AMER. ZOOL., 14:177184 (1974). Crrelates f Ranging Behavir in a Grup f Red Clbus Mnkeys (Clbus badius tephrsceles) THOMAS T. STRUHSAKER New Yrk Zlgical Sciety, Nezu Yrk, New Yrk. and Rckefeller University, New Yrk, New Yrk SYNOPSIS. Data are presented frm 17 mnths f systematic sampling f the fd habits, ranging patterns and distributin f fd f a grup f red clbus mnkeys. N psitive r negative crrelatins were fund between the diversity f ranging patterns and the diversity f diet, distributin f fd species, r percentage f yung grwth in the diet. There was, hwever, a significant crrelatin between the diversity f ranging pattern and the number f days per mnthly sample that the grup was prximal t r had aggressive encunters with anther grup f red clbus mnkeys. INTRODUCTION Early hyptheses attempting t relate eclgy and scial rganizatin amng primates prved inadequate primarily because there was a paucity f infrmatin n rainfrest species at the time these hyptheses were prpsed (Crk and Gartlan, 1966). Even mre recent reviews prve inadequate as mre data n rain I am grateful fr the invaluable assistance given in the identificatin f plant specimens t Mr. A. B. Katende f the Makerere University f Kampala Herbarium and t Dr. Alan Hamiltn, previusly with the Department f Btany, Makerere University f Kampala. Dr. Hamiltn als assisted me with the majrity f the tree enumeratins. T bth f them I give my thanks. Prfessr Peter Marler, Dr. Tim CluttnBrck, Messrs. J. F. Oates, Steven Green, Peter Waser and Mrs. Mary Sue Waser all prvided valuable discussin n the subject f this paper, which has been t its advantage. I am grateful t Mr. M. L. S. B. Rukuba, Chief Cnservatr f Frests, Uganda Frest Department fr his permissin t study in the Kibale Frest. Mr. A. M. Stuart Smith, Uganda Frest Department, is thanked fr the lan f the BlumeLeiss Optical Height Finder. The kind and helpful assistance f the Uganda Frest Department staff at Frt Prtal and the Kanyawara Frestry Statin is gratefully acknwledged. I thank the Natinal Research Cuncil f Uganda fr permissin t cnduct my studies in Uganda. The American Sciety f Zlgists kindly prvided financial assistance permitting me t read this paper at the 1972 AAAS meetings. The study was financed by U.S. Natinal Science Fundatin grant GB 1147. 177 frest primates becme available (Struhsaker, 1969; Crk, 1970; Eisenberg et al., 1972). This paper cnsiders sme f the eclgical and behaviral factrs affecting ranging behavir in ne grup f red clbus mnkeys, a rainfrest species. These results are part f a mre detailed reprt n the behavir and eclgy f this species, which is currently in preparatin. There is gd reasn t believe that ranging behavir and certain aspects f scial behavir and scial rganizatin may be clsely crrelated amng primates. It is plausible, fr example, that the dispersin f fd resurces may affect ranging patterns and thereby affect grup size r intragrup scial rganizatin. Eisenberg et al. (1972) suggest tw frms f scial rganizatin as adaptatins t explitatin f certain kinds f fruit resurces: 1 (i) small, chesive unimale grups and (ii) large grups that split up int small fraging parties which spread ut and then annunce the lcatin f fd trees. Expressed in anther way, ne might predict that widely dispersed and clumped fd surces may necessitate a wide search pattern. Likewise a species with a predilectin fr a very diverse diet may als require a 1 1 presume they mean fd species whse individuals ccur in widely spaced clumps r as widely spaced individuals.
