foraging strategies of ants traniello

Ann. Rev. Entomol. 1989. 34:191-210Copyright © 1989 by Annual Reviews Inc. All rights reserved

FORAGING STRATEGIES OF ANTS

James F. A. Traniello

Department of Biology, Boston University, Boston, Massachusetts 02215

OVERVIEW: ANT FORAGING STRATEGY AS ANINDIVIDUAL AND SOCIAL PROCESS

Ant foraging is a collective process composed of the activities of individualsas well as behaviorally integrated groups. Therefore, a great challenge in thesocioecology of foraging is to explain how the behavior of such a potentiallylarge and complex system as an ant colony emerges as a function of theproperties of its individual components. The task of studying foraging in antsin simplified by the fact that foragers, owing to their sterility, may do littlemore than forage during their tenure as food harvesters. However, eusocialitypenetrates virtually every facet of foraging strategy and adds additionalcomplicating social dimensions to its analysis.

Individual and social processes of foraging can be categorized into com-ponents to facilitate the analysis of foraging at the level of the single worker,the colony, or the integration of both (Table 1). A generalized ethogram forager behavior can be described to illustrate these processes. A foragerleaves the nest entrance in either a random or a consistent direction. A travelphase ensues, during which the worker maintains a constant compass bearingand moves directly away from the nest. At some point during the travel phasethe forager shows a high frequency of turning, marking the beginning ofsearch. During search, food resources are encountered and selected basedupon a forager’s physical caste, age, and prior experience, the trip distance,thermal stress, resource quality, and the colony’s current nutritional status.Depending on the ant species and the size, density, or quality of the food, theforager may communicate information to ncstmatcs about its location andrecruit additional foragers.

Summing the above-described individual activities across all foragersyields the most basic aspect of cooperative foraging. Changing nutritionaldemands associated with the maturation of reproductives may shift a colony’s

1910066-4170/89/0101-0191 $02. O0

Annual Reviewswww.annualreviews.org/aronline

Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.

http://www.annualreviews.org/aronline

Taige

Highlight

Taige

Highlight

Taige

Highlight

Taige

Highlight

Taige

Highlight

192

Table 1ences

TRANIELLO

Individual and social c,omponents of ant foraging systems, with representative refer-

Individual Social

1. Trip direction, distance, and duration 1.(92, 112, 118, 119)

2. Search pattern and duration (91, 112, 2.118, 119)

3. Loading capacity and retrieval (3, 34, 3.40, 63, 73, 89)

4. Resource assessment and selection (6, 4.23, 55, 64, 70, 79, 86, 89, 92, 99,100, 116, 117, 119)

5. Induction of cooperative foraging (1, 5.19, 109)

Summation of individual efforts (41,119)Temporal and physical caste; colonydemographic distribution (12, 24, 33,59, 75, 78)Tempo (60, 75)

Communication and cooperative re-trieval (1, 34, 50, 53, 109, llO)

Resource assessment and colony regu-lation of foraging (96, 100, 101, 104-106) (see also first column, component

4)

foraging activity among different food types. Communication mediatescooperation among foragers during search and resource retrieval and serves asa control mechanism of colony-level foraging responses. As a result it pro-vides regulatory feedback during the daily and seasonal organization offoraging.

In this review I treat f~raging strategy as a system divisible into elementscomposed of individual and collective action, recognizing that the distinctionbetween the two may often be blurred because of the high degree of socialintegration of colony foraging activity. My goal is to provide a synthesis ofselected current literature to supplement available reviews (9-11, 14, 43, 57,75, 76, 98, 120).

FORAGING SYSTEM EVOLUTION: A COMPONENTANALYSIS APPROACH

q~he traits that are used to categorize ant foraging are highly variable in theirdistribution among the more primitive (e.g. ponerine) or advanced (e.g.formicine) subfamilies of ants. For example, "diffuse foraging" (75), which foragers leave the colony singly and retrieve food solitarily, occurs inthe Ponerinae and Myrmeciinae. The formicines Cataglyphis spp. andOcymyrmex spp. also collect randomly dispersed food largely through in-dividual effort (118, 119), but the ponerines Pachycondyla laevigata andLeptogenys spp. have chemically mediated cooperative foraging (54, 68).Ecological influences on foraging systems, therefore, seem to overridephylogenetic tendencies. Also, any one foraging mode must not be mistaken


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


Taige

Highlight

Taige

Highlight

Taige

Highlight

ANT FORAGING STRATEGIES 193

for a species-typical characteristic when in fact it may be a behaviorallyflexible component of total foraging strategy. The use of such a foragingcategorization to indicate the outcome of higher-level ecological processesmay thus yield conclusions that are not entirely valid. For example, the grosscategorization of ant species as being "individual," "recruit," and/or "group"foragers (4, 5) may be "too weak and artificial to be useful" (52) when used define foraging systems in studies of community organization. Given the widevariety of feeding habits and levels of organization and complexity, I suggestthat foraging systems be analyzed as a series of components that may eachhave individual and social influences and that have all evolved in response toresource distribution patterns, competition, and predation. The designation ofsystems or species as "individual foraging" should be dropped because thebehavior of a forager is probably never completely independent of the activi-ties of other foragers and the state of the colony as a whole. Therefore, theidea of individual foraging is erroneous or at least misleading, even in specieslacking recruitment communication. Some components of foraging behavior,such as search or retrieval, may largely be individual activities. Search andretrieval tactics will depend on the size of resources, their temporal and spatialdistribution patterns, and their resistance to retrieval, as well as on the loadingcapacities of foragers. Therefore, retrieval may be an individual or groupprocess when viewed as a component of foraging, but this one feature shouldnot be used to categorize the entire system. In summary, any singlecategorization of ant foraging systems is inadequate in that it does notconsider the components of foraging behavior and their ecological influences,which are necessary to fully understand the total expression of a colony’sforaging strategy.

Caste Evolution and Foraging Strategy

Because foragers are sterile they do not have conflicting demands on theirtime and energy budgets that involve trade-offs between searching for foodand searching for mates. As a result, they are often viewed as the products ofselection for traits that maximize energy return to the colony. Several socialtraits have consequences that affect a colony’s economy; among these aretemporal polyethism and senescence, caste polymorphism, and foraging tem-po (60, 75, 78). Selection at the colony level can not only affect the be-havioral repertories of foragers to enhance their food harvesting ability, butcan also shape patterns of age demography and mortality. In Pogonomyrmexowyheei, the life expectancy of a forager averages 14 days under naturalconditions; survivorship is similar in the laboratory under conditions ofstarvation (78). However, in Cataglyphis bicolor, foragers have a life ex-pectancy of 6.1 days in the field but live for months or longer in the laboratory(93). Colony fitness may be correlated with the mrrphology and size frequen-


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


Taige

Highlight

Taige

Highlight

194 TRANIELLO

cy distribution of foragers. Their structural, morphology per se may reflectfeeding habit. Although it is clear in the case of some specialist predators suchas Amblyopone, Odontomachus, and Strumigenys species that mandibularshape and head structure reflect feeding habits, the relationship betweenmorphology and foraging ecology is often unclear. Recent studies usingdigitization analysis to detect the ecological correlates of variation in headmorphology have shown that head shape, as differentiated from size, isrelated to diet (B. Cole, person, al communication). Other studies haveascribed a role to vertebrate predation as a selective agent of form (56).

