a review of ecological determinants of territoriality within vertebrate species

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A Review of Ecological Determinants of Territoriality within Vertebrate SpeciesAuthor(s) CHRISTINE R MAHER and DALE F LOTTSource The American Midland Naturalist 143(1)1-29 2000Published By University of Notre DameDOI httpdxdoiorg1016740003-0031(2000)143[0001AROEDO]20CO2URL httpwwwbiooneorgdoifull1016740003-0031282000291435B00013AAROEDO5D20CO3B2

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1

The American Midland NaturalistPublished Quarterly by The University of Notre Dame Notre Dame Indiana

Vol 143 No 1January 2000

Am Midl Nat 1431ndash29

A Review of Ecological Determinants of Territoriality withinVertebrate Species

CHRISTINE R MAHER1

Department of Biological Sciences University of Southern Maine Portland 04104

AND

DALE F LOTTDepartment of Wildlife Fish and Conservation Biology University of California Davis 95616

ABSTRACTmdashWe reviewed papers that compared intraspecific variation in territoriality vsalternative forms of spatial or behavioral organization with three goals (1) to discover whichecological variables act as determinants of territorial behavior and how they might act (2)to extract and evaluate predictions and evidence for determinants of territoriality and (3)to suggest ways for future studies to build upon what the review revealed Twenty ecologicalvariables have been predicted correlated with or experimentally demonstrated to relate toterritoriality within vertebrate species These variables include several characteristics of foodquantity predictability distribution quality renewal rate type density and assessibility Othervariables include nonfood resources population density habitat features mates space ref-ugesspawninghome sites predation pressure host nests (for brood parasites) and energyavailability We suggest several reasons why food resources are cited most often includingtheir biological significance ease of study and publishability of negative results Certaingroups of animals lend themselves to certain methods of study and therefore constrain thevariables measured Many variables are the subjects of apparently contradictory reports iesome papers report that an increase in a given variable increases territoriality and othersreport that a decrease in the variable increases territoriality After summarizing these reportswe hypothesized U-shaped relationships between the ecological variables and behavior thatcould accommodate all these findings However these hypotheses cannot be tested rigorouslyby most current studies because of methodological limitations We recommend a shift toquantification of intraspecifically varying spacing systems combined with simultaneous quan-tification of several ecological variables Relative importance of different determinants ofparticular spacing systems can be revealed via multiple regression analysis Hypothesizedcausal pathways in which one ecological variable determines another variable that in turndetermines territoriality can be tested by path analysis

1 Corresponding author Telephone (207)780-4612 FAX (207)228-8288e-mail cmaherusmmaineedu

2 143(1)THE AMERICAN MIDLAND NATURALIST

INTRODUCTION

Many studies have analyzed the ecological variables determining whether a vertebratepopulation expresses territoriality or an alternative form of spatial organization Grant(1993) reviewed some of this literature primarily that on fish but no one has reviewed thislarge volume of information for all vertebrate taxa to synthesize and evaluate the collectivedata

This paper has three goals The first goal is descriptive We report the ecological deter-minants of territoriality proposed and studied research approaches taken and species stud-ied We asked Are variables predicted to determine territoriality different from those cor-related with the spacing system Which variables have causal effects Are the same variablescited for all taxa

The second goal is synthetic To extract the maximum available information about rela-tionships of specific ecological variables to territoriality both in the investigatorsrsquo thinkingand in their data we compiled the literature by individual ecological variables or combi-nations of variables We evaluated the strength of the empirical evidence and we attemptedto understand why some studies reported a different relationship than others eg largeamounts of food lead to territoriality vs abolish it When authors proposed a causal pathwayin which one variable changed another which then determined a spacing system we re-corded the pathway and asked do authors expect these intervening variables to affect spatialorganization in similar ways eg do authors agree on how food quantity is expected toalter intruder pressure and how intruder pressure then alters territorial behavior

The third goal is methodological We take what we learned about the evidence andmethodological issues and recommend more emphasis on the use of multivariate statisticsto analyze relationships between quantified ecological variables and quantitatively describedsocial systems

CRITERIA FOR SELECTING PAPERS FOR REVIEW

We attempted a complete search of the vertebrate literature with no restrictions on timeperiod or journal to find papers meeting several criteria We chose papers in which theauthors attempted to understand vertebrate territoriality by comparing differences in eco-logical conditions with intraspecific differences in social organization Populations could bespatially separated groups of conspecifics or they could be the same group of animals stud-ied at different times eg before and after manipulation Because we wanted to exploredifferences in social organization we examined papers that addressed presence or absenceof territoriality rather than changes in territory size (eg MacDonald and Carr 1989) Sinceleks are small compressed territories we excluded reports of large territory vs lekkingpopulations (eg Clutton-Brock et al 1988)

Territoriality has been defined many ways (reviewed in Maher and Lott 1995) We pro-pose the following definition of territory a fixed space from which an individual or groupof mutually tolerant individuals actively excludes competitors from a specific resource orresources (Maher and Lott 1995) Relatively few authors operationally defined territorialityso we usually had to rely on conceptual definitions of territoriality We included papersusing a stated or implied definition of territory as a defended area andor an area ofexclusive use In species or situations where defense is difficult to observe (eg small car-nivores) territory sometimes is inferred from exclusive use (Maher and Lott 1995)

In the papers we selected authors identified environmental variables believed to be re-sponsible for differences in spacing systems We primarily used the authorsrsquo terms for en-vironmental variables or we followed Warnerrsquos (1980) definitions of food density variability

2000 3MAHER amp LOTT TERRITORIALITY IN VERTEBRATES

and predictability We excluded demographic variables such as age distribution and sexratio that pertain to the population itself Since population density often is determined byexternal environmental conditions we included it in the review

CURRENT STATE OF THE LITERATURE

CATEGORIES OF INFORMATION

We placed papers into one of three categories depending on the type of relationshipbetween the ecological variable and spatial organization (1) Authors predicted a priorithat territoriality would be determined by a specific ecological variable (eg Armstrong1992) yet authors may or may not have tested these predictions Predictions reveal anauthorrsquos thinking but they are not evidence and we report them simply as predictionsThese studies are indicated by the symbol [P] after the citation (2) Authors interpreteddata about specific ecological variables as being correlated with territoriality (eg Fitch andShapiro 1990) Correlations between a variable and territoriality provide more compellingevidence than predictions alone These studies are indicated by the symbol [C] followingthe citation (3) Authors experimentally demonstrated that an ecological variable deter-mined territoriality usually by manipulating the variable and observing which spacing sys-tem was expressed (eg Ims 1988) These studies provide the most compelling evidencebecause they test causal effects and because investigators usually control all but a smallnumber of variables They are indicated by the symbol [E] following the citation

ECOLOGICAL DETERMINANTS OF TERRITORIALITY AND THE IMPORTANCE OF FOOD

Twenty variables were cited as influencing the expression of intraspecific territorialityand more papers presented evidence of correlations between variables and spacing systemsthan demonstrated or predicted the relationship (Table 1) Fifty-five percent of papersreporting experimental manipulations cited at least one of three variables food quantityfood distribution and population density Food and its many subcategories were universalfactors they were predicted correlated with and experimentally demonstrated to affectspacing systems The broad heading of food included eight variables assessibility (degreeto which food characteristics can be monitored by individuals) food density (quantity offood per unit area) distribution (degree of patchiness or aggregation) predictability (de-gree to which food patches are dependably available) quality (nutritional characteristics)quantity (amount of food available) renewal rates (degree to which the resource is replen-ished per unit time) and type (diet such as fruit or insects) Food quantity was cited inmore papers (24) than any other ecological variable and appeared in each category alongwith food distribution predictability quality and renewal rate

Perhaps these patterns reflect the authorsrsquo approaches to the study of spacing systemsRelatively few studies (23) manipulated ecological variables and observed the effects onspacing systems probably because of problems associated with demonstrating causation(eg controlled conditions in field settings) Whereas food quantity food distribution andpopulation density may be the most important variables the logistics of field experimentsalso may explain why these variables were tested most widely

The importance of food in determining spatial organization may be overplayed (Stamps1994) Because ease of study is a confounding factor in studies of food importance wecannot use frequency of study as a reliable guide to biological significance Obviously foodis an important resource for animals and it is relatively easy to quantify and manipulateFurthermore animals usually are most conspicuous when they feed and much behavioraldata can be collected at that time Whereas the importance of food has been studied inmany species some of the best developed analyses of territoriality have been conducted in


TABLE 1mdashEcological variables listed by category influencing territoriality and the number of papersdiscussing that variable

Variable

Category of relationship

Predicted CorrelatedExperimentallydemonstrated

Food

Quantity 11 36 12Distribution 11 27 10Predictability 4 16 6Quality 1 4 1Renewal rate 2 2 1Type 0 6 0Density 0 2 0Assessibility 0 0 1

Resources

Distribution 0 6 1Quantity 0 1 0Predictability 0 1 0Quality 0 1 0

Population density 2 19 9Habitat features 6 12 3Mates 2 3 6Space 1 2 5Refugesspawninghome sites 1 5 1Predation pressure 0 3 0Host nests 1 2 0Energy availability 0 0 1

nectarivorous birds perhaps because food and energy expended in defense are quantifiedeasily in calories and because energy from food is manipulated easily (eg honeyeatersPhylidonyris novaehollandiae and P nigra Armstrong 1992 [P E] McFarland 1994 [E]Hawaiian honeycreeper Vestiaria coccinea Carpenter and MacMillen 1976 [P C E] reviewCarpenter 1987 [C E] golden winged sunbirds Nectarinia reichenowi Gill and Wolf 1975[C E]) Because of the physiological demands of nectarivores food probably is an impor-tant determinant of spacing systems in these animals however broad generalizations toother taxa eg ectotherms may not be justified

Food could be seen as the most important ecological variable if it explained most of thestatistical variance in experimental results However few investigators examined the amountof variance explained by each ecological variable Also many variables are not independentof each other Analyses such as partial correlation or multiple analysis of variance can beused to assign relative importance to quantified variables but relatively few researchersquantify ecological or behavioral data

Another reason for the apparent importance of food may be related to the lsquolsquofile drawerproblemrsquorsquo ie positive results tend to be published more often than negative results (Csadaet al 1996) For example if a researcher manipulated food and observed no change inthe spacing system this could indicate food was not important but that other unknownfactors were relevant These results probably would remain unpublished and further biasthe literature Until recently only a few papers made predictions or manipulated variables


and reported negative results however more papers reporting negative results now seemto appear in journals For example even in nectarivorous birds experiments do not alwaysfind that food determines territoriality Experimental studies of honeyeaters that examinedrelationships between territorial defense and nectar quantity and between nectar levels andintruder pressure did not find causal links between these variables (Armstrong 1992 [PE] McFarland 1994 [E]) Although behavior patterns changed territoriality did not dis-appear as a result of food manipulations Hofer and East (1993 [C]) also concluded foodwas not an important determinant of territoriality in spotted hyenas (Crocuta crocuta) attheir study site These data do not contradict reports that food acts as the controllingdeterminant in other circumstances They do not even show that food was unimportant inthese particular circumstances Rather they suggest that its importance sometimes is over-ridden by other variables Negative results may contain as much information as positiveresults and biologists are becoming more sophisticated at incorporating them into bodiesof knowledge (eg by evaluating their significance via power tests)

Less easily measured subcategories of food are studied less often (Table 1) Food qualityis difficult to assess especially in the field Even predictability can be hard to quantify whatcriteria does an animal use to gauge how predictable its food resources are Likewisewhereas food distribution can be manipulated to some extent it may be difficult to measuresince it can vary temporally andor spatially (Pielou 1969) A researcher first must deter-mine which scales are relevant to the study organisms (ie one might expect the relevantscale of distribution of food over space and time to be smaller for an herbivorous prong-horn Antilocapra americana than for a carnivorous coyote Canis latrans) then quantifyfood distribution over appropriate temporal and spatial scales

