidence for absolute territories remains sketchy throughout the remainder of the table and is weakest when documented only in congeners from different geographic provinces (entries inside square brackets in Table 1). Most problematic is that even these very abundant tropical ants can rarely be assigned specific names, and consequently, it is difficult to associate particular dominants with ecological data from other studies. For example, two known level III species of Myrmicaria occur in the Asian tropics, where Stork’s (1991) samples were collected (A. Weissflog & U. Maschwitz, pers. comm.), but they cannot be linked directly to the species dominating the sample. Similarly, ants in the taxonomically difficult genus Azteca have not been identified to species in any of the studies listing Azteca as the most common ants in a sample. Of the three Azteca species studied by Adams (1990a, 1994), only Azteca trigona might be present in regions where the canopy arthropod

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surveys took place ( J. Longino, unpublished notes on Azteca species). For this species, intraspecific and/or interspecific territorial behaviours include clustering of unusually excitable workers (especially major workers) at territorial boundaries, alarm posturing, brief periodic probing of neighbouring territories, mutual assessment by neighbours, pheromonal and tactile recruitment of nestmates to disputed areas, and capture and killing of workers from conspecific neighbouring colonies (Adams, 1990a, 1994). In mangrove habitats, Adams (1994) also confirmed the maintenance of mutually exclusive territories by A. trigona, two other Azteca species, and Crematogaster brevispinosa. Because both C. brevispinosa ( J. Longino, pers. comm.) and Dolichoderus thoracicus (see Maschwitz et al., 1991) are members of unresolved species complexes, descriptions of level III territoriality under these names (Adams, 1994, and Way & Khoo, 1989, respectively) do not necessarily apply to species in respective canopy samples (Adis et al., 1984; Floren & Linsenmair, 1997). Where species can be named, experimental or statistical evidence is sometimes available (e.g. Greenslade, 1971; Room, 1975; Majer, 1976a, b, c; Jackson, 1984) and other times absent (e.g. Leston, 1978). It is encouraging, however, that untested assertions about mutually exclusive territories (Leston, 1973) have often proven to be correct in subsequent tests (e.g. by Majer, 1976a, c; Jackson, 1984). Clearly, the data set must be much more complete before we can test rigorously for the postulated relationship between the abundance of exudate-feeding ants in canopy samples and the defence of absolute territories. By explicitly calling attention to the hypothesis, I hope to promote more detailed reporting of data in future canopy studies. Finally, although mutually exclusive territories appear to be typical of a number of species in the tropical arboreal zone ( Jackson, 1984), they are atypical in terrestrial ant faunas of the tropics ( Jackson, 1984), and where they have been demonstrated for terrestrial species (Brown, 1959; Vanderplank, 1960), they exist, not on the ground, but only where the ants have colonized palms ( Jackson, 1984). Jackson (1984) considers several explanations for these patterns: (1) arboreal resources (Homoptera) are richer and more worthy of defence than are terrestrial resources; (2) the 3-dimensional forest volume may be easier to defend, because ant densities are generally lower on foliage, or because defence can be concentrated at key points, e.g., branch junctures; (3) the highly complex recruitment and alarm systems of Oecophylla longinoda (Ho¨lldobler & Wilson, 1978) may be the main determinant of the organization of ant mosaics (in Africa). To these (not mutually exclusive) explanations, I would add a fourth. Terrestrial species are less likely than are arboreal nesters to forage in the sunlit canopy, where high plant productivity translates into ready availability of plant and homopteran exudates. Therefore, they are less apt to have excess CHO to fuel the defense of absolute territories.