Caste, Competition, and Community Organization

Among monomorphic species, body size may shift owing to interspecificcompetition and may facilitate coexistence. It is assumed that there is acorrelation between forager size and food-item size, so that morphologicaldivergence produces resource partitioning. Body size of C. bicolor foragers isconsiderably smaller in populations in Greece than in Tunisia, apparentlyowing to the sympatry of the smaller-bodied Cataglyphis albicans in the latterenvironment (119). In Greece, where C. albicans is absent, the body size ofC. bicolor foragers is intermediate in size between that of C. albicans and C.bicolor in Tunisia, which suggests that a morphological shift has occurredbecause of local competition. Several studies have indicated a correlationbetween body size and food-item size for desert seed-eating ant communitiesand communities of generalist ant species (16, 17, 21, 38, 75, 110, 118).However, given the limitations of the use of body size as an indicator of foodchoice and niche (46, 47, 122) and the fact that the food recruitment systemsof ants make them less constrained by their morphology than other animals(14, 20, 110), size-based partitioning of resources among sympatric speciesmay be the exception rather than the rule in ants (21).

The species diversity of granivorous ants of the southwest desert in NorthAmerica is related to productivity, and coexistence is based upon body sizedifferences or foraging strategies that are correlated with seed size selection orseed density distributions (21, 22). In the Australian arid zone, speciesdensity is similar to that of North American deserts, but there is less separa-tion by size among sympatric species (72). Also, differences in productivityamong sites do not appear to have a strong influence on associated harvesterant communities in Australia as in North America, seemingly because popula-tion density is not limited by food availability (7, 8). Vegetation structure,and perhaps productivity, appears to be related to community organization (2,7, 8, 25). Worker size/seed size correlates can be found among some species,but other factors such as seed morphology and biochemistry affect seed choiceas well (25). In the Negev Desert one of three sympatric Messor speciesshows a small but significant correlation between forager size and seed size


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


Taige

Highlight

Taige

Highlight


harvested (S. Rissing, personal communication). In North-Temperate openfield ants and other communities of ants with similar generalist feeding habits,prey size is correlated with body size but mechanisms of cooperative foragingand interference also seem to be important determinants of prey selection andcommunity-level interactions (1, 22, 29, 31, 49, 53, 65, 109, 110).

Caste Polymorphism and Foraging Ecology

Although it occurs in a small fraction of ant species, the role of castepolymorphism in foraging has received much attention. Has natural selectionadaptively shaped colony demography? Do the proportions of workers ofdifferent size castes match the characteristics of food resources, and if so,how closely (75)? Size matching, the pairing of forager size and food-itemsize, has been suggested for a number of species (21, 24, 75, 80), but thecorrelation explains little of the variance in food choice (83, 84). Competi-tion, diet expansion, and polymorphism might be linked in Pogonomyrmexspp. (75), but in the polymorphic Pogonomyrmex badius there is only a low,insignificant correlation between polymorphism and diet (J. F. A. Traniello S. N. Beshers, unpublished). Colonies of Veromessor pergandei show in-creased size variation of workers in areas of relaxed interspecific competition(24). However, less than 4% of the variance in the size of seeds collected V. pergandei is explained by Ibrager body size, and worker body size changesduring seasonal cycles, showing little correlation with seed size or the per-formance of any task (83, 84). In this species, worker size may changeaccording to levels of resource availability, usable foraging time, and alateproduction, rather than according to selection for size pairing (83).

Polymorphism in Eciton burchelli is thought to enhance foraging efficiencyby lowering prey retrieval costs. Submajors, which comprise 3% of thecolony, are disproportionately active in prey transportation, representing 26%of all prey carders (33). Leg length allometry may increase foraging velocity.Across physical castes, prey dry weight is significantly correlated with workerdry weight; submajors carry the largest prey loads, although loaded submajorsdo not transport prey more rapidly than other castes (33). The inverserelationship between ant body size and respiratory rate (3, 63) and computersimulations (80) support the notion of enhanced foraging efficiency in polymorphic series, but critical demonstrations are lacking.

FORAGER LOAD CAPACITY AND CASTE EFFICIENCY One of the most

striking features of ant biology that bears on foraging efficiency is the abilityof an individual forager to carry a resource load that is considerably heavierthan its own body weight. The loading ability of a forager, measured asburden (Mant q- Ml°ad/Mant, where M is mass (3, 82), is 1.5-7.5 in Attacephalotes (89), 1.2-1.5 in E. burchelli (34), on average 2.2 in Pogono-


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


196 TRANIELLO

myrmex occidentalis (32), and 1.1-1513 in Formica schaufussi (J. F. A.Traniello, unpublished.)Eciton burchelli submajors have disproportionatelylong legs and mandibles, and can easily straddle and transport prey. Whilethis mode of rapid prey transport appears efficient, the burden capacity of loneforagers is greater in species such as F. schaufussi that drag rather than lifttheir prey. In this latter case prey transport speed decreases sharply withincreasing load weight, most likely because of frictional resistance (J. F. A.Traniello, unpublished). In polymorphic species, large workers may carrylarger loads, but the cost of producing these workers and the energetic gainfrom their input to a colony’s nutritional economy are unclear. For example,in Eciton spp. increasing forager weight increases load capacity and possiblyefficiency (12, 34). However, a standard calculation of burden reveals loadratios are 1.2, 1.3, and 1.5, respectively, for 2.5-, 5-, and 10-mg workers;therefore, larger workers have only slightly greater load capacities. Transportcosts decrease with increasing body size in ants in general, and in Ecitonhamatum the gross and net costs of transport decrease with body mass andrunning speed (3). However, the cost for polymorphic foragers of transportingaverage-size burdens must be estimated before transport efficiency can befully evaluated.

RESOURCE DISTRIBUTION, POLYMORPHISM, AND COOPERATIVE RE-TRIEVAL A significant body size/prey size correlation does not necessarilyimply that competition has led to divergence in worker morphology. First,morphology permits a worker to collect not only prey matched to its bodysize, but also any smaller load as well. This conclusion is supported by thefact that for some species variance in prey size increases as body sizeincreases (110). Second, the range of prey sizes available or actually takenmay be extremely large in comparison to the range of worker body sizes insome sympatric ant species, so body size variation can at best adapt a colonyto collecting a limited range of available prey. Third, recruitment communica-tion, which is common in many species, provides a flexible mechanism forsimulating a larger-bodied forager by organizing a cooperative retrieval group(34, 53, 109). Given the unpredictable distribution patterns of the foodsources of many ant species, the flexibility of caste simulation throughcooperative retrieval appears to best adapt a colony to temporal, spatial, andsize variability; resource distribution patterns may vary on a relatively briefecological time scale, but worker size demography cannot be shifted withinthe same time frame.

Cooperative prey retrieval occurs in many species of ants, but its evolution,mechanics, and energetics are poorly understood. In Lasius neoniger, F.schaufussi, and E. burchelli, transport group size is correlated with preyweight, seemingly to maximize carriage efficiency (34, 109; J. F. A. Tra-


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.



niello, unpublished). In E. burchelli, groups are structured teams composedof major workers plus one submajor; this group composition seems tominimize rotational forces during prey movement (34). In other ants, howev-er, groups often seem to lack structure beyond a forager number/prey weightrelationship and to lack coordination. In F. schaufussi.only some of the ants ina recruited group are involved in load carriage; some workers ride atop theprey while others pull in opposing directions. The loading capacity of coop-erative retrieval groups ranges from 1.7 to 8.9, which is lower than theloading capacity of single workers. In this species, and in Novomessor spp.,cooperative retrieval may be organized to decrease interference competitionthrough resource defense rather than to move prey with greater energeticefficiency (J. F. A. Traniello, unpublished).