To understand better why populations are territorial future studies should examine fac-tors other than food including habitat features population density and predation pressureFor example Pyke (1979) proposed several models to explain sunbird territoriality relyingexclusively on measurements of calories available from food and calories and time spent invarious activities However his models did not include predation effects Certainly testingthe relevance of predation pressure will be difficult (Isbell and Young 1993) yet severalauthors predicted predation should affect spatial organization andor correlated predationwith expression of a spacing system (Case 1978 [P C] Myers 1980 [P C] Kavanagh 1981[C])

INTERRELATIONSHIPS OF ECOLOGICAL VARIABLES WITH SPECIES

We next explored relationships between studies of ecological variables and vertebratetaxa which included bony fish amphibians reptiles birds and mammals We present thedata in two forms by species (Tables 2ndash5) and summarized by class (Table 6) Just 26 ofpapers reported on ecological determinants of variable spacing systems in fish amphibiansand reptiles and 11 variables out of the 20 reported have become candidates for determin-ing territoriality in those groups However certain variables such as population densitypredation pressure habitat features space mates (including their density and distribution)and homeshelter sites can be applied broadly to many species

Population density and space were cited as determinants of territoriality in 31 of fishpapers perhaps partly because of the use of aquaria in fish research Manipulations gen-erally involved changing the size of aquaria (space) or adding or subtracting the total num-ber of fish in aquaria (population density) Researchers can seldom change experimentalconditions so easily with other vertebrates Population density was reported in just 7 ofbird papers Perhaps other density dependent factors operate to influence territoriality or


TABLE 2mdashEcological variables listed by species of fish Abbreviations used [P] 5 predicted relation-ship [C] 5 correlated relationship [E] 5 experimentally demonstrated relationship AS 5 assessibilityDE 5 density DS 5 distribution EA 5 energy availability HB 5 habitat features HN 5 host nestsMA 5 mates PD 5 predation pressure PO 5 population density PR 5 predictability QL 5 qualityQN 5 quantity RE 5 renewal rate RF 5 refuges homeshelter or spawning sites SP 5 space TY 5type

Species Reference Food Other

Oncorhyncus mykiss Newman 1956 [C] HBJenkins 1969 [E] QNCole and Noakes 1980 [C E] PO HB

Salmo trutta Kalleberg 1958 [C] HBJenkins 1969 [E] QN

Salmo salar Kalleberg 1958 [C] HBSalvelinus fontinalis Newman 1956 [C] HB

Grant and Noakes 1987 [C] TYBiro et al 1997 [C] HB

Plecoglossus altivelis Kawanabe 1969 [C] POBrachydanio (5Danio) rerio Grant and Kramer 1992 [P E] RE

Basquill and Grant 1998 [E] HBTheragra chalcogramma Ryer and Olla 1995 [E] DS SPOryzias latipes Magnuson 1962 [E] DS QN PO

Bryant and Grant 1995 [E] PRCyprinodon pecosensis Kodric-Brown 1988 [E] PO SPCyprinodon variegatus Itzkowitz 1977 [E] PO SPPoecilia reticulata Magurran and Seghers 1991 [E] POElassoma evergladeii Rubenstein 1981b [E] DS PR POLepomis cyanellus Greenberg 1947 [E] SPCichlasoma nigrofasciatum Grant and Guha 1993 [E] DS

Grand and Grant 1994 [E] PREtroplus maculatus Wyman and Hotaling 1988 [E] QNPelmatochromis subocellatus kribensis Wyman and Hotaling 1988 [E] QNDascyllus trimaculatus Fricke 1977 [C] QN RFPomacentrus albicaudatus Fricke 1977 [C] QN RFHalichoeres garnoti Robertson 1981 [C] RFThalassoma bifasciatum Fitch and Shapiro 1990 [C] TY HBXyrichtys splendens Nemtzov 1997 [C E] RF HBScarus croicensis Barlow 1975 [C] DS PR POScarus iserti Dubin 1981 [C] RFScarus taeniopterus Barlow 1975 [C] DS PR PO

Dubin 1981 [C] RFSparisoma aurofrenatum Barlow 1975 [C] DS PR PO

Dubin 1981 [C] RFSparisoma viride Barlow 1975 [C] DS PR PO

birds may choose other options when habitat is too crowded eg not breed disperse orstay and help raise breedersrsquo offspring (Brown 1987)

Mate distribution and mate density were considered in only one reptile paper (MrsquoCloskeyet al 1987 [E]) one fish paper (Grant 1997 [E]) and a few mammal papers (Liberg 1984[C] Ostfeld 1986 [P E] Ims 1987 [C] 1988 [E] Carranza et al 1995 [E] 1996 [C]Nelson 1995 [C E]) they were absent from bird and amphibian papers In mammals a


TABLE 3mdashEcological variables listed by species of amphibian and reptiles Abbreviations as shownin Table 2

Species Reference Food Resources Other

Plethodon vehiculum Ovaska 1988 [P] DS HBFamily Iguanidae Case 1978 [P C] PDAnolis aeneus Stamps 1973 [P] DS QNUrosaurus ornatus MrsquoCloskey et al 1987 [E] MASceloporus jarrovi Middendorf 1979 [P E] QN POSceloporus undulatus Ferguson et al 1983 [E] QNCtenosaura hemilopha Brattstrom 1974 [E] DSCtenosaura pectinata Evans 1951 [C] DSSauromalus obesus tumidus Prieto and Ryan 1978 [P C] QN PO

malersquos territory may overlap several femalesrsquo home ranges Some birds show a spatial dis-tribution similar to mammals however females generally settle in territories that malesalready have established Also for many birds the sex ratio is skewed little if at all Manymammals have a highly skewed sex ratio and a higher incidence of polygyny thus a malecan defend several female home ranges as his territory and gain exclusive access to them

Contrary to the limited treatment of mates as ecological determinants of territoriality inmuch of the literature Grant (1997) reported that fish defend mates and spawning sitesmore often than they defend food He suggested that spatial distribution of mates andspawning sites can be clumped in a smaller area during the relatively short reproductiveseason and this is more defensible than food which is more widely distributed and mustbe defended for more than one season

Some authors reported variables that appear important for a particular species (eg hostnest availability in brown headed cowbirds Molothrus ater Elliott 1980 [C] and spawningsites in coral reef fishes Dubin 1981 [C] Robertson 1981 [C]) These variables could beexamined in similar species to determine if they can be applied across taxa

EXTRACTING AND EVALUATING FINDINGS

NATURE OF THE EVIDENCE

Earlier we explained that depending on the type of data we assigned papers to one ofthree categories predicted correlated or experimentally demonstrated relationship In ourview any one interpretation of these data becomes less compelling as the number of likelyalternative interpretations increases Two major sources of alternative interpretations areunnoticed causes of correlations and phylogenetic inertia

Unnoticed causes of correlations are variables that determine territoriality but that theinvestigator does not record For example perhaps territoriality actually was determined byhigher population density but the observer recorded food quantity only and thus attributedincreased territoriality to increasing food levels This potential error is inherent in anydesign in which one variable is correlated with one or more other variables Such studiescannot discover if the correlation represents causality A spacing system probably is deter-mined by multiple factors with no one variable accounting for all the variance and perhapsnot even most of it Consequently when fewer variables are considered in a correlativestudy it is more likely that other unrecorded variables actually determine the spacing sys-tem

Unnoticed causes of correlation are less problematic in controlled experiments where


TABLE 4mdashEcological variables listed by species of birds Abbreviations as shown in Table 2


CLASS AVES Lott 1991 [P] HBMelanerpes formicivorus Hannon et al 1987 [C] QNCentrocercus urophasianus Gibson and Bradbury 1987 [C] HBArdea herodias Krebs 1974 [C] DS PRPorphyrio p melanotus Craig 1979 [C] QNSelasphorus rufus Kodric-Brown and Brown 1978 [C] QN

Gass and Lertzman 1980 [C] QNCalypte anna Ewald and Carpenter 1978 [E] EAFamily Anatidae Nudds and Ankney 1982 [C] PRFamily Scolopacidae Myers et al 1979b [C] DS PR RE PDTryngites subruficollis Myers 1980 [P C] DS PR PDCalidris alba Myers et al 1979a [C] QN DE

Myers et al 1981 [C] DS QN DEPluvialis squatarola Turpie 1995 [C] POCatoptrophorus semipalmatus McNeil and Rompre 1995 [C] TYCatharcta maccormicki Pietz 1987 [C] PRCatharcta lonnbergi Pietz 1987 [C] PRStercorarius spp Pitelka et al 1955 [C] TY

Andersson and Gotmark 1980 [C] TYOpisthocomus hoazin Strahl and Schmitz 1990 [C] HBCorvus spp Rowley 1973 [C] QNGarrulus glandarius Rolando et al 1995 [C] QN POAnthornis melanura Craig and Douglas 1986 [C] DSPhainopepla nitens Walsberg 1977 [C] QN PRParus atricapillus Smith and Van Buskirk 1988 [P] QN RF

Desrochers and Hannon 1989 [P C] DS QLNectarinia reichenowi Gill and Wolf 1975 [C E] QNVestiaria coccinea Carpenter and MacMillen 1976 [P

C E]QN

Carpenter 1987 [C E] QNPhylidonyris nigra Armstrong 1992 [P E] QNPhylidonyris novaehollandiae Armstrong 1992 [P E] QN

McFarland 1994 [E] QNMotacilla alba yarrelli Davies 1976 [C] DSMotacilla alba Davies and Houston 1983 [C] QNMotacilla alba alba Zahavi 1971 [E] DS QN PRPrunella modularis Davies and Hartley 1996 [E] DS PRTurdus migratorius Young 1956 [C] QNTurdus merula Snow 1956 [C] QNTurdus philomelos Davies and Snow 1965 [C] QNTurdus pilaris Tye 1986 [E] QN PR QL ASMyadestes townsendi Lederer 1981 [C] DSQNTiaris olivacea Pulliam et al 1972 [C] HBMolothrus ater Elliott 1980 [C] HN

Dufty 1982 [C] HNRothstein et al 1984 [C] POTeather and Robertson 1985 [P] HN


only one variable is manipulated The effects of such a variable can be seen separately andthe interpretation that the variable at least partly determined territoriality is not ambiguousFor example the failure of males to establish territories when Ims (1988 [E]) experimen-tally placed grey sided vole (Clethrionomys rufocanus) females in a clumped distributiondemonstrated that another variable perhaps higher intruder pressure was overriding re-source distribution Likewise when Nelson (1995 [C E]) found no relationship betweenfemale spatial distribution and territoriality in male field voles (Microtus agrestis) the effectof female density in producing more exclusive male home ranges apparently was confound-ed by the positive correlation between home range size and amount of overlap

Phylogenetic inertia is another alternative explanation of data Territorial behavior maybe seen in two groups of animals because of genes they share through descent from acommon ancestor rather than because of one or more shared features of their ecology(Alcock 1998) Furthermore territorial behavior may not be seen in two groups despitetheir sharing critical features of the ecology because they have inherited different geneticpredispositions (Alcock 1998) The possibility of phylogenetic inertia and other issues ofevolutionary vs ecological vs behavioral time scales and of fixed vs plastic responses oftencan be eliminated as explanations by studying animals that show intraspecific variation insocial systems Lott (1991) Shapiro (1991) and Warner (1991) discussed advantages ofintraspecific variation as a tool in behavioral ecology and those systems will generate thestrongest evidence of ecological determinants of territoriality We acknowledge that manyperhaps most species are not plastic enough for research on them to yield the most com-pelling data and accordingly recognize the value of interspecific comparison (Barlow1993) as the only feasible approach for many species At the same time we believe research-ers cannot achieve the same level of certainty about ecological determinants of territorialityin those species compared to more flexible species