Diets and defences Although the inclusion of ants in Table 1 is based on their numerical dominance, defined here as dominance in numbers, biomass and/or frequencies in canopy arthropod samples, many of the listed species overlap with those recognized as ‘dominant ants’ in the well-studied ‘dominance mosaics’ of ants in plantations forests of Africa and Australasia (e.g. Leston, 1973, 1978; Room, 1971, 1975; Majer, 1976 a,b,c, 1990); Taylor, 1977, 1978; Jackson, 1984). This overlap includes at least the

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two Oecophylla species (Majer, 1990), Azteca, Dolichoderus and Crematogaster species (Leston, 1978), Technomyrmex albipes Smith (Room, 1975), and Crematogaster striatula Emery (Majer, 1976a). Within the ant mosaic, dominance is defined by the defence of mutually exclusive territories (Leston, 1973), equivalent to level III territories in more recent parlance, but competitive dominance is also implied. If excess dietary CHO preadapts ants to evolve high tempo foraging and level III territoriality, these latter traits may promote competitive dominance and (therefore) its correlate, numerical dominance. However, competitive dominance clearly depends on other traits as well, and this section explores some potential effects of CHO:protein ratios on one such trait, chemical weaponry. The ants dominating canopy arthropod samples have diets strongly skewed toward consumption of CHO-rich exudates, and in those taxa with a modified proventriculus, workers may be supported mainly by a liquid (CHO) diet. Given these observations, the resource balance hypothesis would predict that workers of these species should be more likely than those of predatory species to use nitrogen-free (strictly carbonbased) compounds in alarm/recruitment or alarm/defence, two functions that might increase the success of canopy dominants in exploitative or interference competition with other ants. An indirect test of this hypothesis would be to map dietary specializations and exocrine products onto a phylogenetic template and then search for character correlations (see e.g. Maddison, 1990; Sillen-Tullberg, 1993). Fortuitously, particular types of exocrine compounds often appear to define whole ant genera or even subfamilies (e.g. Ho¨lldobler & Wilson, 1990a). However, no phylogeny yet exists for the ant genera, and the phylogenies of subfamilies (e.g. Shattuck, 1992b; Baroni-Urbani et al., 1992; Fig. 2) may not provide a sufficient number of taxa to resolve this issue. Nevertheless, some interesting patterns do exist at the subfamilial and generic levels. Proteinaceous stings are plesiomorphic in the aculeate hymenoptera from which ants are descended (Buschinger & Maschwitz, 1984), and the most predatory ants (subfamilies Nothomyrmeciinae, Myrmeciinae, Pseudomyrmecinae, Ecitoninae, Dorylinae, Aneuretinae, Aenictinae, Cerapachyinae, and most species of the Ponerinae and Myrmicinae) have functional stings associated with a venom (or poison) gland, containing proteinaceous, neurotoxic and/or histolytic toxins (Ho¨lldobler & Wilson, 1990a). (At least one pseudomyrmecine, Tetraponera sp., is unique in having a modified spatulate sting, unsuitable for injection, but used to apply alkaloidal contact toxins to its enemies [Daloze et al., 1987; Merlin et al., 1988]). In contrast, among the ant taxa most dependent on CHO-rich plant resources, and most prominent as canopy dominants (Table 1), there is interesting variation in the fate and function of the poison gland (reviewed by Buschinger & Maschwitz, 1984; Ho¨lldobler & Wilson, 1990a). In formicines, an hypertrophied poison gland produces (nitrogen-free) formic acid, which functions in alarm/defense and can be present in both prodigious amounts (to 2 mg/worker) and concentrations (to at least 60%) (Blum, 1981). Peptides and amino acids are exceptional (Attygalle & Morgan, 1984), and although formic acid may be made from nitrogen-containing serine (Hefetz & Blum, 1978), nitrogen is probably not lost in the process. In dolichoderines, workers have a reduced poison gland, and have transferred alarm/defense functions (in part) to the hypertrophied pygidial gland (also called the anal gland, or Janet’s gland). A diversity of nitrogen-free products have been identified from the dolichoderine pygidial gland and include acyclic ketones, cyclopentanoid monoterpenes, disub-