FORAGING THEORY AND DIET SELECTION

It has been argued that ants are ideally suited to test predictions of theories offeeding strategies because of their eusociality; natural selection has madeforagers efficient food harvesters that maximize a colony’s energy intake(75). Equally convincing is the argument that difficulties arise in the applica-tion of optimization models to ants because the forager population of a colonyis often large and sometimes polymorphic, and worker foraging activity isseverely constrained by temperature (80). Although there have been manydemonstrations of food selection in ants (6, 23, 30, 55, 64, 70, 79, 81, 86,89, 92, 99, 100, 116, 117, 119), tests of theory have shown varying degreesof correspondence between ant foraging behavior and the predictions ofmodels (23, 48, 94, 100). The seed-harvester ants Pogonomyrmex rugosusand Pogonomyrmex barbatus increased diet specialization with increasingdistance of seed patches from the nest, but showed partial preferences (23).Similar tests conducted with P. occidentalis and Pogonomyrmex californicusshowed no significant change or a nonsignificant trend in seed size choice as afunction of distance (48,100). However, distances at which seed patches wereoffered were variable for the different species (3-12 m vs 3-7 m), and for californicus the maximum distance was 85 cm from the nest. The basicpremise of these studies is that the net energy value of seeds of all sizesdecreases with increasing distance from the nest owing to the added cost oftravel and transport, so that energy maximization is achieved at the moredistant patches through the selection of large seeds. The assumption is thatenergetic costs of search or travel and transport are significant relative toenergy gain. However, foraging costs for P. occidentalis workers are lessthan 0.1% of the caloric content of an average collected seed (32). Thissuggests that feeding selectivity may not change substantially with increasing


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


198 TRANIELLO

travel costs and that time cost and net energetic gain rate may be importantcriteria in foraging strategy (32).

Ants are poikilothermic, and their foraging activity is therefore constrainedby temperature, water stress, and other physical factors that might affect theenergetic costs of foraging or the use of time. Several studies have demon-strated a significant effect of ambient temperature on metabolic rate asmeasured by oxygen consumption (26, 77). In F. schaufussi the elevated rateof oxygen consumption appears to be an important component of foragingcost that influences prey selection (114). The role of travel distance and itsimportance relative to temperature as a foraging cost has also been examinedin F. schaufussi. Prey of two different sizes were offered at distances of 1 and5 m from the nest at low and high temperatures. At both 1 and 5 m, increase intemperature produced a decrease in selectivity; increasing travel costs at eitherlow or high temperature, however, did not affect selectivity (R. V. Bowen J. F. A. Traniello, unpublished). The magnitudes of temperature-inducedcosts and travel costs seem therefore to be very different; temperature pro-duces the more important constraint, if in fact temperature represents aforaging cost rather than a thermal risk factor.

Laboratory studies of patch use by Solenopsis geminata have shown thatcolonies recruit more foragers to sucrose patches that are closer to the nest,larger, or of higher concentration than to more distant, lower-quality, orsmaller patches (100). Patterns of recruitment and patch use in S. geminatasupport models of energy maximization rather than time minimization. Sim-ilar support for the hypothesis of energy maximization is provided by P.rugosus and P. barbatus, which recruit more foragers to seed patches close tothe colony (100).

Leafcutting ants select tree species based on the presence or absence ofsecondary plant compounds, water content, and leaf density (6, 55, 86, 116,117). Colonies are more selective of species the more distant they are from thenest, although at these foraging loci they sometimes do not harvest the leavesof neighboring palatable species (86). Foraging by leafcutting ants follows theprediction of optimal diet theory, which states that colonies should showgreater diet diversity and lower resource constancy when average resourcequality is low; colonies indeed shift their leafcutting among a greater numberof tree species when the average palatibility of resource trees is low, andspecialize in richer-resource environments (86, 95). Also, 70% of observedcolonies cut relatively close to the nest, and foragers cut leaves from higher-quality tree species with increasing distance from the nest (86).

Risk as a factor influencing foraging decisions has been examined throughstudies of both simulated and natural predation (37, 66, 121) and competition(49, 113), which result in a decrease or cessation of foraging or a change foraging direction. The influence of competitors on the spatial patterning of


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.



foragers and resource use has been described in Pogonomyrmex spp. (49) andin L. neoniger (113). In these species confrontation between foragers fromadjacent colonies leads to altered trail system directionality and search pat-tern, respectively, without a reduction in overall foraging activity. In Lasiuspallitarsus, resource use (patch choice) is affected by the presence of Formicasubnuda workers; L. pallitarsus workers shift foraging activity to a safe,competitor-free patch, even if it is of lower quality (74).

Theories of foraging strategy provide an important organizationalframework with an emphasis on energetics that is valuable for the study of theforaging economy of ants. But optimization models should be cautiouslyapplied because the economics of foraging cannot be studied in isolation fromother aspects of ecology, energetics, social organization, and the intrinsicbehavioral limitations of ants. For example, some models (97) assume foragerknowledge of the resource base as a requirement for optimal feeding strategy,yet the relatively short life span of a forager may limit an individual ant’sexperience. Moreover, if resources are unpredictably distributed, it is difficultto see how such information would modify future individual or colonydecisions. The spatial pattern of foraging may also limit the acquisition ofinformation about resource distribution. Low encounter rates and foragingsuccess may be additional complications. Little is known of the memorycapability of ants in regard to food choice; a few studies show they have theability to store information and use it in foraging decisions (81, 87, 114; R.Johnson, personal communication). Should foragers have knowledge of re-source availability, how are the preferences of individuals summed to yield acolony-wide pattern of choice? The role of these factors in the implementationof foraging strategy is poorly understood.

The social organization of foraging may influence spatial patterns of searchand therefore resource assessment. The trunk trail systems of Atta spp., forexample, originate from pheromone deposition and guide foragers to a tree tobe attacked; ultimately, a path between the nest and the tree is cleared ofobstruction. While this path enhances leaf transport efficiency, it limits ants tosearching for new host trees only near the trunk route’s end and sides (86, 94).Similarly, the use of paths cleared of vegetation by P. occidentalis foragersenhances gain rate but probably canalizes search (32).

SEARCH PATTERN

Search pattern can be analyzed at two levels. First, search concerns the use offoraging space by colonies within populations, and intra- and interspecificterritorial interactions may contribute to the partitioning of space betweencolonies (42, 49, 51, 62, 90, 113, 115). Therefore, search pattern involvescolony-level regulation of the spatial allocation of foragers. Second, each trip


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


200 TRANIELLO

made by a forager has its own ecologically influenced sl~atial and temporalorganization (41, 91, 112, 118, 119). There is also a relationship betweenindividual and colony-wide search patterns, since a forager may influence thesearch patterns of nestmates through communication. At both levels, resourcedistribution in space and time and competition should be major influences onthe organization of search.