Many studies we cite were designed to investigate the role of a particular ecological var-iable in the territoriality of a particular species in a particular situation In doing so authorsprovided evidence that many ecological variables act as determinants But if many differentvariables determine territoriality no one variable is likely to determine it every time andunrecorded variables will produce apparent contradictions Our first reaction to studies thatdid not agree about determinants was that one must be right and the other wrong and ifthe numbers of pro and con reports were similar perhaps the contradiction could not beresolved Certainly some papers provide weaker data than others do For example someof the older literature relies more heavily on a descriptive rather than a quantitative ap-proach (eg Snow 1956 [C] Young 1956 [C] Prior 1968 [C]) Furthermore whereas someauthors quantify ecological variables they do not quantify territorial behavior (eg Smith1968 [C] Prieto and Ryan 1978 [P C] Rothstein et al 1984 [C]) Even when variablesare quantified two authors rarely measure the same variables in the same way Despite theseproblems however most authors probably are correct about their findings Thus we regardnegative reports as supplementing rather than contradicting positive reports

Finally whereas many papers report on particular taxa we chose to try to synthesize theliterature by focusing on similarities across taxa Findings usually crossed taxonomic linessuggesting substantial similarities among disparate species

WHAT A REVIEW DETERMINANT BY DETERMINANT REVEALS

Whereas most authors implied or used the lsquolsquoeconomic modelrsquorsquo (Brown 1964 Stamps1994) which assumes individuals should exclude others from nonshareable resources iffitness benefits exceed costs we do not discuss the cost-benefit analyses that provide anadaptive justification for the predictions and correlations Many people have discussed this


TABLE 5mdashEcological variables listed by species of mammals Abbreviations as shown in Table 2


Didelphis virginiana Ryser 1995 [C] DS PR QLOryctolagus cuniculus Cowan and Bell 1986 [C] RFOrder Primates Mitani and Rodman 1978 [C] DS DSPropithecus verreauxi Richard 1974 [C] DS QNPapio ursinus Hamilton et al 1976 [C] DSPresbytis melalophos Bennett 1986 [C] DS QN PRCercopithecus aethiops tan-

talusKavanagh 1981 [C] QN PR PD

Marmota monax Ferron and Ouellet 1989 [C] POTamiasciurus spp Smith 1968 [C] QNMus musculus Davis 1958 [E] PO

Anderson 1961 [P C] DS QN HB SPPoole and Morgan 1976 [E] SP

Mus musculus Bronson 1979 [P] QN PR HBClethrionomys rufocanus Ims 1987 [C] DS PO MA

Ims 1988 [E] MANeotoma lepida latirostra Vaughan and Schwartz 1980 [C] DSMicrotus agrestis Nelson 1995 [C E] MA POMicrotus californicus Ostfeld 1986 [P E] DS QN RE MAProechimys semispinosus Adler et al 1997 [C] DS RE PR POUrsus americanus Rogers 1987 [P C] DS QN PR

Hellgren and Vaughan 1990 [C] DS PRMustela nivalis Lockie 1966 [C] POMeles meles Kruuk and Parish 1987 [C] QNTaxidea taxus Goodrich and Buskirk 1998 [C] DS QN PR POCerdocyon thous Brady 1979 cited in Moehlman

1989 [C]TY

Canis lupus Peterson 1979 [C] QNVulpes vulpes Kolb 1986 [P] HB

Tsukada 1997 [C] DSFamily Felidae Liberg and Sandell 1988 [P C] DS PR MAAcinonyx jubatus Caro and Collins 1986 [C] QNFelis rufus Bailey 1974 [P C] DS

Zezulak and Schwab 1979 [C] POFelis domesticus Liberg 1980 [C] PO

Liberg 1984 [C] DS MAKonecny 1987 [C] QN DS

Panthera tigris Sundquist 1981 [C] DS PROrder Artiodactyla Leuthold 1977 [C] POEquus caballus Rubenstein 1981a [C] DS QLEquus asinus Woodward 1979 [C] DS QN PRHippopotamus amphibius Karstad and Hudson 1986 [C] SPCervus elaphus Carranza et al 1990 [C] DS QN

Carranza et al 1995 [E] DS QN MACarranza et al 1996 [C] DS QN MA

Odocoileus hemionus Geist 1981 [C] DS QNOdocoileus h columbianus Miller 1974 [C] QNCapreolus capreolus Prior 1968 [C] QNDama dama Langbein and Thirgood 1989 [C] HB PO


TABLE 5mdashContinued


Gazella granti Walther 1977 [C] HBOreotragus oreotragus Jarman 1974 [C] HBKobus leche leche Lent 1969 [C] HBAepyceros melampus Warren 1974 [C] PO

Jarman 1979 [C] QN QL POAntilocapra americana Bromley 1977 [P] DS QN RE HB

Kitchen and OrsquoGara 1982 [C] DS QL PODeblinger and Alldredge 1989 [C] DSMaher 1994 [C] QN POByers 1997 [C] PO

rationale eg why it pays an animal to defend a resource at intermediate levels of abun-dance but not at high or low levels (eg Brown 1964 Wittenberger 1981 Krebs and Davies1993) Alternatively researchers could employ an Evolutionarily Stable Strategy or gametheoretical approach which emphasize fitness consequences of behavior to understand whyspacing systems vary Yet whereas many investigators have reported on ecological variablesaffecting a particular spacing system few (if any) authors have measured the fitness ofanimals under particular spacing systems This approach while rarely taken should proveprofitable even though measuring fitness has its own difficulties (Krebs and Davies 1993)

We chose to focus on determinants that are discussed most often or determinants forwhich the apparently contradictory evidence indicates a complex relationship that wouldmerit further analysis Unlike Grantrsquos (1993) review of fish we did not treat all resourcesas equivalent since some have different properties than others We designed the followingdiscussion to be browsed much like a table rather than read as text per se At the beginningof each of the longer sections we summarize the relevant studies we encourage readerswho want more details on that variable to read the section further We follow the summarywith a hypothesized relationship of the ecological variable to territoriality Whereas thesehypotheses fit most reports they are perhaps most useful as possibilities to be examined infuture research

Food quantitymdashTwelve papers (Young 1956 [C] Davies and Snow 1965 [C] Smith 1968[C] Zahavi 1971 [E] Rowley 1973 [C] Craig 1979 [C] Peterson 1979 [C] Myers et al1981 [C] Ferguson et al 1983 [E] Ostfeld 1986 [P E] Carpenter 1987 [C E] Ims 1987[C]) reported territoriality decreased as amount of food increased and two papers (Fricke1977 [C] Carpenter 1987 [C E]) reported that limited food increased territoriality How-ever four papers (Miller 1974 [C] Gill and Wolf 1975 [C E] Carpenter and MacMillen1976 [P C E] Carranza et al 1990 [C]) found that abundant food increased territorialitywhereas ten papers (Snow 1956 [C] Prior 1968 [C] Walsberg 1977 [C] Kodric-Brownand Brown 1978 [C] Gass and Lertzman 1980 [C] Lederer 1981 [C] Caro and Collins1986 [C] Hannon et al 1987 [C] Kruuk and Parish 1987 [C] Maher 1994 [C]) reportedthat limited food was associated with a lack of territoriality Davies and Houston (1983 [C])and Wyman and Hotaling (1988 [E]) reported both findings increased food producedterritoriality and further increases in food quantities terminated territoriality We also foundreports of both abundance and scarcity having no effect on territoriality (Armstrong 1992[P E] Hofer and East 1993 [C] McFarland 1994 [E]) We conclude the relationship of

12143(1)

TH

EA

ME

RIC

AN

MID

LA

ND

NA

TU

RA

LIST

TABLE 6mdashSummary of ecological variables reported for each taxon Numbers represent number of papers citing that variable within that class Numbersin parentheses are numbers of papers reporting on species in that class Abbreviations as given in Table 2

Variable

Class

Food

DS DE QN PR RE QL TY AS

Resources in general

DS QU QN PR PO PD HB SP MA RF HN EA

Osteichthyes (N5 26) 6 0 4 4 0 0 2 0 0 0 0 0 8 0 7 4 0 4 0 0

Amphibia (N 5 1) 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0Reptilia (N 5 8) 2 0 4 0 0 0 0 0 1 0 0 0 2 1 0 0 1 0 0 0Aves (N 5 43) 9 2 22 7 1 2 3 1 0 0 0 1 3 2 4 0 0 1 3 1Mammalia (N 5

57) 22 0 22 12 2 4 1 0 6 1 1 0 16 1 8 3 8 1 0 0


FIG 1mdashA Inverted U function of the relationship between food quantity and the net benefits ofterritoriality (solid line) and the relationship between territoriality and food quantity (dashed line) BAlternative U function of the relationship between food quantity and the net benefits of territoriality(solid line) possible with many studies From low to medium food levels increased amounts decreaseterritoriality (dashed line) but from medium to high quantities increased amounts increase territori-ality

food quantity to territoriality is not linear and contrary to Grantrsquos (1993) hypothesis foodis sometimes too abundant in nature for territories to be maintained

The relationship of food quantity to territoriality often is modeled as an inverted Ufunction (eg Brown 1964 [P] Gill and Wolf 1975 [C E] Carpenter and MacMillen 1976[P C E] Davies and Houston 1983 [C] Wyman and Hotaling 1988 [E] Grant 1993 Fig1A) This model proposes that when food quantities are very low costs of defending re-sources exceed the benefits because energy spent defending resources would be greaterthan energy gained andor because competitors are so rare that the small amount of re-sources lost to them does not justify defense The cost-benefit ratio shifts toward territorialityas the level of food increases and it eventually reaches a point at which territoriality is costeffective If food becomes very abundant territoriality ceases to be beneficial because theamount of food exceeds the intruders so competition ceases andor because competitorsare so numerous (perhaps measured as rate of intrusions per unit time) that excludingthem all would take more energy than defense of the resource warrants

Thus the relationship of territoriality to food quantity can be conceptualized as a simpledependent variablemdashindependent variable function Ideally the dependent variable wouldbe territorial behavior measured operationally in units such as latency to approach intrud-ers (see the last section) In practice the dependent variable has been the benefits minuscosts of territoriality plotted as a function of the level of the independent variable (foodquantity Gill and Wolf 1975 [C E] Davies and Houston 1983 [C] Wyman and Hotaling1988 [E]) This approach tests the hypothesis that behavior is optimal provided assumptionsabout cost-benefit calculations are correct Alternatively one can test the hypothesis thatthe cost-benefit calculations are correct provided one assumes behavior is optimal How-ever since behavior is recorded as changing only at the threshold points (the transitionbetween benefits exceeding costs and vice versa) territoriality can be plotted only as an off-on either-or function not as a quantity or matter of degree This limitation is compatiblewith the perspective that territoriality is not graded but rather an animal either is or isnot territorial (Fig 1A) The cost-benefit ratio plotted in an optimality approach has cometo serve as a surrogate for behavior eg Wyman and Hotaling (1988 [E]) label that y-axislsquolsquoTerritorial Tendencyrsquorsquo Food quantity data from these studies can be plotted on the in-verted U function Simply place one level of food quantity in the area where benefits of


territoriality exceed costs and place the other point where they do not By placing the valueat which the subject was territorial in the midrange of values and the other outside themidrange we have arranged the data to conform to the inverted U hypothesis

However we must acknowledge that our placement with respect to the horizontal axis israther arbitrary because amount of food often is quantified only at two points on an ordinalscale lsquolsquomorersquorsquo and lsquolsquolessrsquorsquo Since all but two studies were unidirectional (territoriality at onelevel and its absence at another) we also could have plotted nearly all the studies as amirror image With the studies thus arranged the function would be a U function (Fig1B) However given good theoretical reasons to expect an inverted U function and thetwo studies that reported that function (Davies and Houston 1983 [C] Wyman and Ho-taling 1988 [E]) the inverted U function is a useful hypothesis for the relationship betweenfood quantity and territoriality