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Sphecomyrminae

Bradynobaenidae

Aneuretinae

Aneuretinae

Dolichoderinae

–E,P,NF

Formicinae

–E,P,NF

Dolichoderinae

–E,P,NF

Formicinae

–E,P,NF

Nothomyrmeciinae Myrmeciinae

Myrmeciinae Myrmicinae

Myrmicinae Myrmicaria Crematogaster

Nothomyrmeciinae

–E,P,NF –E,P,NF

Pseudomyrmecinae Ponerinae Leptanillinae

Myrmicaria Crematogaster

–E,P,NF –E,P,NF

Pseudomyrmecinae Ponerinae Leptanillinae

Cerapachyinae

Cerapachyinae

Ecitoninae

Ecitoninae

Aenictinae

Aenictinae

Dorylinae

Dorylinae

Baroni Urbani, Bolton & Ward, 1992

Shattuck, 1992

Figure 2. Two contemporary phylogenetic hypotheses for relationships among the subfamilies of ants. Extinct ant subfamilies are omitted from the tree published by Baroni-Urbani et al. (1992). Notations to the right of ant taxa: E = exudate-feeders; P = proventriculus modified (or possibly modified in Crematogaster) for handling large volumes of liquids; ? = no information on proventriculus; NF = alarm/defense exocrine products are nitrogen-free (or mainly carbon-based in Myrmicaria).

stituted acetophenones, orcinol and iridoids (Cavill & Hinterberger, 1960; Wheeler et al., 1975; Blum et al., 1982). Among myrmicines, the sting may be functional or non-functional, and the poison gland produces proteinaceous venoms, sometimes in low quantities and augmented by small, nitrogen-based compounds (alkaloids and amino acids, see, e.g. Tumlinson et al., 1971; Ritter et al., 1973; Jones, 1987). The two myrmicine genera in Table 1 are striking exceptions to this generalization. Crematogaster are distinctive for reduction of the venom gland and hypertrophy of the Dufour’s gland, which produces highly lipophilic contact toxins, smeared onto opponents with a modified, spatulate sting (Buren, 1958; Maschwitz, 1975; Daloze et al., 1987; Pasteels, Daloze & Boeve, 1989). Like the Dufour’s gland products of other ants, those of Crematogaster are nitrogenfree; thus, like formicines and dolichoderines, Crematogaster has substituted a N-free weapon for a proteinaceous venom. In Crematogaster scutellaris Olivier, enzymes from the poison gland are mixed with long-chain primary acetates from the Dufour’s gland and accumulate on the sting, where highly electrophilic aldehydes begin to form (Pasteels et al., 1989). Simultaneously, a nitrogen-free alarm pheromone (acetic acid) is also produced. Myrmicaria species are also unique for their subfamily, in that terpenes are contained in the hypertrophied poison reservoir. Contents consist of equal components of a volatile fraction (97% (+)-limonene, with additional monoterpene hydrocarbons and hexanoic nitrile as minor components) and a non-volatile fraction with one