178 THOMAS T. STRUHSAKER wide search pattern while fraging fr fd. A wide search pattern culd be accmplished in a variety f ways, including large fraging scial grups, small scial grups that have a wide intragrup dispersin but have sme behaviral means f maintaining chesin, r small and chesive scial grups that have very wide daily ranging patterns. An apprach t understanding this relatinship begins by asking: des the distributin f fd r the diversity f diet affect the daily ranging pattern f mnkey grups? One way f cnsidering these questins is t cmpare the diet, distributin f fd, and ranging patterns n a mnthly basis fr a particular grup f red clbus. In ther wrds, des the mnthly ranging pattern f a grup f mnkeys vary with its diet and fd distributin? STUDY AREA AND RESUME OF SOCIAL ORGANIZATION Data presented in this paper were cllected frm red clbus mnkeys (Clbus badius tephrsceles Ellit 1907) living in the Kibale Frest f Western Uganda. Specifically, they are frm the CW grup (my main study grup) which lives in cmpartment 30 near the Kanyawara Frestry Statin (0 34'N, 30 21'E, elevatin 1,24 m). This part f the frest has been classified as a Parinari frest and is typified as being transitinal between trpical lwland and mntane rain frest (Kingstn, 1967). The red clbus f the Kibale Frest typically live in hetersexual scial grups averaging abut 0 in number. There are several adult males in each grup, althugh they are numerically exceeded by adult females. The CW grup was smaller than average grups f red clbus in the Kibale Frest and usually numbered 20. This grup has been under bservatin frm August 1970 t the present. During this perid it has ranged in size frm 19 t 2. Mst f the change in grup size is attributable t births and deaths f infants, with sme apparent and minr turnver in the juvenile membership. Three particular adult males have remained in the grup thrughut this perid, with n ther adult males jining r leaving. Their number was increased t fur in January 1972 when a subadult male reached sexual maturity in his behavir and became almst physically mature. The number f adult females has declined frm eight t six during this perid. Intergrup relatins are typically aggressive, but nt territrial because areas are neither defended nr used t the exclusin f ther grups. Adult and subadult males are the predminant participants and the nly aggressrs in these intergrup cnflicts. The usual utcme is fr ne grup t supplant anther grup, with an apparent dminance hierarchy existing between specific grups. The hme range f the CW grup is verlapped cnsiderably, if nt cmpletely, by the hme ranges f tw ther red clbus grups. METHODS AND DEFINITIONS Data presented in this paper represent the results f systematic samples made n 17 cnsecutive mnths frm Nvember 1970 thrugh March 1972, inclusive. During the first week f each mnth I attempted t fllw the CW grup fr five cnsecutive days. Ideally, the grup was t be fllwed frm sunrise t sunset n each f these days, giving a ttal f at least 1U/*! hr f cntact per day. In fact, this ideal sample was achieved n nly 7 f the 17 mnths (Table 1). Hwever, the amunt f cntact time with the CW grup in ther mnths was cnsidered adequate t permit relative cmparisns f all 17 mnthly samples. During each mnthly sample the mvements f the CW grup were pltted n maps f the study area having a scale f 1:200. The maximum linear spread f this grup rarely exceeded 0 m, and it was, therefre, relatively easy t encircle an area n the map indicating the psitin f the grup. Whenever the grup mved frm ne psitin t anther the time was indicated n the map and in this
RANGING BEHAVIOR OF RED COLOBUS MONKEYS 179 TABLE 1. Systematic mnthly samples j the CW grup f red clbus mnkeys. Mnth and year Nvember 1970 December January 1971 February March April May June August September Octber Nvember December January 1972 February March N. f cmplete days (Si lh/ 2 hr) with grup 4 4 3 2 2 3 N. f incmplete days«lli/ 2 hr) with grup _ 4 3 _ N. f minutes in cntact with grup 3,640. 3,648. 3,607. 3,709. 3,748. 3,696. 2,96. 2,89. '= 1,900. 3,61. 2,172. 3,440. 2,94. 2,114. 2,472. 2,412. 