Whereas using cost-benefit ratio as a dependent variable is valuable plotting behaviordirectly could reveal trends toward or away from defense and so reduce ambiguity Also byeliminating the requirement that behavior crosses a threshold between categories of spacingsystems we could benefit from studies that now get lsquolsquonegativersquorsquo results and go unreportedWe further discuss the importance of quantifying behavior in the last section

Food distributionmdashSome authors stated that clumped food distribution leads to territo-riality (Davies 1976 [C] Woodward 1979 [C] Vaughan and Schwartz 1980 [C] Lederer1981 [C]) but in other cases food was clumped or patchy yet animals were not territorial(Evans 1951 [C] Bailey 1974 [P C] Desrochers and Hannon 1989 [P C] Tsukada 1997[C]) Krebs (1974 [C]) found that more dispersed food produced territoriality

Only two studies experimentally manipulated food distribution alone Evenly distributedfood resulted in grouping whereas territorial behavior was observed when food was dis-tributed in piles (Zahavi 1971 [E]) Similarly when food was more spatially clumped ani-mals monopolized the resource more readily (Grant and Guha 1993 [E]) These obser-vations support correlational data that clumped food distribution leads to territoriality sug-gesting that unrecorded variables may have overridden the effect of distribution in somecorrelated studies

Craig and Douglas (1986 [C]) proposed a continuum to explain the correlation betweenfood distribution and spacing system at one end when resources were extremely clumpedanimals were organized in absolute social hierarchies due to higher costs of aggressionHigher intruder pressure made defense uneconomical Conversely when resources weremore spatially dispersed animals were more territorial and when food was concentrated insmall patches some animals could maintain exclusive access to that food The hypothesismost compatible with these data is an inverted U shaped model of the effect of food dis-tribution highly clumped or evenly distributed resources are not defended but moderatelyclumped resources are defended

Food predictabilitymdashFour papers (Walsberg 1977 [C] Woodward 1979 [C] Grand andGrant 1994 [E] Bryant and Grant 1995 [E]) reported that territoriality or resource mo-nopolization was correlated with a spatially or temporally predictable food base The hy-pothesis that best conforms to these data is a linear relationship between food predictabilityand net benefits of territoriality (Fig 2) However food caching species may behave contraryto this rule Tye (1986 [E]) demonstrated that temporally unpredictable food led to terri-toriality in fieldfares (Turdus pilaris) He suggested that territoriality was an adaptation bywhich these birds could store their food supplies (apples) against periods of scarcity

Food typemdashWhereas several authors discussed food type few discussed the same catego-ries in similar ways and all evidence was correlational When resources can be defended


FIG 2mdashRelationship between degree of spatial predictability of food and net benefits of territoriality(solid line) and relationship between territoriality and predictability (dashed line)

presumably due to characteristics such as quantity distribution or predictability animalsmaintain territories that include those food items

Brook charr (Salvelinus fontinalis) feeding on drift in fast water were territorial yet whenthey fed on benthic organisms in slow water they were not territorial (Grant and Noakes1987 [C]) Brady (1979 [C] cited in Moehlman 1989) observed that crab eating foxes(Cerdocyon thous) were territorial when eating crabs and vertebrates but they foraged inoverlapping home ranges when eating fruit and insects Pitelka et al (1955 [C]) and An-dersson and Gotmark (1980 [C]) reported that jaegers (Stercorarius spp) feeding on abun-dant lemmings were territorial but jaegers feeding on fish via kleptoparasitism were notThe lsquolsquovictimsrsquorsquo of kleptoparasitism could not be defended but a patch of ground with itsresident lemmings was defensible thus food type relates to underlying food distributionpatterns

Population densitymdashIn most empirical reports territoriality was more likely as populationdensity decreased (Davis 1958 [E] Zezulak and Schwab 1979 [C] Liberg 1980 [C] Ims1987 [C] Langbein and Thirgood 1989 [C] Nelson 1995 [C E] Adler et al 1997 [C])Lockie (1966 [C]) reported that moderate population density correlated with territorialitywhereas Ferron and Ouellet (1989 [C]) found that low and intermediate densities werecorrelated with territoriality

Davis (1958 [E]) Cole and Noakes (1980 [E]) and Magurran and Seghers (1991 [E])demonstrated that territoriality ceases at high density This relationship also was reportedby Kawanabe (1969 [C]) Prieto and Ryan (1978 [P C]) Jarman (1979 [C]) and Ferronand Ouellet (1989 [C]) The best experimental evidence is presented by Cole and Noakes(1980 [E]) and Magurran and Seghers (1991 [E]) They showed that when other things


are equal increased population density can end territoriality because of increased rates ofinteraction (intruder pressure)

A few studies reported apparently contradictory results Turpie (1995 [C]) reported thatterritoriality occurred when density exceeded a threshold value Lockie (1966 [C]) Kitchenand OrsquoGara (1982 [C]) Rothstein et al (1984 [C]) Maher (1994 [C]) and Byers (1997[C]) reported low density was not compatible with territoriality

These apparent contradictions have several possible explanations One possibility is thatthe terms lsquolsquohighrsquorsquo and lsquolsquolowrsquorsquo signify different things to different investigators Another pos-sibility is that population density accounts for little of the variance in degree of territorialityand unobserved variables actually determined the outcomes Yet another possible expla-nation is that densities used in laboratory settings were not representative of densities seenin natural circumstances Langbein and Thirgood (1989 [C]) admit to the somewhat arti-ficial nature of the parks in which they conducted studies on fallow deer (Dama dama) andCole and Noakes (1980 [E]) cite a lack of information about fish densities in the wild forcomparison with densities used in the laboratory Perhaps population density can be toolow to support territoriality due to low benefits as well as too high If we regard thesecontradictions as signal rather than noise they prove compatible with the hypothesis of aninverted U function The evidence for this hypothesis certainly is strong enough to justifysystematic testing

HabitatmdashStructural complexity and water current are two habitat features most com-monly asserted as determinants of territoriality Predictions about the effect of structuralcomplexity on territoriality are contradictory Bronson (1979 [P]) predicted lsquolsquoreasonablersquorsquostructural complexity will support territoriality as long as food is abundant and predictableWalther (1972 [C]) and Gibson and Bradbury (1987 [C]) agreed that complex habitatscorrelate with territoriality due to availability of landmarks by which animals can demarcateboundaries Kolb (1986 [P]) however predicted territoriality is more likely in a less struc-tured habitat because boundaries are easier to demarcate Although Kolb did not observeterritoriality in his study of red foxes (Vulpes vulpes) Basquill and Grant (1998 [E]) foundthat zebra fish (Danio rerio) were more aggressive and showed higher monopolization offood in a simple vs complex habitat Species differences could be important here in thatdifferent species rely on different types of marking to delineate boundaries (eg dung pilesor behavioral displays vs glandular secretions on vegetation) Structural complexity is likelyto affect important features of an individualrsquos biology such as predator avoidance and for-aging energetics Consequently it should be studied further and it may reveal the impor-tance of other determinants that covary with structural complexity such as population den-sity or food distribution

Several studies have examined the effect of water current on territoriality in stream fishesbut all these studies have been conducted on salmonids which feed on materials driftingfrom upstream Researchers have consistently found that such fish are more territorial inflowing water than in still water (Newman 1956 [C] Kalleberg 1958 [E] Cole and Noakes1980 [C] Biro et al 1997 [C])

SpacemdashReports of the effect of space availability are contradictory despite the high qual-ity of the evidence Anderson (1961 [P C]) Poole and Morgan (1976 [E]) Karstad andHudson (1986 [C]) Kodric-Brown (1988 [E]) and Strahl and Schmitz (1990 [C]) all re-ported that confinement reduces territoriality However Greenberg (1947 [E]) and Itzkow-itz (1977 [E]) demonstrated experimentally that decreasing space produced territorialityItzkowitz also found that increasing the amount of space increased the amount of territo-riality however responses also depended on presence or absence of females suggestingchanges in the cost-benefit ratio and therefore economic defensibility of space


Apparent contradictions in these experimental findings may be explained by the differentsized habitats used in the experiments Whereas Itzkowitz (1977 [E]) and Kodric-Brown(1988 [E]) both experimented with pupfishes (Cyprinodon spp) Itzkowitzrsquos manipulationsof space involved small tanks measuring 0072 m3 or 0036 m3 Kodric-Brown used muchlarger aquaria measuring 441 m3 and 109 m3 which mimicked wild habitats LikewiseGreenbergrsquos experiments with sunfish (Lepomis cyanellus) used small spaces the largest was0151 m3 Thus researchersrsquo lsquolsquolargersquorsquo spaces are not comparable to each other because onestudyrsquos lsquolsquolargersquorsquo space is another studyrsquos lsquolsquo(very) smallrsquorsquo space

Differing results could be consistent with an inverted U model of the effect of space onterritoriality moderate amounts of space support territoriality but because they are noteconomically defensible small and large amounts do not However no single study spansa broad enough range of space to produce both onset and termination of territorialityMoreover in the two pupfish studies the largest space in one study is smaller than thesmallest space in the other Consequently territoriality is reported at the highest and lowestlevels but it is eliminated when intermediate amounts of space are available This wouldplot as a U function Clearly this relationship needs systematic study

Determination by combinations of ecological variablesmdashMany authors predicted or reporteddata indicating that territoriality resulted from two or more variables acting in combinationIn the real world several determinants will usually perhaps always operate simultaneouslyWhereas we commend steps in this direction the methodology of these studies does notallow us to partition the contribution of each separate variable

The analysis would be more illuminating with a multiple regression technique Since thatapproach rarely has been used in territorial studies multideterminant studies offer consid-erable insight into the investigatorrsquos reasoning but not necessarily as much informationabout how territoriality is determined However a pattern may be revealed when severalstudies of multiple determinants have some but not all variables in common eg in studiescombining food predictability with another variable

Combinations of food variablesmdashAll authors who discussed food quantity and distributiontogether had consistent findings although most evidence was correlational Konecny (1987[C]) observed that limited but patchy food led to less exclusive home ranges ie moreterritoriality Carranza et al (1995 [E]) created patches of scarce food which allowed fe-males to concentrate in specific areas and males then established territories Other studiesalso found that when food was abundant and patchily distributed animals were not terri-torial (Magnuson 1962 [E] Richard 1974 [C] Rogers 1987 [P C])

Bronson (1979 [P]) predicted that if food was both abundant and predictable animalswould be territorial Kavanagh (1981 [C]) reported that limited but predictable food sourc-es were defended Both authors discussing food quantity and predictability agreed with eachother on the effects of predictability

One paper (Liberg and Sandell 1989 [P C]) predicted that the combination of predict-able evenly distributed food would lead to territoriality and two papers (Sundquist 1981[C] Hellgren and Vaughn 1990 [C]) reported this relationship Zahavi (1971 [E]) andKrebs (1974 [C]) described an allied finding that large unpredictable clumped food sourc-es precluded territoriality Davies and Hartley (1996 [E]) also found increased territoryoverlap (but territories were not abandoned) when food was patchy and unpredictableFinally Rubenstein (1981b [E]) demonstrated experimentally that predictable clumped dis-tributions of food produced territoriality

Predictability when combined with patchy food distribution may account for most of thevariance in the data This also may explain findings reported under food distribution alonefood predictability may have varied in those studies as well Predictability might be especially


powerful in behaviorally flexible species since it could operate via learning and unpredict-ability might produce extinction