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major constituent (>80%, a probable alkaloid, >3.1% N) (Kaib & Ditterbrand, 1990; see also Brand et al., 1974). When applied to the substrate or to antagonists at sites of combat or contests over protein resources, this mixture of compounds serves alarm/recruitment and alarm/defence functions. High and low volatility fractions (in a 1:2 ratio) act synergistically, with the latter serving as a fixative to extend the effective period of the limonene signal, and the former acting as the solvent to enhance the spread of the low volatility fraction on the cuticles of enemies or prey (Kaib & Dittebrand, 1990). This description is based on Myrmicaria natalensis eumenoides (Bolton, 1995, for nomenclature) in East Africa, and some geographic variation is known to occur within the species. The generality of these results cannot be confirmed for the species in Table 1 until the ants in Stork’s (1991) Bornean samples have been identified and studied. Although M. n. eumenoides nests terrestrially and feeds preferentially on arthropod prey (mainly social insects like ants and termites, Kaib & Dittebrand, 1990), it does tend Homoptera in low vegetation (Dejean et al., 1994). In contrast, at least some Myrmicaria (M. arachnoides var. lutea [cf. Bolton, 1995]) of Asian rain forests are ecologically unusual for myrmicines, and similar to several of the more intensively studied dominants, such as Camponotus femoratus, and Oecophylla species. According to A. Weissflog and U. Maschwitz (pers. comm.), these arboreal ants are polygynous and polydomous, inhabit carton nests, and tend homoptera intensively outside their nests. It would be interesting to study components of the poison reservoir in this and ecologically similar Myrmicaria species. The resource balance model from plant biology may indeed explain some of the variation in defensive compounds of ants, though it is wise to remain cautious since exocrine products have been characterized in just a small minority of ant taxa. From the plesiomorphic condition of functional stings and proteinaceous venoms, it appears that ants with N-free or mainly C-based (Myrmicaria) alarm/defense products have evolved independently at least four times, always in association with diets high in exudates (CHOs) (Fig. 2). First, although the Formicinae and Dolichoderinae may be sister groups (Shattuck 1992b, but see Baroni-Urbani et al., 1992), their dependence on N-free defensive products is almost certainly independently evolved, since both the compounds themselves and their source glands differ between the two sub-families. Second, venomous stings are typical within both the 4-taxon clade containing the Myrmicinae and the monotypic Aneuretinae, in the sister group of that clade. Consequently, it seems likely that evolutionary losses of functional stings and gains of mainly carbon-based alarm/defence compounds occurred independently in those two clades. Third, within the Myrmicinae, there is no evidence that Crematogaster and Myrmicaria and particularly closely related, and intergeneric differences in both the chemistry of alarm/defence products and their source glands again suggest that mainly carbon-based alarm/defence weaponry has evolved independently in these two chemically unique taxa. As many tropical ecologists can attest, Paraponera clavata is the exception among ants in Table 1. Despite its significant dependence on plant exudates (Young & Hermann, 1980), it has not evolved away from a proteinaceous sting. This species could be a comparatively recent arrival in the arboreal zone (see below), and over the long term (!), it might be predicted to gradually evolve away from proteinaceous stings and toward nitrogen-free defences. Also noteworthy, perhaps, is that unlike more strictly predatory ponerines, including Dinoponera gigantea, P. clavata apparently produces no nitrogen-based compounds in its mandibular glands (Hermann et al., 1984).

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Although the canopy dominants in Table 1 are the focus of this study, carbonbased alarm/defense products may also be characteristic of other arboreal ants with high dietary ratios of CHO: protein. Thus, Pheidole biconstricta Mayr, a species thriving on homopteran honeydew and extrafloral nectar in Colombian coffee plantations (Kugler, 1979), uses products of a greatly enlarged pygidial gland for alarm/defensive functions. Although these products have yet to be characterized, pygidial gland products in another subfamily, the Dolichoderinae, are N-free (see above). Second, in two Crematogaster species, C. inflata Smith and Crematogaster difformis Smith (C. deformis is a synonym, see Bolton 1995), hypertrophied metapleural glands release alarmrepellent or repellent products (Maschwitz, 1974; Buschinger & Maschwitz, 1984), confirmed as hydrocarbons in the latter species (Attygalle et al., 1989). The diet of at least C. difformis is CHO-rich (Attygalle et al., 1989; Fiala & Maschwitz, 1991). Alternative explanations should also be considered for the relationship between CHO-rich diets and nitrogen-free defensive compounds. First, since stings are used in predation as well as in defence, functional stings and nitrogen-based venoms may simply have been lost when they became obsolete due to reduced dependency on sturdy live prey. As ant taxa came to rely more strongly on homopteran exudates, they may also have turned increasingly to delicate homopteran nymphs as a protein source (Way, 1954; Pontin, 1978). Based on available data, it is difficult to confirm or refute the hypothesis that the taxa listed in Table 1 rely little on sturdy live prey. The results of Davidson & Patrell-Kim (1996) suggest reduced dependency on predation and scavenging in several exudate-feeding genera, and active hunting is apparently absent in one highly specialized homopteran tending dolichoderine (Maschwitz & Ha¨nel, 1985). However, Maschwitz & Kloft (1971) have argued that chemical sprays can be more useful than stings in subduing arthropod prey, and at least some of the canopy dominants with CHO-rich diets, non-functional stings and nitrogen-free defensive compounds, are formidable predators. The predatory behaviors of Oecophylla species are especially well documented (Ho¨lldobler, 1979, 1983; Fiedler & Maschwitz, 1989). Second, it is also possible that increasing use of plant and homopteran exudates led to escalating contests among ants over these rich, localized and dependable energy sources. If carbon-based chemical sprays or contact toxins were more efficient than stings against other social insects (Maschwitz & Kloft, 1971; Davidson et al., 1988), selection for such weaponry might have been stronger in these ants than in predatory species foraging for dispersed prey. However, predatory ants with functional stings probably also compete (both within and among species) for large-bodied prey to which multiple colonies have recruited. Clearly, these issues cannot be resolved here, and distinguishing among the various alternative explanations for the cooccurrence of CHO-rich diets and mainly carbon-based or nitrogen-free alarm/ defense chemistry remains a challenge for the future. Finally, both alarm pheromones from the mandibular and Dufour’s glands, and recruitment or trail pheromones, tend to be nitrogen-free (e.g. Attygalle & Morgan, 1984; Ho¨lldobler & Wilson, 1990a), perhaps because highly volatile or moderately volatile hydrocarbons, respectively, perform these functions best (Ho¨lldobler & Wilson, 1990a). Nevertheless, one might also predict that more profligate use of these nitrogen-free compounds could correlate with high dietary ratios of CHO to protein. The multiple recruitment systems of Oecophylla, and the release of mandibular alarm pheromones by the violent, jerking motions of Oecophylla species and Camponotus femoratus are possible examples (Ho¨lldobler & Wilson, 1978; Davidson, 1988).