2,307. way their distributin f time in space culd be cmputed and pltted. The daily range maps were analyzed by superimpsing a transparent grid ver them. The grid was cmpsed f quadrats that were equivalent t 0 m n a side r 0.2 hectares. This quadrat size was selected because it seemed t represent the minimal size pssible cnsidering my mapping accuracy, which was abut ± 10 m. The amunt f time the grup spent in each specific quadrat was tallied fr each day and all days f each mnthly sample were then summed t give a mnthly summary f their distributin f time in space. The amunt f time tallied in this way exceeds the ttal amunt f time the grup was bserved because at sme time in every mnthly sample they ccupied at least tw quadrats simultaneusly. A quadrat was scred if it cmprised at least 2% f the area ccupied r if the grup extended at least 10 m int this quadrat at any given mment. In an attempt t express the diversity f the CW grup's ranging pattern an index f quadrat utilizatin diversity was cmputed fr each systematic mnthly sample. The ShannnWiener infrmatin measure (Wilsn and Bssert, 1971) was used t cmpute this index, N H= Xpi lg e pi, i = \ where H equals the amunt f diversity in the time spent inat quadrats fr a particular mnthly sample and where p { equals the relative amunt f time tallied fr the j'th quadrat [and lg e > t equals the natural lgarithm f this quantity]. Fr example, if the CW grup used nly fur quadrats in a particular mnth and the amunt f time spent in each quadrat was equal (2%), the index f quadrat utilizatin diversity wuld be 1.39. If in anther mnth they als used nly fur quadrats, but spent 70% f their time in ne and 10% in each f the remaining three quadrats, the index f quadrat utilizatin diversity wuld be 0.94, which represents a less diverse ranging pattern than in the previus example. Anther expressin f ranging pattern is the average daily distance traveled by the grup during each mnthly sample. This daily travel distance was determined fr each day in which the grup was fllwed frm sunrise t sunset and was measured directly frm the plts n the map. The majr disadvantages f this measure are that it fails t weight area in relatin t time spent in it and that it can nly be measured fr days in which the grup was fllwed fr at least \U/ 2 hr, thereby reducing the sample size. In each mnth mre than 100 feeding bservatins were made f red clbus. In the 17 mnths cnsidered here the number f mnthly feeding bservatins ranged
l'8o THOMAS T. STRUHSAKER frm 104 t 468. Each feeding bservatin usually cnsisted f the identificatin f the specific part eaten by the mnkey. On a few ccasins it was nt pssible t identify the plant species, but rather nly the part eaten. On a mnthly average such cases cmprised less than 1% f the ttal sample. Feeding bservatins were peratinally distinguished frm ne anther by the fllwing criteria: (i) a different individual mnkey feeding n the same item, (ii) the same individual mnkey feeding n a different item f the same fd species, (iii) the same individual mnkey feeding n a different fd species, r (iv) the same individual mnkey feeding n the same fd item f the same fd species at least 1 hr after any previus such bservatin. Fr example, if five mnkeys were feeding n yung leaves f the same tree species, this item wuld be scred five times. If these same five mnkeys cntinued feeding n the same item fr mre than 1 hr, this item wuld again be scred five times after 1 hr had passed since the previus scring. If the same five mnkeys then began eating leaf buds f the same tree, this item wuld be scred five times regardless f the time interval between the feeding n leaf buds and n the yung leaves f the same species. The majrity f feeding bservatins were made f the CW grup during the systematic mnthly samples. Hwever, sme bservatins were made utside f this time perid and f ther red clbus grups living in the same area. It was assumed that red clbus living in the same area wuld have similar diets regardless f their grup that the few feeding bservatins made f ther grups wuld nt bias the results f the CW grup when added t them. The index f fd species diversity was cmputed fr each mnth using the same ShannnWiener infrmatin measure described abve fr ranging patterns. In this case pj equals the prprtin f mnthly feeding bservatins tallied fr the uh fd species. Again, a larger index reflects a mre diverse mnthly diet. The distributin f fd species was estimated n the basis f strip enumeratins thrughut the hme range f the CW grup. Ft trails which had been previusly cut alng cmpass bearings and prvided access t all parts f the CW grup's hme range were used fr the strip enumeratin. The clearing f these trails in n way affected the current density f the trees enumerated. All trees within 2. m f the trail and that were 10 m r mre in height were identified. A height f 10 m was selected because the red clbus rarely descend belw this level. The transect sampled was 2,873 m lng and m wide. Excluding verlap areas that ccurred at trail junctins gave a ttal sample area f 1.43 hectares. This represents abut 3% t 4% f the ttal area ccupied by the CW grup. Densities f the varius tree species were cmputed directly frm these enumeratin data and expressed as number per hectare. Indices