Territoriality and Search Pattern

The significance of the spacing patterns of ant colonies and the division offoraging area has chiefly been approached by measuring dispersion and/or bystudying territorial interactions (51, 62). Cost/benefit explanations suggest interplay of the economics of foraging and defense and allow predictions to bemade about how colonies should allocate workers to related tasks in time andspace (51, 58). Dispersion patterns may change seasonally and appear to nonrandom in most species for which data are available (42, 45, 49, 62, 90,115).

Trail systems provide a mechanism by which the search patterns of foragersare directed away from neighboring colonies (42, 49, 90, 113). They alsoreduce search or travel time by directly channeling foragers to a persistentresource (49, 94, 95). In some cases more than one function maybe served.Colonies of P. rugosus and P. barbatus feed at seed patches, and foragerstravel along spatially separated trunk trails; the average nearest-neighbordistance between nests is 17-18 m (49). In contrast, Pogonornyrmex marico-pa takes evenly distributed seeds, and foragers seem to depart randomly fromthe nest and collect seeds individually; colonies of this species are on average46 m apart, apparently owing to the absence of trail systems (49). In bicolor, the radius of an area in which 90% of all search activity occursapproximates the average internest distance (119). In Pheidole militicida,trunk routes branch into smaller trails, and the persistence of use of thesecomponents of the trail system varies, with the trunk being most stable (52).Trunk routes in P. militicida channel foragers to areas where seeds areavailable, and the routes are abandoned when the resources are depleted. Thebiochemical ecology of trail system formation has been studied in regard tolevel of specificity and forager orientation (51, 52, 108, 113). Trail pher-omones may reduce search time by serving as initial guides to areas of highseed density and may also perhaps decrease homing time, although visualcues are also important in orientation (49, 113). In L. neoniger the colony-specific persistent components of trail pheromone appear to direct foragersearch paths away from neighboring colonies, which may be as close as 5 cm(108, 113, 115). The highly directional patterns of foraging become randomfollowing confrontation with foragers from an alien nest, which suggests thatthe trail systems of this species minimize aggressive confrontation withcompetitors (113).


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.



Geometry of Search at the Colony Level

In the desert harvester ant V. pergandei the direction of foraging columns isrotated in a clockwise or counterclockwise manner between consecutiveforaging periods, and the size of a foraging column is adjusted to seedproduction and patch distance (85). As food density decreases, columnsincrease in length and rotate more frequently. Column rotation seems torepresent a system of sectorial search with a radial shift following resourcedepletion. Consecutive raids of the army ant E. burchelli are systematicallyrotated an average of 123° during the statary phase (35). Raiding also appearsto be systematic in the nomadic phase, again seemingly for avoidance ofredundant search. The geometry of search appears to be determined solely byprior raid direction, perhaps with modifications to avoid contact of foragerswith other E. burchelli colonies (35).

Such systematic search during the statary and nomadic phases does not,however, appear to be the rule among army ants. In Neivarnyrmex nigrescensthe directions and distances of emigrations vary unpredictably during thenomadic phase (71). The striking differences in the search and raiding pat-terns of E. burchelli and N. nigrescens may be related to the distribution andabundance of prey or to nest sites and climatic factors (71). However, thedensity of prey species of ants in the southwest desert or grassland environ-ment of N. nigrescens is approximately 3000 colonies/ha (71), and the densityof ant species actually or potentially taken by E. burchelli is on average 6600--- 2200 colonies/ha (range 4000-9000 colonies/ha) (61). The highly orga-nized raid pattern of E. burchelli may therefore reflect selection for efficientprey harvesting given the greater abundance of its prey, but the role of preydistribution is not clear. Limited study of the nomadic obligate termitepredator Pachycondyla (=Termitopone) laevigata has shown no predictableraiding pattern (30).

Search Patterns of Individual Foragers

Forager decisions may include where to search, how long to search at a givensite, and whether or not to return to a site where search was previouslyconducted. Some species, such as Pachycondyla (=Neoponera) apicalis,show strong route fidelity, each worker restricting its foraging activity to agiven site (36). In C. bicolor search effort is concentrated in sectors ofapproximately 50° and 30-m radius, and average search path length differsamong populations according to food availability (119). The search pattern a colony contains random components as evidenced in the exponential dis-tribution of search times of foragers, increasing average distance of search inproportion to the square root of time, and selection of initial foraging direc-tion. Thus the colony-level search pattern approximates a random diffusionprocess, which may be an efficient solution to harvesting food that is un-predictably distributed (41). In F. schaufussi, search pattern is related to food


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


202 TRANIELLO

distribution; collecting a single crop load of carbohydrate food produces amore spatially restricted and accurate search during a return trip than collect-ing a single load of insect prey (J. F. A. Traniello & A. J. Kozol, un-published).

SEARCH DURATION AND PERSISTENCE Search by C. bicolor foragersshows distinctive temporal patterns that are correlated with food availability.Colonies in Greece collect less prey biomass than colonies in Tunisia, andindividuals in Greece make roughly double the number of trips, although tripduration is shorter (119). Trip duration is also dependent upon the type food collected; it is longer for ants collecting plant secretions (39).

The tendency of a forager to return to and search at a site where it has foundfood has been studied in C. bicolor (91) and F. schaufussi (111, 112). In bothspecies foragers differ in their tendency to restrict their search to the site of aprior find. Persistent foragers show intensive local search, whereas nonpersis-tent foragers often completely bypass a prior reward site. In C. bicolor theseindividually different search strategies appear to categorize foragers through-out their lives and reflect foraging specializations. Search pattern in F.schaufussi appears to be adjusted in response to food type, and searchpersistence seems to be correlated with the spatial and temporal persistence ofthe insect prey and homopteran excretions that compose this species’ diet(112). Consecutive rewards of carbohydrate food tend to produce a shift fromnonpersistent to persistent searching and increase search duration (112). Thedegree of spatial accuracy of search is greater in response to feeding oncarbohydrate than on insect prey, but it does not improve with successivemultiple rewards of either type of food, which indicates that spatial patterningof search and information acquired to control search are fixed resource-dependent parameters. However, search duration may be conditioned andmay at least have a local effect on persistence. In C. bicolor, search persis-tence increases with the distance of the food to the nest (91), and in pergandei the frequency of seed sampling in a patch increases with thedistance of the patch from the nest (84). Increasing search time in V. per-gandei results in the sampling of a larger number of seeds in a patch.

SOCIAL REGULATION OF FORAGING

Age Polyethism and Development of Foraging Behavior

Workers of many ant species sequentially change tasks as they mature,beginning with brood care following worker eclosion and culminating withforaging (59, 75). Several factors affect the onset of foraging behavior. Thecompletion of physiological processes related to cuticular sclerotization andthe acquisition of sensory receptor competence may be required before forag-


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.



ing can begin. A callow phase during which tanning takes place may benecessary to provide time for the completion of physiological maturation;these processes occur during pupal development in some species (107).Feeding habits could affect the pattern of age polyethism if brood care isdirectly associated with foraging. This may be true for species such asAmblyopone pallipes that directly provision larvae with prey (107). In thetemporal polyethism of most species, tasks with high associated risks, such asforaging, are scheduled as the ultimate worker contribution to a colony’seconomy (75). Ergonomically, loss is minimized if forager mortality is highbecause foragers hold fewer energy reserves in the form of lipid stores thanyounger workers (67).