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Intraspecific variation in defences Over evolutionary time, diversion of excess CHOs to traits that enhance protein acquisition might be expected to consume most of the excess and leave exudatefeeding ants with relatively balanced diets. However, as in plants, such evolutionary trajectories do not necessarily preclude the occurrence of substantial environmentally correlated variation in the expression of those traits (see e.g. Folgarait & Davidson, 1994, 1995). In considering the metabolism of individual plants, plant biologists distinguish between primary metabolism (growth of new tissue) and secondary metabolism (differentiation, or the production of specialized tissues, organs or compounds not enhancing resource capture [Herms & Mattson, 1992]). Growth predominates when resources are abundant, but differentiation occurs when a dearth of particular resources limits growth more than energy capture (photosynthesis). Applied to ants, this theory would posit that CHOs may be shunted first to growth or primary metabolism, and only secondarily to defense, territoriality and high tempo activity. If so, then environmentally based resource imbalances may influence CHO investment in secondary metabolic pathways committed exclusively to the products or functions of those pathways (but see Baldwin et al., 1994 for plants). What is the evidence for environmentally correlated variation in the tempos, territoriality and defences of ants? While I am familiar with no data to address this question, a possible example involves the very aggressive Camponotus femoratus, a resident of ant gardens. During my studies of these ants, I noted repeatedly that workers in colonies from dark, dense vine tangles (created in part by hemiepiphytes in the ant gardens themselves) were much less aggressive than were those in exposed environments, where abundant light contributed to luxuriant growth of both antgarden epiphytes and host-plants from which the ants derived extrafloral nectar or homopteran exudates. It is possible that these ants become more active and aggressive when the dietary ratio of CHO to protein is high. The amount of formic acid in the poison gland could provide a proximate cue that determines individual worker behaviors. Environmentally correlated variation in resource imbalances should suggest experimentally tractable tests of the putative importance of such imbalances to ants and other social insects. Although studies of intraspecific variation in foraging tempos, territoriality, and/or the production of alarm/defence exocrine compounds would not constitute tests of the evolutionary hypotheses advanced here, evolutionary hypotheses are notoriously difficult to test, and intraspecific comparisons might at least provide preliminary evidence strengthening or weakening the plausibility of the evolutionary scenarios. Such comparisons would be especially valuable if designed to discriminate between predictions of a resource balance model and those of alternatives such as optimal defence models (Baldwin et al., 1994).

OTHER CONSIDERATIONS

Nests near the fuel pump Many of the ants listed in Table 1 have congeners with smaller colony sizes and different lifestyles. Why have some species become tropical dominants and others not? Particular evolutionary innovations of diverse types (physiological, behavioral,

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T 2. Nesting habits of ants dominating canopy samples in numbers, biomass and/or frequency in samples Species

A/Ta

 Camponotus femoratus

A

Camponotus spp.

?

Oecophylla spp.