Only two papers attempted to address the combination of food distribution quantity andpredictability Rogers (1987 [P C]) reported that if abundant and patchy food was unpre-dictable it would lead to increased home range overlap terminating territoriality Bennett(1986 [C]) reported the related finding that when food was abundant and evenly distrib-uted but unpredictable animals were not territorial The difference between the studies isfood predictability again suggesting it may be more important as a determinant than othervariables

Combinations of population density and other variablesmdashRolando et al (1995 [C]) re-ported that high food quantity and population density did not produce territoriality andMiddendorf (1979 [P E]) demonstrated that at high population density even with supple-mental food animals were not territorial but at intermediate population densities someanimals were territorial He concluded population density was a more important determi-nant of spatial organization than was food quantity

When food was clumped males maintained exclusive areas regardless of population den-sity However when food was randomly distributed in space males at high and low densitiesdid not maintain territories Only males exposed to intermediate population densities con-tinued to maintain territories (Rubenstein 1981b [E]) This lends support to the hypothesisthat the relationship between population density and territoriality is not linear

Two papers investigated the combination of population density and amount of space Insmall areas with low population densities animals were not territorial but they switched toterritoriality when density was high because of increased competition for breeding sites(Kodric-Brown 1988 [E]) Itzkowitz (1977 [E]) also found that in larger areas as densityincreased territoriality increased He concluded that total area was just as important indetermining spatial organization as was population density

Mate distribution and abundancemdashA pattern of abundant evenly distributed females waspredicted to lead to male territoriality (Liberg and Sandell 1988 [P C]) Liberg (1984 [C])reported that a less concentrated and predictable female distribution correlated with partialterritoriality in males males could not exclude all competitors However Ims (1987 [C])reported that clumped and abundant (because of synchronous breeding) females alongwith low male density promoted male territoriality Carranza et al (1996 [C]) reportedsimilar findings Yet Nelson (1995 [C E]) found that the pattern of female distribution inspace had no effect on territoriality in males Although males were more territorial at higherdensities of females after he corrected for the relationship between home range size andexclusivity he found that mate density did not affect territoriality directly

SUMMARY OF THE FINDINGS

The foregoing review demonstrates that territoriality can be affected by many differentecological variables The review also shows that the more times a single variable eg foodquantity has been tested as a determinant of territoriality the more likely apparently con-tradictory studies occur in the literature However many of these apparent contradictionsappear to be resolvable

Only food predictability is linearly correlated with territoriality the relationship betweenseveral other variables and territoriality appears to have an inverted U shape This patternalready has been proposed for food quantity ie very abundant food and very scarce foodwould not be defended but intermediate levels would be defended (Gill and Wolf 1975[C E] Carpenter and MacMillen 1976 [P C E] Wyman and Hotaling 1988 [E]) and thesame model can be applied to other variables such as population density or food distribu-


tion Grantrsquos (1993) analysis of fish studies concluded that resource density theoreticallyhas an inverted U effect on territoriality but he suggested the upper threshold will seldomif ever be reached in nature Our review of all instances of intraspecific variation in allvertebrate classes suggests that results from studies of food quantity food distribution pop-ulation density and perhaps spatial variation strongly hint that an upper threshold frequent-ly is reached Like Grant (1993) we note that the variable with the most consistent effectmdashpredictabilitymdashseems unlikely to be subject to nonlinear effects We caution that weaklyquantified data readily can be molded to the reviewerrsquos model and in analyses of a multi-determined phenomenon like territoriality the influence of any single studied variable maybe overridden by the influence of one or more unrecorded variables Consequently somereported effects eg of food quantity on territoriality may fit our hypothesized inverted Ufunction because they can be placed somewhat arbitrarily Still we conclude that the evi-dence strongly suggests that an inverted U function explains much of the data

CAUSAL PATHWAYS

Most reports assert that the ecological variable induces territoriality directly rather thanindirectly by altering an intervening variable that then acts as a determinant However insome cases authors propose a two or more step process or causal pathway Most causalpathways we report were described in empirical papers but the pathways themselves werenot examined in the study Rather they were post hoc explanations of the observationsPath analysis provides a method for testing hypotheses about causal pathways (Mitchell1993) We are not aware however that it has been employed in studies of ecological de-terminants of territoriality Although the validity of the proposed pathways cannot be eval-uated they may offer a useful starting point in the search for proximate mechanisms bywhich ecological variables determine territoriality Therefore we summarize them below

Intruder pressure was the most frequently proposed intervening variable The patternfor its operation was that a change in quantity of some resource would alter intruder pres-sure in a way that facilitated territoriality Desrochers and Hannon (1989 [P C]) suggestedthat clumped distribution of high quality food would increase intruder pressure and terri-toriality would decrease in response to increased intruder pressure Several authors pro-posed that increased quantity or density of food would decrease territoriality in the sameway (Young 1956 [C] Davies and Snow 1965 [C] Rowley 1973 [C] Craig 1979 [C] Myerset al 1979a [C] 1981 [C]) and Davies and Houston (1983 [C]) attributed acceptance ofsatellites into territories as a response to higher intruder pressure created by increased foodIms (1987 [C]) proposed a similar pathway with mates as the resource spatially clumpedfemales induce reproductive synchrony among themselves which then reduces male densityand intruder pressure and enhances territoriality among males

This view conflicts somewhat with the proposal that scarce (rather than abundant) foodincreases intruder pressure and so decreases territoriality (Ewald and Carpenter 1978 [E]Kodric-Brown and Brown 1978 [C] Tye 1986 [E]) Moreover Ewald and Carpenter (1978[E]) demonstrated experimentally that increased intruder pressure (attributed to less food)reduced territoriality In contrast Tye (1986 [E]) demonstrated that smaller amounts offood increased intruder pressure and led to territoriality in his view this pattern of foodavailability created a smaller area from which to exclude competitors compared to areascontaining larger amounts of food A U shaped model of the relationship between foodquantity and territoriality again could accommodate these apparent contradictions Fur-thermore the spatial scale over which food increases will be important Resources concen-trated over a larger regional area may attract more intruders than those distributed in asmaller local area (Carpenter 1987 [C E])


Rubenstein (1981a [C]) proposed female group stability as an intervening variable lead-ing to a spacing system He suggested foraging conditions that precluded permanent groupsof females (low quality widely scattered patchy vegetation) would support male territorialitybecause males could not defend those females whereas conditions supporting stable femalegroups (larger more evenly distributed patches of high quality food) would not produceterritoriality among males males would defend groups of females and move freely withthem rather than defend a fixed location

Mate dispersion also was proposed as an intervening variable Langbein and Thirgood(1989 [C]) suggested open habitat decreased male territoriality because it led to greaterfemale cohesion making defense of female groups more feasible whereas Cowan and Bell(1986 [C]) suggested burrow availability could produce male territoriality by causing fe-males to group Low amounts of food can lead to fewer numbers of females in an areacausing males to abandon territories (Caro and Collins 1986 [C]) Similarly higher foodproductivity or patchy distribution of food could attract females to areas then males estab-lish territories there (Carranza et al 1990 [C] 1996 [C]) Few studies have attempted todemonstrate this relationship experimentally but addition of supplemental food inducedfemales to aggregate in particular areas which males then defended as territories (Carranzaet al 1995 [E])

THE FUTURE ADDITIONAL METHODS FOR STUDYING ECOLOGICAL DETERMINANTS OF

TERRITORIALITY

Our review suggests that progress can proceed more rapidly by increased use of threetools (1) quantification of ecological variables (2) quantification of social systems (viaquantification of behavior) and (3) use of multiple regression and path analysis to explorethe relationship of these two sets of variables The first and third tools are established andwe discuss them only briefly Quantification of social systems however is not well developedso we discuss it further

Researchers have perfected measurement and manipulation of many ecological variableseg we can precisely determine plant or prey density and chemical composition Foodquantity is perhaps the most frequently quantified variable Gill and Wolf (1975) and Lottand Lott (1992) measured ml of nectar in flowers the food resource for sunbirds Myers etal (1979a) quantified both density of invertebrates that territorial sanderlings (Calidrisalba) ate and intruder density Kitchen (1974) quantified food quantity by measuring freshand dry weights available to pronghorns Water velocity has been quantified in studies ofstream fishes (Grant and Noakes 1987 Lott and North 1998)

The way experiments are performed ie on a regional or local scale affects results andthe possibility of a shift in the observed spacing system (Carpenter 1987 Armstrong 1992)Manipulations should be performed over relevant time periods and in dimensions appro-priate to the species Indeed negative results could be an artifact of a limited time scalemost studies are conducted over a period of days or weeks Furthermore the entire regionrelative to localized feeding areas may need to be considered as in the case of nectarivorousbirds (Carpenter 1987)

Multiple regression techniques also are well established Several studies of territorialityused multivariate procedures (multivariate analysis of variance Cole and Noakes 1980factor analysis Ims 1987 discriminant analysis Langbein and Thirgood 1989 Middendorf1979 multiple regression and partial correlation Myers et al 1981) Of the available tech-niques multiple regression is often best suited for explaining the determination of one ora few dependent variables (eg the amount of one or a few indices of territoriality) by thecombined effect of several independent variables (Kerlinger and Pedhazur 1973) Multiple


regression techniques may give the field worker a level of rigor in analysis comparable tothat achieved in laboratory experiments without losing the complexity of the natural envi-ronment (Brown et al 1978 Ims 1987 Langbein and Thirgood 1989) plus they cancalculate the amount of variation accounted for by each variable and the direction of itseffects (Draper and Smith 1981 Ludwig and Reynolds 1988 Phillipi 1993)

To adopt a multiple regression approach one must identify several variables to measureclearly define those variables and measure them quantitatively These measurements couldbe conducted for territorial and nonterritorial individuals for territorial and nonterritorialpopulations or for members of the same population at different times such as before andafter an experimental manipulation Our search of the literature yielded 20 ecological var-iables that at least sometimes act as determinants (Table 1) This listing is probably notexhaustive but it presumably includes most of the important determinants Therefore itprovides a good starting point for investigators seeking likely candidates Our tabulation ofthe variables examined in different taxa also can provide help in searching for variableslikely to operate in a particular taxon (Tables 2ndash6)

Since most ecological variables (eg food quantity population density) are probably notrelated linearly to territoriality they would not meet the linearity assumption of multipleregression However variables can be transformed eg logistically or as quadratic termsso the relationship is linear (Ludwig and Reynolds 1988)

TOWARD A QUANTIFICATION OF TERRITORIAL BEHAVIOR

Researchers have not developed methods to quantify social systems to the same degreethat they have developed methodology to quantify ecological variables Yet recently severalinvestigators have used different behavioral characteristics to quantify territorial behaviorpatterns For example Pyke et al (1996) urged that the spacing system we call territorialitybe defined as a complex of several quantified behavioral attributes including (1) intensityof territorial behavior (2) sharpness of territorial boundary and (3) exclusivity of resourceuse Pyke et al chose these variables as particularly suitable for studies of territoriality inhoneyeaters and they would use the resulting quantitative summary to classify the spacingsystem as territorial or not territorial In a field experiment on another nectarivore thebronzy sunbird (Nectarinia kilimensis) Lott and Lott (1992) chose a different set of vari-ables (1) percent time absent (2) unchallenged intruders per hour present (3) challengedintruders per hour present and (4) latency to displacement of challenged intruders Wymanand Hotaling (1988) studying cichlid fishes (Etroplus maculatus and Pelmatochromis subo-cellatus kribensis) recorded (1) charges (2) rams (3) territories defended and (4) lateraldisplays Lott and North (1998) measured (1) site specificity of aggression (2) site fidelityand (3) exclusivity of space use in rainbow trout (Oncorhyncus mykiss) The several quan-tities generated by such an approach can be arithmetically summarized into a single value(see Lott and North 1998) This value then can represent the aggregate degree of territo-riality and can be plotted as a function of food quantity or other relevant variable Thiswould test directly the predictive power of optimality hypotheses