f dispersin were cmputed fr imprtant fd species using the rati f the variance/ mean (GreigSmith, 1964). When this rati is less than ne, a regular r unifrm dispersin is indicated, if greater than ne, a cntagius r aggregated dispersin. Cmputatin f a variance and mean were pssible because the tree enumeratin data were cllected and segregated in 0 m sectins alng the entire 2,873 m transect. Relative crwn size was determined fr 10 specimens each f 13 cmmn tree species. Only mature specimens were cnsidered. Tw measures were made: maximum crwn depth and maximum crwn diameter. A BlumeLeiss Optical Height Finder was used t measure the maximum and minimum height f fliage, the difference f which was the crwn depth. Maximum crwn diameter was determined with a tape measure and was measured frm the apprximate edge n ne side f the crwn, thrugh the trunk t the apprximate edge n the ther side. Precisin in bth these measures was prbably nt very great, but any surce f errr r bias was believed t be unifrm fr all species. Cnsequently, cmparisn f the relative measures is valid. Ideally, ne wuld like t estimate the ptential fd prducing area f the tree, but because mst trees have
RANGING BEHAVIOR OF RED COLOBUS MONKEYS 181 irregular crwn shapes ne cannt use crwn depth and width t cmpute surface area r vlume as wuld be the case if the tree crwns assumed true gemetrical shapes. I use, therefre, the sum f the maximum crwn depth and maximum crwn diameter as an index f crwn size, which makes the fewest assumptins abut crwn shape. Average values f crwn size were cmputed fr each f the 13 species, i.e., the mean crwn depth plus the mean crwn width. 2 An estimatin f the relative fd prducing area prvided by each f these 13 species is the prduct f their density and mean crwn size, which I call the cver index. All statistical results are based n netailed significance tests f the Spearman Rank Crrelatin Cefficient (r s ) as described in Siegel (196). The indices f the varius parameters were cmputed fr each f the 17 mnths and then ranked and cmpared. Thus, N equals 17. RESULTS There was n significant psitive crrelatin between the fllwing pairs f indices: (i) fd species diversity and quadrat g 36 " D ^ 340 120 g 3 00 Clbus bad/us iephrscetes CW grup 2 80 200 210 220 2 30 2 40 2 0 2 60 2 70 2.80 290 300 310 Index f fd species diversity FIG. 1. Mnthly plts f indices f quadrat utilizatin diversity vs. fd species diversity. Each pint represents the results fr a specific mnth, e.g., F72 is February 1972. r, 0.078. 2 It might be argued that the prduct f these tw means gives a better indicatin f crwn size than des their sum. Hwever, it makes little difference fr this analysis because cmparisn f the sum f these tw means with their prduct fr each f the 13 species gives r f 0.98, which is highly significant (P < 0.01), i.e., there is a psitive crrelatin between the sums and prducts. 3 60 " c 3 60 " jh 3.40 J 72 3.20 070 a 300 2 60 Clbus badius tephrsceles CW grup 071 N7I J7l """" S7I J.g7l F72 ip7l 071 F7I. July 71 June 7 N70 600 800 1,000 1,200 1400 1,600 1,600 2,000 2,200 2,400 Index f cver fr tp fur fd species FIG. 2. Mnthly plts indices f quadrat utilizatin diversity vs. the sum f the indices f cver fr the tp fur fd species in each mnth; abbreviatins as in Fig. 1. r, = 0.349. utilizatin diversity (r s = 0.078; P >0.0; Fig. 1); (ii) average indices f dispersin fr the tp fur fd species f each mnth 3 and quadrat utilizatin diversity (r s = 0.129; P >0.0); (iii) the cmbined indices f cver fr the tp fur fd species 4 f each mnth and quadrat utilizatin diversity (r s = 0.349; P >0.0; Fig. 2); (iv) percentage f yung grwth (flwers, buds, and yung leaves) in the mnthly diet and quadrat utilizatin diversity (r s = 0.177; P >0.0); and (v) the mean daily distance traveled per mnthly sample and the fd species diversity (r, = 0.209; P >0.0). Furthermre, nne f the abve pairs were significantly crrelated inversely. In a final attempt t relate the available measures f fd distributin and ranging pattern diversity, the mnthly data were pltted in a threedimensinal manner. The average cver indices fr the tp fur fd species in each mnth were pltted alng the hrizntal axis f a graph and 3 Only the tp fur fd species were cnsidered fr each mnth because n a mnthly average they cmprised 8.7% f the mnthly diet (range 43.4% t 78.7%). 4 When ne f the tp fur fd species is a species fr which data are nt available t cmpute a cver index then the th r 6th ranking species is used. This was the case in 9 f the 17 mnths, but was nt cnsidered t bias the results, because even in these 9 mnths the fur species used fr cmputing the cver index cmprised, n a mnthly average, 47.1% f the diet.