A

Plagiolepis spp.

?

 Azteca spp. Dolichoderus spp.

A A

Technomyrmex albipes Technomyrmex spp.  Crematogaster limata var. parabiotica Crematogaster striatula Crematogaster brevispinosa Crematogaster spp. Myrmicaria spp.

 Paraponera clavata

Nest type

Referencea

Decaying organics, cemented by Davidson, 1988 carton (see text) Live and dead stems, decaying organic (Wheeler, 1910, Maschwitz, Dumpert material carton, silk & Schmidt, 1985; Dumpert et al., 1989) Live leaves bound with larval silk Ho¨lldobler & Wilson, 1977c, Ho¨lldobler, 1983 ? Carton, live or dead twigs Carton, plant fiber, silk, live leaves cemented by carton Dead wood; among dead leaves ?

(Wheeler, 1910) (Wheeler, 1910, Maschwitz et al., 1991)

A

Carton with organic material (see text)

Davidson, 1988

A A ? A

Hollow dead wood and crevices Live and dead stems and tree hollows Live and dead stems and carton Carton beneath live leaves

Major, 1976b, Dejean et al., 1994 E. Adams PC, J. Longino PC (Wheeler, 1910) Maschwitz et al., 1988; (A. Weissflug & U. Maschwitz, PC, for M. arachnoides, var. lutea)

T/A

Soil at tree base, in debris within tree

Breed & Harrison, 1989

A/T ?

Room, 1971

a References in parentheses refer to nesting habits in the genus as a whole and may not accurately reflect those of species dominating the canopy sample. b A = arboreal; T = terrestrial. Paraponera clavata nests mainly terrestrially but has arboreal outposts.

biochemical, life historical, and social) may characterize only a subset of species. I will not to summarize here the myriad factors that might favour or preclude numerical dominance. Rather, I will mention a single factor that many of the dominants appear to share: the acquisition of specialized nesting habits (Table 2). As ants evolve increasing dependency on CHOs from plant and homopteran exudates, and perhaps also on Homoptera as prey, nesting near the food resource should become increasingly advantageous. Not surprisingly then, most of the ants in Table 1 have evolved more or less elaborate means of nesting in the canopy (Table 2, see also Anderson & Reichel, 1994). Some have found ways of entering and nesting in live plant stems. Others construct nests of carton, or partly decayed vegetative material, cemented together by rectal fluid (Mishra, 1991). Carton may be employed in small amounts (e.g. to cement live leaves into nest chambers) or in quantity (to form the whole of the nest, as well as shelters over homoptera and frequently used trails). When supplemented with organic material, as in some ant gardens, the nests can form a rich medium for growth of epiphytic resource plants (e.g. Davidson, 1988), whose roots lend structural support to the nest (Yu, 1994). The most elaborate ant gardens are built cooperatively by two cohabiting ant species, and result from an especially fortuitous set of circumstances. Crematogaster cf. limata, var. parabiotica supplies the carton, Camponotus femoratus, the organic material,