The percentage of foragers in a colony varies across species (67, 78). Thetheory of adaptive demography predicts that the proportion of workers allo-cated to foraging should differ among populations in different ecologicalcircumstances if worker age determines the transition to foraging performance(75). Recent field-based empirical tests suggest that age caste ratios are highlyvariable, and the proportion of older workers in a colony shows no clearcorrelation with ecology. Censuses of whole, field-collected Pheidole dentatacolonies from two habitats showing significant differences in food resourcebiomass, ant species diversity, predation, and competitive environment re-vealed that older workers, which are typically foragers, make up a varyingproportion of the total worker force (P. Calabi & J. F. A. Traniello, un-published). Although temporal caste ratios vary, colonies with very differentdemographic profiles have very similar labor profiles. This suggests thatchanging foraging requirements are met by rapid changes in the task perfor-mance patterns of individual workers in response to colony need rather thanby changes in age demography. This intercolony consistency in the proportionof total labor involved in foraging suggests a flexible switching of thebehavior of individual workers in response to immediate foraging require-ments. A worker’s shift from another task to foraging is therefore related notonly to age but also to the perception of social stimuli carrying informationabout the current nutritional status of a nest and/or the activities of othercolony members. In Novomessor albisetosus, callow workers in colonies inwhich older workers were experimentally removed matured behaviorally inone third the time of normal development and began foraging at an earlier agethan workers in unmanipulated control colonies (69). This type of sociallymediated behavioral development appears to be common in ants (59).Flexibility in temporal polyethism appears to represent a major mechanism ofsocial compensation of forager number in response to short-term ecologicalfluctuations.

Studies of trail system organization in Formica spp. have illustrated therole of age polyethism in the development of foraging behavior (15, 87).Foragers captured and marked in autumn and recaptured in the spring retained


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


204 TRANIELLO

the use of their initial route through a period of winter inactivity. Thesetopographic traditions result in a transfer of spatial foraging informationthrough several worker generations. Rootes have a spatiotemporal polyethicstructure; mature (pioneer) foragers head the foraging column, whereas youn-ger workers (recruits) are found close to the nest. The behavior of youngforagers gradually changes to that of mature foragers, as evidenced fromchanges in their location along a foraging trail.

Because foraging behavior is often coordinated through chemical com-munication, maturatiorial, social, or perceptual abilities may be associatedwith the onset of foraging. Callow army ants (N. nigrescens) travel alongchemical trails with other colony members during emigration on the firstnomadic day but do not begin foraging (raiding) until they are 3-7 days old.The absence of foraging behavior is not due to the sensory inability ofcallows, however, as these immature workers tbllow artificial trails as well asadults; thi~ suggests that other social stimuli affect the development offoraging (102). That callows remain in the nest while mature workers conductraids seems to be due to the absence of mechanical stimuli that are part of themass-recruitment communication signals that accompany emigration and arerequired by callows to induce trail following (103).

LEARNING AND FORAGING BEHAVIOR

The unpredictability of the resource environment of a colony may require thatforaging be fine-tuned through experience-based change in the behavior ofindividual workers to enhance efficiency. Simple and complex types oflearning have been described in ants, which may reflect selection for learningtraits that have evolved in response to dietary habits and foraging ecologyunder the constraints of life span, sociality, and caste and the temporal,spatial, and size variability of food resources. Recent studies of ant learninghave emphasized either ecology (81) or theoretical modeling (27, 28); addi-tional empirical studies on the natural history of ant learning will be useful indefining the limits of individual flexibility and measuring forager competence(44). Veromessor pergandei and P. rugosus foragers develop preferences forharvesting the seeds of certain plants, which results in an individual foragingspecialization that may persist for up to two weeks or longer (81). Learningrate and memory retention may be correlated with spatial variability in seedspecies in these ants (R. Johnson, personal communication). Similar foragerspecializations appear to occur in Chelaner spp. (25). The mechanism specialization may be a learning process that permits a forager to identifyqualitative properties of seeds and to narrow search image quickly to fix on aspecific foraging task. This specialization may increase the net rate of energyreturned to the colony. Learning may also have a role in the development of


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.



foraging in other species. In omnivorous species such as Formica spp. andCataglyphis spp., workers tend homopterans or lick plants to collect carbo-hydrate secretions and also forage for arthropod prey (111, 112, 119). Thesetwo resources differ in their spatial and temporal patterns of distribution andtherefore provide different patterns of reward. Workers of C. bicolor tend tospecialize on collecting either type of food (39). In F. schaufussi, the abilityof workers to modify their search behavior seems to depend on a foodresource-dependent learning process. Local search duration is more easilyconditioned by carbohydrate food rewards (sucrose) than by protein (freshlykilled insects) (111, 112). The conditioning of search duration by carbo-hydrate food seems to be independent of resource quality. Repeated rewardsof insect prey do not produce a more accurate search pattern, nor do theyresult in increased search effort. Search accuracy is greater after a reward of asingle crop load of I-M sucrose than after a reward of insect prey. However,for a given food type, there is no significant change in search accuracy overfour or eight consecutive rewards (J. F. A. Traniello & A. J. Kozol, un-published). Further studies are needed to determine if foraging specializationsdevelop through resource-related learning processes. Resource-related learn-ing processes may also be involved in the persistence of route fidelity andmemory shown in Formica spp. (18, 88). At the colony level, learning mayunderlie competitor recognition systems and may mediate community in-teractions (13).

CONCLUSIONS

The principal ecological determinants of ant foraging strategy are the distribu-tion of food resources in size, time, space, and quality; competition withsympatric ant species; and predation. Because a colony is generally sessile,the resource and competitive environment is in essence defined by its loca-tion. A colony must therefore spatially pattern foraging to harvest foodefficiently and minimize competition. This is accomplished through in-dividual and colony-wide foraging.

Elements of social organization are linked to virtually every aspect offoraging strategy. Although patterns of physical and temporal caste evolutionhave been shown to be integral components of some foraging systems, moresensitive empirical tests are required to provide detailed explanations of theorigin and ecological significance of forager size and age-related behavior.Similarly, forager functional morphology and biomechanical characteristicsassociated with loading capacity should be examined to describe precisely therole of form as well as size and behavior in ant foraging ecology. The overallconceptualization of ant foraging strategy should therefore encompass theoryand analyses on subjects ranging from the major elements of colony organiza-


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


206 TRANIELLO

tion such as caste and division of labor to the time and energy budgets offoragers. Although in this review I have suggested a components approach,foraging systems must be analyzed as whole entities. The pitfalls of extremeadaptationist reasoning that might develop from fragmenting the systemshould and can be avoided through an emphasis on social integration. Aprudent application of foraging models, theories on caste evolution andecology, and basic knowledge of natural history and social regulatory mech-anisms can provide the necessary theoretical and empirical framework. Final-ly, it will be possible to evaluate ant foraging strategy fully when theenergetics of foraging and the caloric and nutritional benefits of selectedresources are quantitatively measured and used to estimate the conversion offood intake into alates. This analysis will remove the inaccuracies of assump-tions of the energetic costs of foraging and will permit colony foragingeconomics to be quantified in terms of reproductive output.

ACKNOWLEDGMENTS

I thank many colleagues for their reprints and unpublished manuscripts, andregret that a lack of space prohibited me from including the results of a largernumber of studies. The manuscript benefited from critical readings by SamuelBeshers, Michelle Scott, and Steve Rissing. I gratefully acknowledge thesupport of the National Science Foundation and the Whitehall Foundation.