Such measures also allow us to examine our preconceptions about territoriality For ex-ample do all measures always have the same relationship to one another thus suggestingthat territoriality always takes the same form Perhaps animals actually pursue a set of some-what independent strategies eg remaining site faithful under many circumstances butonly challenging intruders under some of them only threatening under some circumstanc-es and both threatening and attacking under others or maintaining sharp boundaries un-der some circumstances and only threatening whereas maintaining soft boundaries under


other circumstances but both threatening and attacking Such analyses offer the possibilityof greater insight into spatial strategies

A quantified description of territoriality also can be related to a quantified alternativesocial system Bromley (1977) measured the degree to which the outcome of a dominanceinteraction is a function of the location where it occurs Lott and North (1998) developeda method for quantitatively describing the degree to which (1) a spatial strategy (territori-ality) and (2) a relational strategy (dominance) may contribute to a single social systemvalue They discovered that individuals could not be placed into discrete categories of dom-inance and territoriality instead individuals displayed components of both types of socialsystems By quantifying behavior patterns and assigning numerical scores to individuals Lottand North detected more subtle differences in individual behavior and social organizationas ecological conditions changed Minta (1990) has taken this approach a step further bycreating a three dimensional model that allows a quantitative summary of the joint contri-bution of territoriality dominance and temporal avoidance strategies to a three dimensional(three strategy) social system

Treating territoriality and (or) its behavioral components as quantities also would allowus to benefit more from studies currently regarded as yielding negative results A changein food quantity may cause a shift along a continuum of spatial behavior in one directionor the other (eg toward completely overlapping home ranges or toward exclusive homeranges) however the change may not be great enough to change the category to whichthe social organization is assigned ie to undefended home range or to territory

Different quantitative indices of territoriality could be used as separate behavioral indicesof territoriality in a multivariate procedure (eg Ims [1987] used factor analysis to cate-gorize behavior in animalsrsquo own home ranges and in home ranges of other individuals)They also could be combined into a single index to be regressed against a set of ecologicalvariables

We noted earlier that several authors hypothesized causal pathways by which ecologicalvariable A determines ecological variable B which in turn determines the degree of ter-ritoriality Verbal models of such hypotheses are not testable but path analysis (Mitchell1993) provides a quantitative statistical method for modeling such hypotheses and rigor-ously testing them Consequently it provides a useful means to understand how ecologicalvariables determine territoriality Path analysis has weaknesses similar to multiple regressioneg effects of the variables should be linear and all important variables should be identified(Mitchell 1993) and this method works best when variables are manipulated experimen-tally (Smith et al 1997)

Stephens and Dunbar (1993) have applied another technique dimensional analysis tothe question of territory size and their model illustrates the potential power of this ap-proach in behavioral ecology As currently developed the model only predicts whether ornot an animal should be territorial as a function of the size of the space available to defendand it treats territoriality as a categorical variable (ie animals are either territorial or theyare not) rather than a quantitative one Consequently its use in answering the questionswe raise is not yet clear However dimensional analysis clearly facilitates comparisons andquantitative analysis of ecological variables

Thus far the study of ecological determinants of territoriality has been conceptually richbut not always rigorous enough to draw robust conclusions Future progress in our under-standing not only of which determinants influence territoriality but how they influencebehavior patterns at a proximate level could be accelerated by quantifying both the inde-pendent (ecological) variables and the dependent (behavioral) variables and by makingmore use of multivariate techniques


AcknowledgmentsmdashWe thank G Barlow R Bowen M Daly J W A Grant D Hu L Isbell B JakobS Minta C Pennuto N Solomon J Stamps D Van Vuren and three anonymous reviewers for thetime and effort they spent reviewing earlier versions of this manuscript This research was partiallysupported by the Department of Wildlife and Fisheries Biology Hatch Fund No 3915 and the Universityof Southern Maine

LITERATURE CITED

ADLER G H M ENDRIES AND S PIOTTER 1997 Spacing patterns within populations of a tropical forestrodent Proechimys semispinosus on five Panamanian islands J Zool (Lond) 24143ndash53

ALCOCK J 1998 Animal behavior an evolutionary approach 6th ed Sinauer Associates Inc Sunder-land Massachusetts 640 p

ANDERSON P K 1961 Density social structure and nonsocial environment in house-mouse populationsand the implication for regulation of numbers Trans NY Acad Sci 23447ndash451

ANDERSSON M AND F GOTMARK 1980 Social organization and foraging ecology in the Arctic skuaStercorarius parasiticus a test of the food defendability hypothesis Oikos 3563ndash71

ARMSTRONG P 1992 Correlation between nectar supply and aggression in territorial honeyeaters cau-sation or coincidence Behav Ecol Sociobiol 3095ndash102

BAILEY T N 1974 Social organization in a bobcat population J Wildl Manage 38435ndash446BARLOW G W 1975 On the sociobiology of four Puerto Rican parrotfishes (Scaridae) Mar Biol 33

281ndash293 1993 Fish behavioral ecology pros cons and opportunities Mar Behav Physiol 237ndash27

BASQUILL S P AND J W A GRANT 1998 An increase in habitat complexity reduces aggression andmonopolization of food by zebra fish (Danio rerio) Can J Zool 76770ndash772

BENNETT E L 1986 Environmental correlates of ranging behaviour in the banded langur Presbytismelalophos Folia primatol 4726ndash38

BIRO P A M S RIDGWAY AND D L G NOAKES 1997 The central-place territorial model does notapply to space-use by juvenile brook charr Salvelinus fontinalis in lakes J Anim Ecol 66837ndash845

BRATTSTROM B H 1974 The evolution of reptilian social behavior Am Zool 1435ndash49BROMLEY P T 1977 Aspects of the behavioural ecology and sociobiology of the pronghorn (Antilocapra

americana) PhD Dissertation University of Calgary Calgary 370 pBRONSON F H 1979 The reproductive ecology of the house mouse Quart Rev Biol 54265ndash299BROWN J L 1964 The evolution of diversity in avian territorial systems Wilson Bull 76160ndash169

1987 Helping and communal breeding in birds Princeton University Press Princeton 354 p D D DOW E R BROWN AND S D BROWN 1978 Effects of helpers on feeding of nestlings in

the grey-crowned babbler (Pomatostomus temporalis) Behav Ecol Sociobiol 443ndash59BRYANT M J AND J W A GRANT 1995 Resource defence monopolization and variation of fitness in

groups of female Japanese medaka depend on the synchrony of food arrival Anim Behav491469ndash1479

BYERS J A 1997 American pronghorn social adaptations and the ghosts of predators past Universityof Chicago Press Chicago 300 p

CARO T M AND D A COLLINS 1986 Male cheetahs of the Serengeti Natl Geogr Res 275ndash86CARPENTER F L 1987 Food abundance and territoriality to defend or not to defend Am Zool 27

387ndash399AND R E MACMILLEN 1976 Threshold model of feeding territoriality and test with a Hawaiianhoneycreeper Science 194639ndash642

CARRANZA J F ALVAREZ AND T REDONDO 1990 Territoriality as a mating strategy in red deer AnimBehav 4079ndash88

P FERNANDEZ-LLARIO AND M GOMENDIO 1996 Correlates of territoriality in rutting red deerEthology 102793ndash805

A J GARCIA-MUNOZ AND J DE DIOS VARGAS 1995 Experimental shifting from harem defenceto territoriality in rutting red deer Anim Behav 49551ndash554


CASE T J 1978 A general explanation for insular body size trends in terrestrial vertebrates Ecology591ndash18

CLUTTON-BROCK T H D GREEN M HIRAIWA-HASEGAWA AND S D ALBON 1988 Passing the buckresource defense lek breeding and mate choice Behav Ecol Sociobiol 23281ndash296

COLE K S AND D L G NOAKES 1980 Development of early social behaviour of rainbow trout Salmogairdneri (Pisces Salmonidae) Behav Proc 597ndash112

COWAN D P AND D J BELL 1986 Leporid social behaviour and social organization Mamm Rev 16169ndash179

CRAIG J L 1979 Habitat variation in the social organization of a communal gallinule the pukekoPorphyrio porphyrio melanotus Behav Ecol Sociobiol 5331ndash358

AND M E DOUGLAS 1986 Resource distribution aggressive asymmetries and variable access toresources in the nectar feeding bellbird Behav Ecol Sociobiol 18231ndash240

CSADA R D P C JAMES AND R H M ESPIE 1996 The lsquolsquofile drawer problemrsquorsquo of non-significantresults does it apply to biological research Oikos 76591ndash593

DAVIES N B 1976 Food flocking and territorial behavior of the pied wagtail (Motacilla alba yarrelliGould) in winter J Anim Ecol 45235ndash254

AND I R HARTLEY 1996 Food patchiness territory overlap and social systems an experimentwith dunnocks Prunella modularis J Anim Ecol 65837ndash846

AND A I HOUSTON 1983 Time allocation between territories and flocks and ownersmdashsatelliteconflict in foraging pied wagtails Motacilla alba J Anim Ecol 52621ndash634

DAVIES P W AND D W SNOW 1965 Territory and food of the song thrush Brit Birds 58161ndash175DAVIS D E 1958 The role of density in aggressive behavior of house mice Anim Behav 6207ndash210DEBLINGER R D AND A W ALLDREDGE 1989 Management implications of variations in pronghorn

social behavior Wildl Soc Bull 1782ndash87DESROCHERS A AND S J HANNON 1989 Site-related dominance and spacing among winter flocks of

black-capped chickadees Condor 91317ndash323DRAPER N R AND H SMITH 1981 Applied regression analysis 2nd ed John Wiley and Sons Inc

New York 709 pDUBIN R E 1981 Social behaviour and ecology of some Caribbean parrotfish (Scaridae) PhD Dis-

sertation University of Alberta Edmonton 336 pDUFTY A M JR 1982 Response of brown-headed cowbirds to simulated conspecific intruders Anim

Behav 301043ndash1052ELLIOTT P F 1980 Evolution of promiscuity in the brown-headed cowbird Condor 82138ndash141EVANS L T 1951 Field study of the social behavior of the black lizard Ctenosaura pectinata Am

Museum Novitates 14931ndash26EWALD P W AND F L CARPENTER 1978 Territorial responses to energy manipulations in the Anna

hummingbird Oecologia 31277ndash292FERGUSON G W J L HUGHES AND K L BROWN 1983 Food availability and territorial establishment

of juvenile Sceloporus undulatus p 134ndash148 In P B Huey E R Pianka and T W Schoener(eds) Lizard ecology Harvard University Press Cambridge

FERRON J AND J P OUELLET 1989 Temporal and intersexual variations in the use of space with regardto social organization in the woodchuck (Marmota monax) Can J Zool 671642ndash1649

FITCH W T S AND D Y SHAPIRO 1990 Spatial dispersion and nonmigratory spawning in the blueheadwrasse (Thalassoma bifasciatum) Ethology 85199ndash211

FRICKE H W 1977 Community structure social organization and ecological requirements of coralreef fish (Pomacentridae) Helgolander wiss Meeresunters 30412ndash426

GASS C L AND K P LERTZMAN 1980 Capricious mountain weather a driving variable in hummingbirdterritorial dynamics Can J Zool 581964ndash1968

GEIST V 1981 Behavior adaptive strategies in mule deer p 157ndash222 In O C Wallmo (ed) Muleand black-tailed deer of North America University of Nebraska Press Lincoln

GIBSON R M AND J W BRADBURY 1987 Lek organization in sage grouse variations on a territorialtheme Auk 10477ndash84


GILL F B AND L L WOLF 1975 Economics of feeding territoriality in the golden-winged sunbirdEcology 56333ndash345