182 THOMAS T. STRUHSAKER against the average indices f dispersin fr the same fd species alng the vertical axis. At each mnthly intersectin f these crdinates was entered the index f quadrat utilizatin diversity fr that particular mnth. If sme cmplicated, but predictable relatinship existed between these three indices, ne might expect t find "cnturs" n the graph, with the arrangement f indices f quadrat utilizatin diversity frming sme pattern. In fact, n such "cnturs" emerged and in sme cases very different indices f quadrat utilizatin diversity ccurred at the same intersectin n the graph. These results are cntrary t ne's intuitive feeling that ranging patterns are related t and vary with fd distributin. Hwever, even if such a relatinship exists, the nature f it is nt readily predictable even n an intuitive basis. A simple crrelatin between dispersin, density, r cver indices f fd species and the ranging pattern f red clbus grups may nt exist, because similar ranging patterns might result frm very different trphic reasns. Fr example, restricted ranging patterns culd result either frm: (i) feeding n a rare species with a clumped distributin, but having a high density f fd per tree, and (ii) feeding n a cmmn and widely dispersed species als having a high density f fd per tree. Furthermre, the analysis in this paper fails t cnsider an imprtant variable, namely, the degree f phenlgical synchrny amng the fd species. Fr example, if the animals are feeding n a cmmn and widespread fd species, they will nt mve far if nly a few trees are bearing fd in a restricted area, i.e., if it is an asynchrnus fd species. Similar cmplexities can als be expected when they feed heavily n a rare and widely spaced fd species that lacks phenlgical synchrny. Hwever, if ne accepts the available results as reflecting the actual relatin between fd distributin and ranging patterns, it appears that the least diverse ranging pattern prvides adequate fd fr the red clbus mnkeys, at least n a shrtterm mnthly basis. Any mnthly ranging pattern mre diverse than this is apparently in respnse t ther variables. One f the mst likely variables affecting ranging patterns is intergrup cnflict. As mentined in the resumi f scial rganizatin, there is nearly cmplete verlap in the hme range f the CW grup and tw ther grups f red clbus. In additin, at least tw ther grups f red clbus infrequently enter the CW grup's hme range. The aggressive nature f intergrup cnflicts, including chasing and cunterchasing and the usual supplantatin f ne grup by the ther, has bvius effects n the mvements f the grups invlved in these encunters. There is, in fact, a psitive crrelatin between the number f days per ttal days in the mnthly sample n which the study grup had intergrup cnflicts and the index f quadrat utilizatin diversity (r, = 0.20; 0.0> P >0.01; Fig. 3). There t 3 80 > ^ 3.60 a JJ 3.40 0 320 Clbus badius lephrsceles CW grup.n7i F7I 070 Urn 71 S7I H7O. 'O'ln " I 0.2 0 3 0.1 0. 0.6 0 7 0.8 0.9 1.0 N days with intergrup cnflict per ttal days in mnthly sample FIG. 3. Mnthly plts f indices f quadrat utilizatin diversity vs. the number f days n which the CW grup had cnflicts with ther red clbus grups per ttal number f days in the mnthly sample, r, 0.20. is als a psitive crrelatin between the number f days per mnthly sample n which the CW grup was prximal (within 0 m) t anther red clbus grup and the index f quadrat utilizatin diversity (r s = 0.64; P «=> 0.01; Fig. 4). In ther wrds, in thse mnths when the CW grup interacted mre frequently with