Li~rature Ci~d

1. Adams, E. A., Traniello, J. F. A. 1981.Chemical interference competition byMonomorium minimum. Oecologia 51:270-75

2. Andersen, A. N. 1986. Patterns of antcommunity organization in mesic south-eastern Australia. Aust. J. Ecol. 11:87-97

3. Bartholomew, G. A., Lighton, J. R. B.,Feener, D. H. 1988. Energetics of trailrunning, load carriage, and emigrationin the column-raiding army ant Ecitonhamatum. Physiol. Zool. 61:57-68

4. Bernstein, R. 1974. Seasonal food abun-dance and foraging activity in some des-ert ants. Am. Nat. 108:490-98

5. Bernstein, R. 1975. Foraging strategiesof ants in response to variable food den-sity. Ecology 56:213 19

6. Bowers, M. A., Porter, S. D. 1981.Effect of foraging distance on water con-tent of substrates harvested by Atta co-lumbica (Guerin). Ecology 62:273-75

7. Breise, D. T. 1982. Patterning of re-sources amongst seed-harvesting ants inan ant community in semi-arid Aus-tralia. Aust. J. Ecol. 7:299-307

8. Breise, D. T., Macauley, B. J. 1981~Food collection within an ant communi-ty in semi-arid Australia, with specialreference to seed harvesters. Aust. J.Ecol. 6:1-19

9. Brian, M. V. 1978. Production Ecologyof Ants and Termites. Cambridge, Mass:Cambridge Univ. Press

10. Brian, M. V. 1983. Sociallnsects: Ecol-ogy and Behavioural Biology. London:Chapman & Hall

11. Buckley, R. C. 1982. Ant-Plant In-teractions in Australia. The Hague: Junk

12. Burton, J. L., Franks, N. R. 1985. Theforaging ecology of the army ant Ecitonrapax: an ergonomic enigma? Ecol. En-tomol. 10:131--41

13. Carlin, N. F., Johnston, A. 1984.Learned enemy specification in the de-fense recruitment system of an ant.N aturwissenschaften 71:156-57

14. Carroll, C. R., Janzen, D. H. 1973.Ecology of foraging by ants. Ann. Rev.Ecol. Syst. 4:231-57

15. Cherix, D. 1987. Relation between dietand polyethism in Formica colonies. SeeRef. 76, pp. 93-115


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.



16. Chew, R. M., Chew, A. E. 1980. Bodysize as a determinant of small-scale dis-tribution of ants in evergreen woodlandin southeastern Arizona. lnsectes Soc.27:18~20

17. Chew, R. M., DeVita, J. 1980. Forag-ing characteristics of a desert ant assem-blage: functional morphology and spe-cies separation. J. Arid Environ. 3:75-83

18. Cosens, D., Toussaint, N. 1985. An ex-perimental study of the foraging strategyof the wood ant Formica aquilonia.Anim. Behav. 33:541-52

19. Crawford, D. L., Rissing, S. W. 1983.Regulation 0f recruitment by individualscouts in Formica oreas Wheeler (Hy-menoptera; Formicidae). Insectes Soc.30:177-83

20. Culver, D. 1974. Species packing inCaribbean and north temperate ant com-munities. Ecology 55:974-88

21. Davidson, D. W. 1977. Species diver-sity and community organization in des-ert seed-eating ants. Ecology 58:711-24

22. Davidson, D. W. 1977. Foraging ecolo-gy and community organization in seed-eating ants. Ecology 58:725-37

23. Davidson, D. W. 1978. Experimentaltests of the optimal diet in two socialinsects. Behav. Ecol. Sociobiol. 4:35-41

24. Davidson, D. W. 1978. Size variabilityin the worker caste of a social insect(Veromessor pergandei Mayr) as a func-tion of the competitive environment.Am. Nat. 112:523-32

25. Davison, E. A. 1982. Seed utilization byharvester ants. See Ref. 11, pp. 1-6

26. Davison, E. A. 1987. Respiration andenergy flow in two Australian species ofdesert harvester ants, Chelaner roth-steini and Chelaner whitei. J. Arid. En-viron. 12:61-82

27. Deneubourg, J. L. 1985. The role oferrors and memory in the efficiency ofant foraging. Ann. Soc. t{. Zool. Belg.115:109-10

28. Deneubourg, J. L., Goss, S., Pasteels,J. M., Fresneau, D., Lachaud, J. P.1987. Self-organizing mechanisms inant societies (II): Learnirtg in foragingand division of labor. See Ref. 76, pp.177-96

29. DeVita, J. 1979. Mechanisms of in-terference and foraging among coloniesof the harvester ant Pogonomyrmex cali-fornicus in the Mojave Desert. Ecology60:729-37

30. Downing, H. 1978. Foraging and mi-gratory behavior of the ponerine antTermitopone laevigata. BA thesis.Smith Coll., Northampton, Mass. 121pP.

31. Fellers, J. H. 1987. Interference and ex-ploitation in a guild of woodland ants.Ecology 68:1466-78

32. Fewell, J, 1988. Energetic and timecosts of foraging in harvester ants,Pogonomyrmex occidentalis. Behav.Ecol. Sociobiol. 22:401-8

33. Franks, N. R. 1985. Reproduction,foraging efficiency, and worker poly-morphism in army ants. In ExperimentalBehavioral Ecology and Sociobiology,ed. B. H/511dobler, M. Lindaner, pp. 81-108. Stuttgart: Fischer

34. Franks, N. R. 1986. Teams in socialinsects: group retrieval of prey by armyants (Eciton burchelli, Hymenoptera:Formicidae). "Behav. Ecol. Sociobiol.18:425-29

35. Franks, N. R., Fletcher, C. A. 1983.Spatial patterns in army ant foraging andmigration: Eciton burchelli on BarroColorado Island, Panama. Behaw Ecol.Sociobiol. 12:261 ~70

36. Fresneau, D. 1985. Individual foragingand path fidelity in a ponerine ant. ln-sectes Soc. 32:109-16

37. (3entry, J. B. 1974. Response to preda-tion by colonies of the Florida harvesterant Pogonomyrmex badius. Ecology55:1328-38

38. Hansen, S. E. 1978. Resource utiliza-tion and coexistence of three species ofPogonomyrmex ants in an upper Sonorangrassland community. Oecologia 35:105-17

39. Harkness, M. L. R., Harkness, R. D.1970. Functional differences betweenindividual ants Cataglyphis bicolor. J.Physiol. 25:124-25

40. Harkness, R. D. 1978. The speed ofwalking of Cataglyphis bicolor (F.)(Hym., Formicidae). Entomol. Mon.Mag. 114:203-10

41. Harkness, R. D., Maroudas, N. G.1985. Central place foraging by an ant(Cataglyphis bicolor Fab.): a modelof searching. Anita. Behav. 33:916-28

42. Harrison, J. S., Gentry, J. B. 1981.Foraging pattern, colony distribution,and foraging range of the Florida harves-ter ant, Pogonomyrmex badius. Ecology62:1467-73

43. Heinrich, B. 1978. The economics ofinsect sociality. In Behavioural Ecology,ed. J. Krebs, N. Davies, pp. 97-128.Sunderland, Mass: Sinauer