GOODRICH J M AND S W BUSKIRK 1998 Spacing and ecology of North American badgers (Taxideataxus) in a prairie dog (Cynomys leucurus) complex J Mammal 79171ndash179

GRAND T C AND J W A GRANT 1994 Spatial predictability of food influences its monopolizationand defence by juvenile convict cichlids Anim Behav 4791ndash100

GRANT J W A 1993 Whether or not to defend The influence of resource distribution Mar BehavPhysiol 23137ndash153

1997 Territoriality p 81ndash103 In J-G J Godin (ed) Behavioural ecology of teleost fishesOxford University Press Oxford

AND R T GUHA 1993 Spatial clumping of food increases its monopolization and defense byconvict cichlids Cichlasoma nigrofasciatum Behav Ecol 4293ndash296

AND D L KRAMER 1992 Temporal clumping of food arrival reduces its monopolization anddefence by zebrafish Brachydanio rerio Anim Behav 44101ndash110

AND D L G NOAKES 1987 Movers and stayers foraging tactics of young of the year brookcharr Salvelinus fontinalis J Anim Ecol 561001ndash1013

GREENBERG B 1947 Some relations between territory social hierarchy and leadership in the greensunfish (Lepomis cyanellus) Physiol Zool 20267ndash299

HAMILTON W J III R E BUSKIRK AND W H BUSKIRK 1976 Defense of space and resources by chacma(Papio ursinus) baboon troops in an African desert swamp Ecology 571264ndash1272

HANNON S J R L MUMME W D KOENIG S SPON AND F A PITELKA 1987 Poor acorn crop dom-inance and decline in numbers of acorn woodpeckers J Anim Ecol 56197ndash207

HELLGREN E AND M VAUGHAN 1990 Range dynamics of black bears in Great Dismal Swamp Virginia-North Carolina Proc Annu Conf Southeast Assoc Fish Wildl Agenc 44268ndash278

HOFER H AND M L EAST 1993 The commuting system of Serengeti spotted hyaenas how a predatorcopes with migratory prey I Social organization Anim Behav 46547ndash557

IMS R A 1987 Responses in spatial organization and behaviour to manipulations of the food resourcein the vole Clethrionomys rufocanus J Anim Ecol 56585ndash596

1988 Spatial clumping of sexually receptive females induces space sharing among male volesNature 335541ndash543

ISBELL L A AND T P YOUNG 1993 Human presence reduces predation in a free-ranging vervetmonkey population in Kenya Anim Behav 451233ndash1235

ITZKOWITZ M 1977 Interrelationships of dominance and territorial behaviour in the pupfish Cypri-nodon variegatus Behav Proc 2383ndash391

JARMAN M V 1979 Impala social behaviour territory hierarchy mating and the use of space AdvEthol 211ndash92

JARMAN P J 1974 The social organisation of antelope in relation to their ecology Behaviour 48215ndash266

JENKINS T M JR 1969 Social structure position choice and microdistribution of two trout species(Salmo trutta and Salmo gairdneri) resident in mountain streams Anim Behav Monogr 21ndash123

KALLEBERG H 1958 Observations in a stream tank of territoriality and competition in juvenile salmonand trout (Salmo salar L and S trutta L) Rep Inst Freshw Res 3955ndash98

KARSTAD E AND R J HUDSON 1986 Social organization and communication of riverine hippopotamiin southwestern Kenya Mammalia 50153ndash164

KAVANAGH M 1981 Variable territoriality among tantalus monkeys in Cameroon Folia primatol 3676ndash98

KAWANABE H 1969 The significance of social structure in production of the lsquolsquoayursquorsquo Plecoglossus altiv-elis p 243ndash251 In T G Northcote (ed) Symposium on salmon and trout in streams Van-couver 1969 University of British Columbia Vancouver

KERLINGER F N AND E J PEDHAZUR 1973 Multiple regression in behavioral research Holt Rinehartand Winston New York 534 p

KITCHEN D W 1974 Behavior and ecology of the pronghorn Wildl Monogr 381ndash96


AND B W OrsquoGARA 1982 Pronghorn p 960ndash971 In J A Chapman and G A Feldhamer(eds) Wild mammals of North America biology management and economics Johns HopkinsUniversity Press Baltimore

KODRIC-BROWN A 1988 Effect of population density size of habitat and oviposition substrate on thebreeding system of pupfish (Cyprinodon pecosensis) Ethology 7728ndash43

AND J H BROWN 1978 Influence of economics interspecific competition and sexual dimor-phism on territoriality of migrant rufous hummingbirds Ecology 59285ndash296

KOLB H H 1986 Some observations on the home ranges of vixens (Vulpes vulpes) in the suburbs ofEdinburgh J Zool 210636ndash639

KONECNY M J 1987 Home range and activity patterns of feral house cats in the Galapagos islandsOikos 5617ndash23

KREBS J R 1974 Colonial nesting and social feeding strategies for exploiting food resources in thegreat blue heron (Ardea herodias) Behaviour 6199ndash131

AND N B DAVIES 1993 An introduction to behavioural ecology 3rd ed Sinauer AssociatesInc Sunderland 420 p

KRUUK H H AND T PARISH 1987 Changes in the size of groups and ranges of the European badger(Meles meles L) in an area in Scotland J Anim Ecol 56351ndash364

LANGBEIN J AND S J THIRGOOD 1989 Variation in mating systems of fallow deer (Dama dama) inrelation to ecology Ethology 83195ndash214

LEDERER R J 1981 Facultative territoriality in Townsendrsquos solitaire (Myadestes townsendi) SouthwestNat 25461ndash467

LENT P C 1969 A preliminary study of the Okavango lechwe (Kobus leche leche Gray) E Afr WildlJ 7147ndash157

LEUTHOLD W 1977 African ungulates a comparative review of their ethology and behavioral ecologySpringer Verlag Berlin 307 p

LIBERG O 1980 Spacing patterns in a population of rural free roaming domestic cats Oikos 35336ndash349

1984 Home range and territoriality in free ranging house cats Acta Zool Fennica 171283ndash285

AND M SANDELL 1988 Spatial organisation and reproductive tactics in the domestic cat andother felids p 83ndash98 In D C Turner and P Bateson (eds) The domestic cat the biologyof its behaviour Cambridge University Press Cambridge

LOCKIE J D 1966 Territory in small carnivores Symp Zool Soc Lond 18143ndash165LOTT D F 1991 Intraspecific variation in the social systems of wild vertebrates Cambridge University

Press Cambridge 238 pAND D Y LOTT 1992 Bronzy sunbirds Nectarinia kilimensis relax territoriality in response tointernal changes Ornis Scand 22303ndash307

AND G J NORTH 1998 A technique for quantitative description of aggression-produced socialsystems Ethology 104399ndash406

LUDWIG J A AND J F REYNOLDS 1988 Statistical ecology a primer on methods and computing JohnWiley and Sons New York 337 p

MACDONALD D W AND G M CARR 1989 Food security and the rewards of tolerance p 75ndash99 InV Standen and R A Foley (eds) Comparative socioecology Blackwell Scientific PublicationsOxford

MAGNUSON J J 1962 An analysis of aggressive behavior growth and competition for food and spacein medaka (Oryzias latipes (Pisces Cyprinodontidae)) Can J Zool 40313ndash363

MAGURRAN A E AND B H SEGHERS 1991 Variation in schooling and aggression amongst guppy(Poecilia reticulata) populations in Trinidad Behaviour 118214ndash234

MAHER C R 1994 Pronghorn male spatial organization population differences in degree of nonter-ritoriality Can J Zool 72455ndash464

AND D F LOTT 1995 Definitions of territoriality used in the study of variation in vertebratespacing systems Anim Behav 491581ndash1597


MCFARLAND D C 1994 Responses of territorial New Holland honeyeaters Phylidonyris novaehollandiaeto short-term fluctuations in nectar productivity Emu 94193ndash200

MrsquoCLOSKEY R T K A BAIA AND R W RUSSELL 1987 Defense of mates a territory departure rulefor male tree lizards following sex-ratio manipulation Oecologia 7328ndash31

MCNEIL R AND G ROMPRE 1995 Day and night feeding territoriality in willets Catoptrophorus semi-palmatus and whimbrel Numenius phaeopus during the non-breeding season in the tropicsIbis 137169ndash176

MIDDENDORF G A III 1979 Resource partitioning by an iguanid lizard thermal and density influ-ences PhD Dissertation University of Tennessee Knoxville 97 p

MILLER F L 1974 Four types of territoriality observed in a herd of black-tailed deer p 644ndash660 InF Walther and V Geist (eds) The behaviour of ungulates and its relation to managementIUCN Morges

MINTA S C 1990 The badger Taxidea taxus (Carnivora Mustelidae) spatial-temporal analysis di-morphic territorial polygyny population characteristics and human influences on ecologyPhD Dissertation University of California Davis 310 p

MITANI J C AND P S RODMAN 1979 Territoriality the relation of ranging pattern and home rangesize to defendability with an analysis of territoriality among primate species Behav Ecol So-ciobiol 5241ndash251

MITCHELL R J 1993 Path analysis pollination p 211ndash231 In S M Scheiner and J Gurevitch (eds)Design and analysis of ecological experiments Chapman and Hall New York

MOEHLMAN P D 1989 Intraspecific variation in canid social systems p 143ndash163 In J L Gittleman(ed) Carnivore behavior ecology and evolution Cornell University Press Ithaca

MYERS J P 1980 Territoriality and flocking by buff-breasted sandpipers variations in non-breedingdispersion Condor 82241ndash250

P G CONNORS AND F A PITELKA 1979a Territory size in wintering sanderlings the effects ofprey abundance and intruder density Auk 96551ndash561

1979b Territoriality in non-breeding shorebirds Stud Avian Biol 2231ndash246

1981 Optimal territory size and the sanderling compromises in a variable environment p135ndash158 In A C Kamil and T D Sargent (eds) Foraging behavior Garland STPM PressNew York

NELSON J 1995 Determinants of male spacing behavior in microtines an experimental manipulationof female spatial distribution and density Behav Ecol Sociobiol 37217ndash223

NEMTZOV S C 1997 Intraspecific variation in home range exclusivity by female green razorfish Zyr-ichtys splendens (family Labridae) in different habitats Env Biol Fishes 50371ndash381

NEWMAN M A 1956 Social behavior and interspecific competition in two trout species Physiol Zool2964ndash81

NUDDS T D AND C D ANKNEY 1982 Ecological correlates of territory and home range size in NorthAmerican dabbling ducks Wildfowl 3358ndash62

OSTFELD R S 1986 Territoriality and mating system of California voles J Anim Ecol 55691ndash706OVASKA K 1988 Spacing and movements of the salamander Plethodon vehiculum Herpetologica 44

377ndash386PETERSON R O 1979 The wolves of Isle Royalemdashnew developments p 3ndash18 In E Klinghammer

(ed) The behavior and ecology of wolves Garland STPM Press New YorkPHILLIPI T E 1993 Multiple regression herbivory p 183ndash210 In S M Scheiner and J Gurevitch

(eds) Design and analysis of ecological experiments Chapman and Hall New YorkPIELOU E C 1969 An introduction to mathematical ecology Wiley-Interscience New York 286 pPIETZ P J 1987 Feeding and nesting ecology of sympatric South Polar and brown skuas Auk 104

617ndash627PITELKA F A P Q TOMICH AND G W TREICHEL 1955 Ecological relations of jaegers and owls as

lemming predators near Barrow Alaska Ecol Monogr 2585ndash117POOLE T B AND D R MORGAN 1976 Social and territorial behaviour of laboratory mice (Mus mus-

culus L) in small complex areas Anim Behav 24476ndash480


PRIETO A A AND M J RYAN 1978 Some observations of the social behavior of the Arizona chuckwallaSauromalus obesus tumidus (Reptilia Lacertilia Iguanidae) J Herpetol 12327ndash336