RANGING BEHAVIOR OF RED COLOBUS MONKEYS 183 3.80.1 ^ 3.60 2 3.40 Clbus bad/us lephrsceles CW grup J 72 J 71 7. n 0 01 0 2 0.3 0 4 0 0.6 07 0 8 0 9 10 N dys with intergrup prximity per ttal dys in mnthly sample FIG. 4. Mnthly plts f indices f quadrat utilizatin diversity vs. the number f days n which the CW grup was prximal (within 0 m) t anther red clbus grup per ttal number f days in the mnthly sample, r, 0.64. ther grups they had a mre diverse ranging pattern. CONCLUSIONS AND DISCUSSION The distributin f fd as measured and evaluated in this study des nt allw predictin f the ranging pattern, measured either as the diversity f quadrat utilizatin r as the mean daily travel Because sme mnthly samples were cmprised f incmplete days, it might be argued that this wuld reduce the chance f bserving intergrup cnflict r prximity fr thse samples (Table 1). Hwever, incmplete days in the mnthly sample were thse days n which the bserver left the grup fr 3 t 4 hr frm abut 1200 t 100 r 1600 hr. At this time the mnkeys are relatively inactive and it is unlikely that this break affected the results n intergrup cnflicts, as evaluated in this analysis. Furthermre, f the 3 cmplete days f this 17 mnth sample the CW grup was prximal t anther grup n 34 days. On 73.4% f these days they were first prximal t the freign grup befre 1200 hr. On nly 8.8% f these 34 days were they first prximal t a freign grup between 1200 and 100 hr. This supprts the impressin that thse samples n incmplete days did nt unduly bias the results against intergrup encunters. As a final check against this pssible surce f bias, a Spearman Rank Crrelatin Cefficient was cmputed fr a cmparisn f (i) the number f days the CW grup was prximal t anther grup per number f minutes I was with the CW grup in each mnthly sample, and (ii) the indices f quadrat utilizatin diversity fr each mnth. These tw measures are psitively crrelated (r, = 0.41; 0.0 > P > 0.01). distance. CluttnBrck (1972) in anther study f ranging behavir amng red clbus presents data supprting sme f these cnclusins. Fr example, in his Figure 3 are data crrelating the percentage f shts, flwers, and fruit (crrespnding t my categry f yung grwth) and the number f quadrats (crrespnding t my index f quadrat utilizatin diversity) used by his grup f red clbus. I cmputed a Spearman Rank Crrelatin Cefficient fr these data and fund that there was n significant crrelatin (r s = 0.40; P >0.0). Apparently, red clbus grups mve in a mre diverse manner than is necessary fr sufficient fd. Hwever, this cnclusin cannt be accepted unequivcally because tw variables f pssible imprtance have nt been cnsidered. Neither the degree f phenlgical synchrny amng the fd species nr their nutritinal attributes have been evaluated in a way which allws them t be related t the diversity f ranging pattern. As mentined abve, similar ranging patterns culd cnceivably ccur in different mnths when the mnkeys fed n asynchrnus fd species, which differed greatly in their pattern f distributin. Pltting the distributin f the nutrients essential t the red clbus diet seems an verwhelming, if nt impssible, task. The whle prblem is further cmpunded by the pssibility f seasnal changes in the nutritinal value f a specific plant part n a particular individual tree. In spite f the pssible imprtance f these variables, it is apparent that intergrup cnflicts and prximity d increase the diversity f ranging pattern amng the red clbus at Kanyawara. Given a certain minimal mnthly ranging pattern, anything mre diverse than this is dependent n the frequency f intergrup encunters, nt n fd distributin as evaluated in this study. It is suggested as a wrking hypthesis that the relatively diverse diet f red clbus mnkeys permits greater independence f their mnthly ranging patterns frm fd dispersin than fr mnkey species with a mre mntnus diet.
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