44. Herbers, J. M. 1981. Reliability theoryand foraging by ants. J. Theor. Biol.89:175-89

45. Herbers, J. M. 1985. Seasonal structur-ing of a north temperate ant community.lnsectes Soc. 32:224~10


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


208 TRANIELLO

46. Hespenheide, H. A. 1973. Ecologicalinferences from morphological data.Ann. Rev. Ecol. Syst. 4:213-30

47. Hespenheide, H. A. 1975. Prey charac-teristics and predator niche width. InEcology and Evolution of Communities,ed. M. L. Cody, J. M. Diamond, pp.158-80. Cambridge, Mass: Belknap

48. Holder Bailey, K., Polis, G. A. 1987.Optimal and central place foragingtheory applied to a desert harvester ant,Pogonomyrmex californicus. Oecologia72:440~8

49. HOlldobler, B. 1976. Recruitment be-havior, home range orientation and ter-ritoriality in harvester ants, Pogono-myrmex. Behav. Ecol. Sociobiol. 1:3-44

50. H611dobler, B. 1984. Evolution of insectcornmunication. In Insect Communica-tion, ~d. T. Lewis, pp. 349-77. London:Academic

51. Hrlldobler, B., Lumsden, C. 1980. Ter-ritorial strategies in ants. Science 210:732-39

52. H611dobler, B., Moglich, M. 1980. Theforaging system of Pheidole militicida(Hymenoptera: Formicidae). lnsectesSoc. 27:237-64

53. Hrlldobler, B., Stanton, R. C., Markl,H. 1978. Recruitment and food-retriev-ing behavior in Novomessor (Formici-dae: Hymenoptera). I. Chemical signals.Behav. Ecol. Sociobiol. 4:163-81

54. H611dobler, B., Traniello, J. F. A. 1980.The pygidial gland and chemical recruit-ment communication in Pachycondyla(= Termitopone) laevigata. J. Chem.Ecol. 6:883-93

55. Howard, J. J. 1987. Leaf~utting ant dietselection: the role of nutrients, water,and secondary chemistry. Ecology 68:503 15

56. Hunt, J. H. 1983. Foraging and mor-phology in ants: the role of vertebratepredators as agents of natural selection.See Ref. 57, 2:83-103

57. Jaisson, P. 1983. Social Insects in theTropics, Vol. 1, 2. Paris: Presses Univ.Paris XIII

58. Johnson, L. K., Hubbell, S. P., Feener,D. H. 1987. Defense of food supply byeusocial colonies. Am. Zool. 27:347-58

59. Lenoir, A. 1987. Factors determiningpolyethism in social insects. See Ref.76, pp. 219-40

60. Leonard, J. G., Herbers, J. M. 1986.Foraging tempo in two woodland antspecies. Anim. Behav. 34:1172-81

61. Levings, S. C., Franks, N. R. 1982.Patterns of nest dispersion in a tropicalground ant community. Ecology 63:338-44

62. Levings, S. C., Traniello, J. F. A. 1982.Territoriality, nest dispersion, and com-munity structure in ants. Psyche 88:265-319

63. Lighton, J. R. B., Bartholomew, G. A.,Feener, D. H. 1987. Energetics of loco-motion and load carriage and a model ofthe energy cost of foraging in the leaf-

. cutting ant Atta colombica Guer. Physi-ol. Zool. 60:524-37

64. Longhurst, C., Johnson, R. A., Wood,T. G. 1978. Predation by MegaponeraJbetens (Fabr.) (Hymenoptera: Formici-dae) on termites in the Nigerian southernguinea savanna. Oecologia 32:101-7

65. Lynch, J. F., Balinksy, E. C., Vah, S.G. 1980~ Foraging patterns in three sym-patric forest ant species, Prenolepis im-puris, Paratrechina melanderi, andAphaenogaster rudis (Hymenoptera:Formicidae). Ecol. Entomol. 5:353--71

66. MacKay, W. P. 1982. The effect of pre-dation of western widow spiders Lat-rodectus hesperus (Araneae:Theridiiae)on harvester ants Pogonomyrmex rugo-sus (Hymenoptera:Formicidae). Oecolo-gia 53:406-11

67. MacKay, W. P. 1985. A comparison ofthe energy budgets of three species ofPogonomyrmex harvester ants (Hyme-noptera: Formicidae). Oecologia 66:484-94

68. Maschwitz, U., Schonegge, P. 1983.Forage communication, nest movingrecruitment and prey specialization inthe oriental ponerine Leptogenys chinen-sis..Oecologia 57:175-82

69. McDonald, P., Topoff, H. 1985. Socialregulation of behavioral development inthe ant Novomessor albisetosus (Mayr).J. Comp. Psychol. 99:3-14

70. Mirenda, J. T., Eakins, D. G., Gravelle,K., Topoff, H. 1980. Predatory be-havior and prey selection by army ants ina desert-grassland habitat. Behav. Ecol.Sociobiol. 7:119-27

71, Mirenda, J. T., Topoff, H. 1980.Nomadic behavior of army ants in a des-err-grassland habitat. Behav. Ecol. So-ciobiol. 7:129-35

72. Morton, S. R. 1982. Granivory in theAustralian add zone: diversity of harves-ter ants and structure of their communi-ties. In Evolution of the Flora andFauna of Arid Australia, ed. W. R. Bar-ker, P. J. M. Greenslade, pp. 257-62.Adelaide, Australia: Peacock

73. Nielsen, M. G., Jensen, T. F., Holm-Jensen, I. 1982. Effect of load carriageon the respiratory metabolism of runningworker ants of Camponotus herculeanus(Formicidae). Oikos 39:137-42

74. Nonacs, P., Dill, L. M. 1988. Foraging


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.



responses of the ant Lasius pallitarsus tofood sources with associated mortality.lnsectes Soc. In press

75. Oster, G., Wilson, E. O. 1978. Casteand Ecology in the Social Insects.Princeton, NJ: Princeton Univ. Press

76. Pasteels, J. M., Deneubourg, J. L.1987. From Individual to Collective Be-haviour in Social Insects. Basel: Birk-hauser

77. Peakin, G. J., Josens, G. 1978. Respira-tion and energy flow. See Ref. 9, pp.111-63

78. Porter, S. D., Jorgenson, C. D. 1981.Foragers of the ant, Pogonornyrmexowyheei: a disposable caste? Behav.Ecol. Sociobiol. 9:247-56

79. Rettenmeyer, C. ’W., Chadab-Crepet,R., Naumann, M. G., Morales, L.1983. Comparative foraging by neotro-pical army ants. See Ref. 57, 2:5%73

80. Reyes L0pez, J. L, 1987. Optimal forag-ing in seed harvester ants: computer-aided simulation. Ecology 68:1630-33

81. Rissing, S. W. 1981. Foraging spe-cializations of individual seed-harvesterants. Behav. Ecol. SociobioL 9:149-52

82. Rissing, S. W. 1982. Foraging velocityof seed-harvester ants, Veromessor per-gandei (Hy~nenoptera: Formicidae). En-viron. Entomol. 11:905-7

83. Rissing, S. W. 1987. Annual cycles inworker size of the seed-harvester antVeromessor pergandei (Hymenoptera:Formicidae). Behav. Ecol. Sociobiol.20:117-24