PRIOR R 1968 The roe deer of Cranborne Chase Oxford University Press London 222 pPULLIAM R B GILBERT P KLOPFER D MCDONALD L MCDONALD AND G MILLIKAN 1972 On the

evolution of sociality with particular reference to Tiaris olivacea Wilson Bull 8477ndash89PYKE G H 1979 The economics of territory size and time budget in the golden-winged sunbird Am

Nat 114131ndash145 M CHRISTY AND R E MAJOR 1996 Territoriality in honeyeaters reviewing the concept and

evaluating available information Austral J Zool 44297ndash317RICHARD A 1974 Intra-specific variation in the social organization and ecology of Propithecus verreauxi

Folia Primatol 22178ndash207ROBERTSON D R 1981 The social and mating systems of two labrid fishes Halichoeres maculipinna

and H garnoti off the Caribbean coast of Panama Mar Biol 64327ndash340ROGERS L L 1987 Effects of food supply and kinship on social behavior movements and population

growth of black bears in northeastern Minnesota Wildl Monogr 971ndash72ROLANDO A P CAVALLINI B CURSANO AND A OLSEN 1995 Non-territorial behaviour and habitat

selection in the jay Garrulus glandarius in a Mediterranean coastal area during the reproduc-tive period J Avian Biol 26154ndash161

ROTHSTEIN S I J VERNER AND E STEVENS 1984 Radio-tracking confirms a unique diurnal patternof spatial occurrence in the parasitic brown-headed cowbird Ecology 6577ndash88

ROWLEY I 1973 The comparative ecology of Australian corvids II Social organization and behaviorCSIRO Wildl Res 1825ndash65

RUBENSTEIN D I 1981a Behavioural ecology of island feral horses Equine Vet J 1327ndash34 1981b Population density resource patterning and territoriality in the Everglades pygmy sun-

fish Anim Behav 29155ndash172RYER C H AND B L OLLA 1995 Influences of food distribution on fish foraging behaviour Anim

Behav 49411ndash418RYSER J 1995 Activity movement and home range of Virginia opossums (Didelphis virginiana) in

Florida Bull Florida Mus Nat Hist 38177ndash194SHAPIRO D Y 1991 Intraspecific variability in social systems of coral reef fishes p 331ndash355 In P F

Sale (ed) The ecology of fishes on coral reefs Academic Press San DiegoSMITH C C 1968 The adaptive nature of social organization in the genus of three squirrels Tamias-

ciurus Ecol Monogr 3831ndash63SMITH D C AND J VAN BUSKIRK 1988 Winter territoriality and flock cohesion in the black-capped

chickadee Parus atricapillus Anim Behav 36466ndash476SMITH F A J H BROWN AND T J VALONE 1997 Path analysis a critical evaluation using long-term

experimental data Am Nat 14929ndash42SNOW D W 1956 Territory in the blackbird Turdus merula Ibis 98438ndash447STAMPS J A 1973 Displays and social organization in female Anolis aeneus Copeia 1973264ndash272

1994 Territorial behavior testing the assumptions Adv Study Behav 23173ndash232STEPHENS D W AND S R DUNBAR 1993 Dimensional analysis in behavioral ecology Behav Ecol 4

172ndash183STRAHL S D AND A SCHMITZ 1990 Hoatzins cooperative breeding in a folivorous neotropical bird

p 131ndash155 In P B Stacey and W D Koenig (eds) Cooperative breeding in birds CambridgeUniversity Press Cambridge

SUNDQUIST M 1981 The social organization of tigers (Panthera tigris) in Royal Chitwan National ParkNepal Smithson Contrib Zool 3361ndash92

TEATHER K L AND R J ROBERTSON 1985 Female spacing patterns in brown-headed cowbirds CanJ Zool 63218ndash222

TSUKADA H 1997 A division between foraging range and territory related to food distribution in thered fox J Ethol 1527ndash37

TURPIE J K 1995 Non-breeding territoriality causes and consequences of seasonal and individualvariation in grey plover Pluvialis squatarola behaviour J Anim Ecol 64429ndash438


TYE A 1986 Economics of experimentally-induced territorial defense in a gregarious bird the fieldfareTurdus pilaris Ornis Scand 17151ndash164

VAUGHAN T A AND S T SCHWARTZ 1980 Behavioral ecology of an insular woodrat J Mammal 61205ndash218

WALSBERG G E 1977 Ecology and energetics of contrasting social systems in Phainopepla nitens (AvesPtilogonatidae) University of California Press Berkeley 63 p

WALTHER F R 1977 Social grouping in Grantrsquos gazelle (Gazella granti Brooke 1827) in the SerengetiNational Park Zeit Tierpsychol 31348ndash403

WARNER R R 1980 The coevolution of behavioral and life-history characteristics p 151ndash188 In GW Barlow and J Silverberg J (eds) Sociobiology Beyond naturenurture Westview PressInc Boulder

1991 The use of phenotypic plasticity in coral reef fishes as tests of theory in evolutionaryecology p 387ndash398 In P F Sale (ed) The ecology of fishes on coral reefs Academic PressSan Diego

WARREN H B 1974 Aspects of the behaviour of the impala male Aepyceros melampus during the rutArnoldia 61ndash9

WITTENBERGER J F 1981 Animal social behavior Duxbury Press Boston 722 pWOODWARD S L 1979 The social system of feral asses (Equus asinus) Z Tierpsychol 49304ndash316WYMAN R L AND L HOTALING 1988 A test of the model of the economic defendability of a resource

and territoriality using young Etroplus maculatus and Pelmatochromis subocellatus kribensis En-viron Biol Fishes 2169ndash76

YOUNG H 1956 Territorial activities of the American robin Turdus migratorius Ibis 98448ndash452ZAHAVI A 1971 The social behavior of the white wagtail Motacilla alba alba wintering in Israel Ibis

113203ndash211ZEZULAK D S AND R G SCHWAB 1979 A comparison of density home range and habitat utilization

of bobcat populations at Lava Bed and Joshua Tree National Monuments California BobcatResearch Conference Proceedings National Wildlife Federation Scientific and Technical Series 674ndash79

SUBMITTED 22 JANUARY 1999 ACCEPTED 23 JULY 1999

1

The American Midland NaturalistPublished Quarterly by The University of Notre Dame Notre Dame Indiana

Vol 143 No 1January 2000

Am Midl Nat 1431ndash29

A Review of Ecological Determinants of Territoriality withinVertebrate Species

CHRISTINE R MAHER1

Department of Biological Sciences University of Southern Maine Portland 04104

AND

DALE F LOTTDepartment of Wildlife Fish and Conservation Biology University of California Davis 95616

ABSTRACTmdashWe reviewed papers that compared intraspecific variation in territoriality vsalternative forms of spatial or behavioral organization with three goals (1) to discover whichecological variables act as determinants of territorial behavior and how they might act (2)to extract and evaluate predictions and evidence for determinants of territoriality and (3)to suggest ways for future studies to build upon what the review revealed Twenty ecologicalvariables have been predicted correlated with or experimentally demonstrated to relate toterritoriality within vertebrate species These variables include several characteristics of foodquantity predictability distribution quality renewal rate type density and assessibility Othervariables include nonfood resources population density habitat features mates space ref-ugesspawninghome sites predation pressure host nests (for brood parasites) and energyavailability We suggest several reasons why food resources are cited most often includingtheir biological significance ease of study and publishability of negative results Certaingroups of animals lend themselves to certain methods of study and therefore constrain thevariables measured Many variables are the subjects of apparently contradictory reports iesome papers report that an increase in a given variable increases territoriality and othersreport that a decrease in the variable increases territoriality After summarizing these reportswe hypothesized U-shaped relationships between the ecological variables and behavior thatcould accommodate all these findings However these hypotheses cannot be tested rigorouslyby most current studies because of methodological limitations We recommend a shift toquantification of intraspecifically varying spacing systems combined with simultaneous quan-tification of several ecological variables Relative importance of different determinants ofparticular spacing systems can be revealed via multiple regression analysis Hypothesizedcausal pathways in which one ecological variable determines another variable that in turndetermines territoriality can be tested by path analysis

1 Corresponding author Telephone (207)780-4612 FAX (207)228-8288e-mail cmaherusmmaineedu


INTRODUCTION




















Variable



Food


Resources
















































C E]QN





















1989 [C]TY

















12143(1)

TH

EA

ME

RIC

AN

MID

LA

ND

NA

TU

RA

LIST


Variable

Class

Food




Osteichthyes (N5 26) 6 0 4 4 0 0 2 0 0 0 0 0 8 0 7 4 0 4 0 0


57) 22 0 22 12 2 4 1 0 6 1 1 0 16 1 8 3 8 1 0 0

















































CAUSAL PATHWAYS








TERRITORIALITY






















LITERATURE CITED







































































































































































INTRODUCTION




















Variable



Food


Resources
















































C E]QN





















1989 [C]TY

















12143(1)

TH

EA

ME

RIC

AN

MID

LA

ND

NA

TU

RA

LIST


Variable

Class

Food




Osteichthyes (N5 26) 6 0 4 4 0 0 2 0 0 0 0 0 8 0 7 4 0 4 0 0


57) 22 0 22 12 2 4 1 0 6 1 1 0 16 1 8 3 8 1 0 0

















































CAUSAL PATHWAYS








TERRITORIALITY






















LITERATURE CITED

















































































































































































Variable



Food


Resources
















































C E]QN





















1989 [C]TY

















12143(1)

TH

EA

ME

RIC

AN

MID

LA

ND

NA

TU

RA

LIST


Variable

Class

Food




Osteichthyes (N5 26) 6 0 4 4 0 0 2 0 0 0 0 0 8 0 7 4 0 4 0 0


57) 22 0 22 12 2 4 1 0 6 1 1 0 16 1 8 3 8 1 0 0

















































CAUSAL PATHWAYS








TERRITORIALITY






















LITERATURE CITED
















































































































































































































C E]QN





















1989 [C]TY

















12143(1)

TH

EA

ME

RIC

AN

MID

LA

ND

NA

TU

RA

LIST


Variable

Class

Food




Osteichthyes (N5 26) 6 0 4 4 0 0 2 0 0 0 0 0 8 0 7 4 0 4 0 0


57) 22 0 22 12 2 4 1 0 6 1 1 0 16 1 8 3 8 1 0 0

















































CAUSAL PATHWAYS








TERRITORIALITY






















LITERATURE CITED























































































































































































1989 [C]TY

















12143(1)

TH

EA

ME

RIC

AN

MID

LA

ND

NA

TU

RA

LIST


Variable

Class

Food




Osteichthyes (N5 26) 6 0 4 4 0 0 2 0 0 0 0 0 8 0 7 4 0 4 0 0


57) 22 0 22 12 2 4 1 0 6 1 1 0 16 1 8 3 8 1 0 0

















































CAUSAL PATHWAYS








TERRITORIALITY






















LITERATURE CITED















































































































































































12143(1)

TH

EA

ME

RIC

AN

MID

LA

ND

NA

TU

RA

LIST


Variable

Class

Food




Osteichthyes (N5 26) 6 0 4 4 0 0 2 0 0 0 0 0 8 0 7 4 0 4 0 0


57) 22 0 22 12 2 4 1 0 6 1 1 0 16 1 8 3 8 1 0 0

















































CAUSAL PATHWAYS








TERRITORIALITY






















LITERATURE CITED






















































































































































































































CAUSAL PATHWAYS








TERRITORIALITY






















LITERATURE CITED










































































































































































TERRITORIALITY






















LITERATURE CITED























































































































































































LITERATURE CITED






































































































































































a review of ecological determinants of territoriality within vertebrate species

Documents