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and both species retrieve vertebrate feces that may be incorporated into nest walls (Davidson, 1988). Seeds of the epiphytes are carried to the nest by the larger C. femoratus workers. Although some other ant species also retrieve these seeds, their nest substrates are inadequate to support a high biomass of epiphytes (Davidson, 1988). Finally, weaver ants (Oecophylla), which use larval silk to bind living leaves into nest chambers, have one of the most specialized nest constructions known (Ho¨lldobler & Wilson, 1990a). Ants that make their own nests or live in live plant cavities can place their nests on or near preferred resource plants (e.g. Way, 1954, for Oecophylla, Davidson, 1988, for ant-garden ants), and such preferences have probably been important in the evolution of some highly specialized ant-plant relationships (Yu & Davidson, in press). Even in Paraponera clavata, which nests mainly terrestrially but is obligately arboreal in its foraging, queens may found colonies selectively at the bases of particular trees (Ho¨lldobler & Wilson, 1990b; Thurber et al., 1993) that offer either extrafloral nectar (Bennett & Breed, 1985) or especially tall or protected routes to the canopy (Belk, Black & Jorgensen, 1989). As myrmecologists become better botanists, we are sure to notice such associations more frequently. Some of the dominants appear to have moved or be moving recently into the arboreal zone. Such species include Technomyrmex albipes and Paraponera clavata, which nest both terrestrially and arboreally (Table 2, Room, 1971; Breed & Harrison, 1989). The genus Myrmicaria contains both terrestrially and arboreally nesting species ( Jackson, 1984; A. Weissflog & U. Maschwitz, pers. comm.), and terrestrial species can forage on vegetation for extrafloral nectar and honeydew (Dejean et al., 1994; Suzzoni, Kenne & Dejean, 1994, for dominant supercolonies of Myrmicaria opaciventris Emery). In each of these three genera, it appears likely that ants evolved their dependency on plant and homopteran exudates prior to evolving means of nesting in the arboreal zone. Together, high CHO:protein ratios and specialized nesting habits are likely to prove necessary but not sufficient conditions for numerical dominance in rainforest canopies and other habitats. Within genera like Camponotus and Dolichoderus, the vast majority of species are not dominant, and comparisons of these congeneric species with the dominants will be needed if we are ever to identify all of the factors involved in dominance. Resource balance in relationships of ants with plants and butterflies The considerable functional importance of ants in rainforest ecosystems probably traces to their unique combination of large aggregate biomass and individually small sizes and energy requirements (see e.g. Jeanne & Davidson, 1984). The latter permit ants to forage profitably even for minute and dispersed resources that are unavailable to vertebrates. By producing relatively inexpensive food rewards, many plant and animal species have evolved to take advantage of fine-grained foraging by ants, and to manipulate ant activity and behaviour to their own ends. Tropical plants in this category include myrmecophiles (Schupp & Feener, 1991), myrmecophytes (Davidson & McKey, 1993) and myrmecochores (e.g. Davidson & Epstein, 1989). A variety of insects, especially beetles and butterflies, also have evolved extreme dependency on the ants with which they reside, and they trick the ants in various complicated ways (Ho¨lldobler & Wilson, 1990a).

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To manipulate ants to their advantage, organisms may vary the amount of reward, its production rate, its placement and its quality. One aspect of reward quality is the CHO:protein (or amino acid) ratio, and by varying this ratio, organisms might exploit the need for ants to maintain balanced diets. Although this avenue of research is poorly explored, some observations hint that this might be fertile ground for investigation. For example, Carroll & Janzen (1973) noted long ago that most of the food rewards produced by ant-plants consist mainly of CHOs and lipids. They hypothesized that by excluding proteins and amino acids from such rewards, plants might keep ants ‘protein-starved’ and eager to pursue herbivorous insects. Janzen’s (1966) acacias (Acacia, Fabaceae) are exceptional. Perhaps because of their favourable nitrogen balance, these nitrogen-fixing plants produce protein-rich Beltian bodies to supplement extrafloral nectar and provide a relatively well-balanced diet for their pseudomyrmecine ants. In contrast, the obligate associates of Cecropia and Macaranga tend Homoptera, and could theoretically manage and harvest homopteran populations so as to balance their diets. In this light, it is interesting to note that populations of scale insects or mealybugs (Coccoidea or Pseudococcoidea) inside the stems of many true myrmecophytes are often reduced to just a single large individual at each leaf juncture (see Davidson & McKey, 1993), possibly indicative of high rates of harvesting of immature insects. Early studies by Way (1954) provide other evidence that the need for a balanced diet may influence treatment of Homoptera. Way showed experimentally that Oecophylla longinoda consumed more of its tended scale insects when given artificial sources of sugar-water (Way 1954). In the context of Way’s findings, Davidson & McKey (1993) proposed that by producing CHO-rich food rewards, incipient myrmecophilic plants could have benefited from a reduction in populations of anttended Homoptera, as the ants harvested these insects to maintain a balanced diet. (This hypothesis built on Beccera & Venable’s [1989] theory that many contemporary myrmecophilic plants could have evolved under selection favouring the production of food rewards to lure ants away from damaging Homoptera; many Homoptera both deplete plant resources and transmit viral diseases.) Such theories are ripe for testing, and experiments like Way’s would be interesting to perform in other settings. For example, it would be interesting to know whether variation in the composition of ant-attractive food rewards of myrmecophilic and myrmecophytic plants is correlated predictably with behavioral and other traits of associated ants. Experiments similar to Way’s (1954) might also add perspective to analyses of ant manipulation by larvae of the monophyletic and highly diverse lycaenoid and other butterflies (Lepidoptera: Riodinidae and Lycaenidae, as well as Tortricidae, e.g. Pierce et al., 1991; Maschwitz, Dumpert & Tuck, 1986). How, for example, can ants be induced to forego attacking larvae that often compete directly for extrafloral nectar (Fiedler & Maschwitz, 1989; DeVries, 1991a), and to expend considerable energy racing in circles about these larvae (Fiedler & Maschwitz, 1987)? Ants associated with lycaenids and riodinids consist mainly of species feeding on energyrich exudates of plants, Homoptera, and the larvae themselves (Fiedler & Maschwitz, 1987; DeVries, 1991b). Although some lycaenoids may keep the ants alert and attentive by imitating alarm pheromones of their attending ants (Fiedler & Maschwitz, 1987), a more general solution may be the production of amino acid subsidies (e.g. Pierce 1983, 1984; Fielder & Maschwitz 1989; DeVries & Baker, 1989) that attract protein-starved, high tempo ants. If so, such adaptation might help to explain why the most widespread and probably ancestral hosts of Lycaeninae are members of