84. Rissing, S. W., Pollock, G. 13. 1984.Worker size variability and foragingefficiency in Veromessor pergandei(Hymenoptera: Formicidae). Behav.Ecol. Sociobiol. 15:121-26

85. Rissing, S. W., Wheeler, J. 1976. Fo-raging responses of Veromessor per-gandei to changes in seed production.Pan-Pac. Entomol. 52:63-72

86. Rockwood, L., Hubbell, S. P. 1987.Host-plant selection, diet diversity, andoptimal foraging in a tropical leafcuttingant. Oecologia 74:55-61

87. Rosengren, R. 1977. Foraging strategyof wood ants, Formica rufa group. Part1. Age polyethism and topographictraditions. Acta Zool. Fenn. 149:1-30

88. Rosengren, R., Fortelius, W. 1986. Or-streue in foraging ants of the Formicarufa group~hierarchy of orienting cuesand long-term memory, lnsectes Soe.33:306-37

89. Rudolph, S. G_, Loudon, C. 1986. Loadsize selection by foraging leaf-cutter ants(Atta cephalotes). Ecol. Entomol. 11:401-10

90. Ryti, R. T., Case, T. J. 1986. Over-dispersion of ant colonies: a test of hy-potheses. Oecologia 69:446-53

91. Schmid-Hempel, P. 1984. Individuallydifferem foraging methods in the desertant Cataglyphis bicolor (Hymenoptera,Formicidae). Behav. Ecol. Sociobiol.14:263-71

92. Schmid-Hempel, P. 1987. Foragingcharacteristics of the desert ant Cata-glyphis. See Ref. 76, pp. 43-61

93. Schmid-Hempel, P., Schmid-Hempel,R. 1984. Life duration and turnover offoragers in the ant Cataglyphis bicolor(Iqymenoptera, Formicidac). InsectesSoc. 31:345-60

94. Shepherd, J. D. 1982. Trunk trails andthe searching strategy of a leaf-cutter antAtta colombica. Behav. Ecol. Sociobiol.I 1:77-84

95. Shepherd, J. D. 1985. Adjusting forag-ing effort to resources in adjacent colo-nies of the leaf-cutter ant, Atta col-ombica. Biotropica 17:245-52

96. Sorensen, A. A., Busch, T. M., Vinson,S. B. 1983. Behaviour of worker sub-castes in the fire ant, Solenopsis invicta,in response to proteinaceous food. Phys-iol. Entomol. 8:83-92

97. Stephens, D. W, Krebs, J. R. 1986.Foraging Theory. Princeton, NJ: Prince-ton Univ. Press

98. Stradling, D. J. 1978. Food and feedinghabits of ants, See Ref. 9, pp. 81-106

99. Sudd, J. H. 1987. Individual behaviorand mixed diet strategy in ants. See Ref.76, pp. 81-92

100. Taylor, F. 1976. Foraging behavior inants: experiments with two species ofmyrmecine ants. Behav. Ecol. Socio-biol. 2:147-68

101. Taylor, F. 1978. Foraging behavior ofants: theoretical considerations. J.Theor. Biol. 71:541-65

102. Topoff, H., Boshes, N., Trakimas, W.1972. A comparison of trail followingbetween callow and adult workers of thearmy ant (Neivamyrmex nigrescens)(Formicidae: Dorylinae). Anita. Behav.20:361-66

103. Topoff, H., Mirenda, J. 1978. Precocialbehaviour of callow workers of the armyant Neivamyrmex nigrescens: impor-tance of stimulation by adults duringmass recruitment. Anim. Behav. 26:698-706

104. Topoff, H., Mirenda, J. 1980. Armyants do not eat and run: influence of foodsupply on emigration behaviour inNeivamyrmex nigrescens. Anita. Behav.28:1040-45

105. Topoff, H., Mirenda, J. 1980. Army


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


210 TRANIELLO

ants on the move: relation between foodsupply and emigration frequency. Sci-ence 207:1099-100

106. Traniello, J. F. A. 1977. Recruitmentbehavior, orientation, and the organiza-tion of foraging in the carpenter antCamponotus pennsylvanicus DeGeer.Behav. Ecol. Sociobiol. 2:61-79

107. Traniello, J. F. A. 1978. Caste in aprimitive ant: absence of age polyethismin Ambylopone. Science 202:770-72

108. Traniello, J. F. A. 1980. Colonyspecificity in the trail pheromone of anant. Naturwissenschaften 67:360

109. Traniello, J. F. A. 1983. Social organ-ization and foraging success in Lasiusneoniger (Hymenoptera: Formicidae):behavioral and ecological aspects ofrecruitment communication. Oecologia59:94-100

110. Traniello, J. F. A. 1987. Comparativeforaging ecology of north temperateants: the role of worker size and coop-erative foraging in prey selection, ln-sectes Soc. 34:118-30

111. Traniello, J. F. A. 1987. Individual andsocial modification of behavior in re-sponse to environmental factors in ants.See Ref. 76, pp. 63-80

112. Traniello, J. F. A. 1988. Variation inforaging behavior among workers of theant Formica schaufussi: ecologicalcorrelates of search behavior and themodification of search pattern. In ln-terindividual Behavioral Variabili~. inSocial Insects, ed. R. L. Jeanne, pp.91-112. Boulder, Colo: Westview

113. Traniello, J. F. A. 1988. Chemical trailsystems, orientation, and territoriality in

the ant Lasius neoniger. J. Insect Behav.In press

114. Traniello, J. F. A., Fujita, M. S., Bo-wen, R. V. 1984. Ant foraging be-havior: Ambient temperature influencesprey selection. Behav. Ecol. Sociobiol.15:65-68

115. Traniello, J. F. A., Levings, S. C. 1986.Intra- and intercolony patterns of nestdispersion in the ant Lasius neoniger:correlations with territoriality and forag-ing ecology. Oecologia 69:413-19

116. Waller, D. A. 1982. Leaf-cutting antsand avoided plants: defenses against Attatexana attack. Oecologia 52:400-3

117. Waller, D. A. 1982. Leaf-cutting antsand live oak: the role of leaf toughness inseasonal intraslSecific host choice. En-tomol. Exp. Appl. 32:145-50

118. Wehner, R. 1987. Spatial organizationof foraging behavior in individuallysearching desert ants, Cataglyphis (Sa-hara Desert) and Ocymyrmex (NamibDesert). See Ref. 76, pp. 1542

119. Wehner, R., Schmid-Hempel, P., Hark-ness, R. D. 1983. Foraging Strategies inIndividually Searching Ants Cataglyphisbicolor. Stuttgart: Fischer

120. Whitford, W. G. 1978. Foraging byseed-harvester ants. See Ref. 9, pp.107-110

121. Whitford, W. G., Bryant, M. 1979. Be-havior of a predator and its prey: thehorned lizard (Phrynosoma cornutum)and harvester ants (Pogonomyrmexspp.). Ecology 60:68(~94

122. Wilson, D. S. 1975. The adequacy ofbody size as a niche indicator. Am. Nat.109:769-84


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.


Ann

u. R

ev. E

ntom

ol. 1

989.

34:1

91-2

10. D

ownl

oade

d fr

om a

rjou

rnal

s.an

nual

revi

ews.

org

by O

ntar

io C

ounc

il of

Uni

vers

ities

Lib

rari

es o

n 03

/23/

07. F

or p

erso

nal u

se o

nly.

foraging strategies of ants traniello

Documents