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the order Fabales (Fiedler, 1995, see also Pierce, 1984), a group both specialized to grow at high tissue nitrogen levels (reviewed recently by McKey, 1994) and containing many N-fixers. It may also help to account for why predatory ants (with lower dietary CHO:protein) may kill and eat lycaenoid larvae, rather than tending them. It would be interesting to know whether, within and across ant species, ant behaviour toward lycaenoids is generally predictable from dietary ratios of CHO:protein (see, e.g. Pierce et al., 1991), and whether average interspecific differences in CHO: protein ratios of ant rewards lead to different kinds of adaptations on the part of associated lycaenoids.

Generalizing the resource balance model Observations of high tempo foraging, level III territoriality, and nitrogen-free chemical defences in tropical exudate-feeding canopy ants are consistent with predictions of a resource balance model borrowed from plant ecology, and applications of this model are likely more extensive than those reviewed here. First, ants have CHO and protein costs other than those which I have explored, and one might also attempt to quantify, for example, the CHO costs of carton-building, or the protein costs of larval silk used in nest building. Second, the model should apply to ants from habitats other than rain forests. For example, numerical and competitive dominance appear to be correlated with high tempo foraging, level III territoriality, nitrogen-free defences, and spatially or temporally depauperate ant faunas in communities dominated by some ground-nesting Iridomyrmex in arid Australia (Greenslade, 1976), and by Lasius niger Linnaeus and certain Formica species on islands off the Baltic coast of Finland (Vepsa¨la¨inen and Pisarski, 1982). Third, specific features of these other habitats should affect the particular balance of resources upon which tempo, territoriality, etc., may depend. For example, in arid regions, availability of water, which often comes mixed with CHO, may be as essential as, or more essential than, CHO in permitting high tempo activity. In arid canopies of tropical forests with prolonged droughts, limited water and seasonally low plant productivity may preclude the occurrence of high tempo dominants and reduce the overall abundance of ants (Majer, 1990; Tobin, 1994). Finally, the model could theoretically apply to social insects other than ants, and even to nonsocial animals in which CHO- and protein-dependent processes are functionally independent.

ACKNOWLEDGEMENTS

The ideas presented here were developed with support from the National Science Foundation (Awards BSR-9003079 and DEB-9123668). I am very much indebited to A. Floren, K.E. Linsenmair, U. Maschwitz, J. Tobin, and A. Weissflog, who permitted me to include their unpublished data in summary form. Thanks are also due to E. Adams, C. Baroni-Urbani, B. Fiala, K. Fiedler, A. Floren, J. Tobin and A. Weissflog for answering my requests for key literature. Comments by two anonymous reviewers were very helpful.

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