Interspecific associations of Diana monkeys, Cercopithecus diana, in Sierra Leone, West Africa: biological significance or chance?

Anim.

Behao.,

1989,37,760-776

Interspecific associations of Diana monkeys, Cercopithecus diuna, in Sierra Leone, West Africa: biological significance or chance? Department

of Biology,

GEORGE University

H. WHITESIDES of Miami, Coral Gables, FL 33124, U.S.A.

Abstract. The advantages of interspecific associations are invoked frequently without first testing the null hypotheses: (1) observed associations occur by chance, and (2) when associations do occur, the organism’s behaviour is unaffected. During a study of two groups of Diana monkeys on Tiwai Island, Sierra Leone, the duration and frequency of interspecific associations were recorded along with behavioural and ecological data. Interspecific associations occurred in 36.6% of the samples from one group and 89.5% of the samples from the other. Predicted values of association based on null hypothesis 1 were generated using both Waser’s gas model and computer simulation based on species density and group spread. For interspecific associations of Diana monkeys with the six other species of forest monkeys resident on Tiwai Island, only associations with olive colobus, Procolobus verus, could not be accounted for by random events (i.e. exceeded null model predictions). For both study groups, associations were non-random with respect to their range use. The frequency of different behavioural categories of Diana monkeys was not independent of association status, but both varied with time of day. No significant relationship between interspecific association and behaviour was found for either study group, when controlling for time of day. The effects of random processes must be considered before biological significance is attributed to interspecific associations.

Most accounts of animal groups have been concerned primarily with those composed of one species (i.e. monospecific groups). However, some groups of animals consist of more than one species (i.e. interspecific, polyspecific, multispecific, or heterospecific groups or associations). Documentation of these interspecific associations has a long history, especially for tropical birds (Bates 1864; Wallace 1869; Belt 1874). Interspecific associations reported thus far for vertebrates are restricted to three taxa. Fish, especially on coral reefs, form such groupings (e.g. Ehrlich & Ehrlich 1973; Barlow 1974; Itzkowitz 1977; Wolf 1985). Bird flocks of mixed species in both temperate and tropical regions have received much attention (e.g. Moynihan 1962; Morse 1970, 1978; Ulfstrand 1975; Greig-Smith 1978; Herrera 1979; Thompson & Barnard 1984; Berner & Grubb 1985). Mammals, including ungulates (Lamprey 1963; Keast 1965), cetaceans (Pilleri & Knuckey 1969) and primates (e.g. Gartland & Struhsaker 1972; Struhsaker 1981; Gautier-Hion et al. 1983; Terborgh 1983; Waser 1987) also form interspecific associations. In addition, associations may occur between animals belonging to different orders (Altmann & Altmann 1970; Elder & Elder 1970; Struhsaker 1981), classes (Rasa 1983), or even 0003-3472/89/050760

+ 17 $03.00/O

phyla (McFarland & Kotchian 1982; Newton 1984). Why might interspecific associations occur? Most authors assume, at least implicitly, that associations occur because they provide benefits to the participants (i.e. animals that take part in interspecific associations are favoured via natural selection over those that do not), and thus attribute functional advantages to such associations. Functional explanations usually fall within two broad categories: foraging advantages and predator avoidance. The foraging advantage hypotheses include: (1) reduction of duplication of effort and regulation of return time (Cody 1971; Whitesides 1981; Terborgh 1983; Cords 1987), (2) increased prey capture rate (Klein & Klein 1973; Barlow 1974; Rudran 1978; Munn & Terborgh 1980), (3) increased resource detection (Gartlan & Struhsaker 1972; Krebs 1973; Caldwell 1981; Struhsaker 1981; Barnard & Stephens 1983), (4) availability of food items otherwise unavailable (Barlow 1974; Robertson et al. 1976; Merritt 1980; Struhsaker 1981; Gautier-Hion et al. 1983; Waser 1987), and (5) increased intraspecific competitive ability (Gautier-Hion et al. 1983; Waser 1987). The hypotheses that postulate predator avoid01989 The Association for the Study of Animal Behaviour 760

Whitesides:

Interspecific

ante advantages include: (1) increased detection of predators (Pulliam 1973; Struhsaker 1981), (2) increased confusion of predators, i.e. confusion effect (Morse 1977; Landeau & Terborgh 1986) (3) decrease in the probability of discovery or capture by predators (Hamilton 1971; Treisman 1975; Kiltie 1980; Wolf 1985; Turner & Pitcher 1986; Waser 1987) and (4) increased defence against or discouragement of predators (Struhsaker 1981). Members of interspecific associations could potentially benefit from a combination of foraging and predator avoidance advantages. For example, a decrease in vigilance behaviour afforded by interspecific associations could allow greater foraging efficiency (Barnard et al. 1982; Thompson & Barnard 1983; Sullivan 1984; Beveridge & Deag 1987). Before attempting to explain observed interspecific associations in terms of foraging or predator avoidance advantages, however, one must first reject the null hypotheses that: (1) the proportion of time, frequency and duration that organisms occur in association do not exceed values predicted by chance, and (2) when associations occur, the organism’s behaviour is unaffected. If the null hypotheses cannot be rejected, no basis exists for the assumption that the observed associations were the product of natural selection (Endler 1986). The generation of null models is one method by which null hypothesis 1 can be tested. Such a model for interspecific associations formed by species living in social groups can be envisioned as follows. The location of individual members of a social group defines the space or area occupied by that group. Even if groups of other species move independently within overlapping ranges, they will at times occupy adjacent or coincident areas such that the criterion for association is met. Waser (1982, 1984, 1987) generated a null model for Cercocebus albigena, interspecific mangebey, associations in the Kibale Forest, Uganda, using the perfect gas model to simulate independently moving primate groups. I also generated null models via computer simulation. The computer simulations predicted the expected percentage of time that focal groups of Diana monkeys spend in association with other primate species, given home range sizes and shapes of the Diana monkey groups, their intensity of use of different areas, the density of other species, and the species-typical group spreads. Both the computer simulation and gas models can be applied to species which do not normally form social groups.

associations

of C. diana

761

The advantage of the gas model is that, in addition to predictions of the percentage of time in association, it can also generate expected encounter rates and expected mean durations of association for the focal group with other species, by accounting for the speed of movement of the groups under consideration. Advantages of the computer simulation model include its use of home range size and configuration, and its incorporation of the focal group’s non-random range use in generating expected values. But perhaps the most important advantage is that, because the computer simulation model is iterative, it can produce a distribution of expected values against which observed association rates can be compared statistically. Failure to reject the null hypothesis that random (chance) processes cause the observed levels of association does not mean necessarily that the null hypothesis is correct. These associations still could be biologically significant (with either positive or negative ramifications for the species involved) without occurring more frequently or for longer durations than expected by chance. However, any biological significance should be manifested by differences in the behaviour and/or ecology of the animals involved. In addition to testing observed association values against null model predictions, I examined behavioural and ecological data from the two focal groups of Diana monkeys to determine whether these groups moved at different rates when in association and whether frequencies of behaviour differed along with association status. Although primate interspecific associations have been reported from South and Central America (Klein & Klein 1973; Mittermeier & van Roosmalen 1981; Pook & Pook 1982; Terborgh 1983) and Asia (Bernstein 1967; Rodman 1973) more reports come from Africa. These associations occur throughout the African rain forest zone from Kenya and Uganda in the east (Haddow 1952; Hayashi 1975; Struhsaker 1975, 1981; Rudran 1978; Struhsaker& Leland 1979; Waser 1980, 1982; Cords 1987) to Gabon and Cameroon (Gautier & Gautier-Hion 1969; Gartlan & Struhsaker 1972; Gautier-Hion & Gautier 1974; Whitesides 1981; Gautier-Hion et al. 1983), and to Ghana (Booth 1956) and Sierra Leone in the west (this paper; Oates & Whitesides, unpublished data). Most reports from Africa primate interspecific associations concern rain forest species of the genus Cercopithecus. In fact, all arboreal species of this genus studied thus far are reported to form such

762

Animal

Behaviour,

associations. Diana monkeys were chosen as the focal species for this study, because preliminary observations indicated that about half their time was spent in interspecific associations. This facilitated comparison of activity and ranging behaviour when focal groups were and were not in association. Species that either rarely occur or almost always occur in association require many more observations to yield sufficient data in each association state to allow such comparisons. STUDY

AREA

Tiwai Island (7”33’N, 1l”2l’W) lies approximately 60 km inland from the mouth of the Moa River in southern Sierra Leone and is 80-l 10 m above sea level. The island is approximately 12 km2 in area. Mean annual rainfall on Tiwai is about 3000 mm. In most years a distinct rainy season occurs from May through October with over 80% of the annual rainfall occurring during these 6 months. The dry season comprises the months December through March, when less than 5% of total rain falls. Temperature and humidity regimes follow typical patterns for most tropical forest regions. Tiwai Island lies within the Upper Guinean rain forest zone, and at one time undoubtedly supported classical mature lowland rain forest. Currently, the island is a mosaic of active farms, regenerating farmbush, palm swamps and old secondary forest. The old secondary forest habitat covers over one-half of the island; in this habitat many individual trees are 15 m or more in height, and emergents taller than 30 m are common. I used two non-adjacent study areas on Tiwai Island; these are identified as the east and west study areas. Both areas contained a grid of trails cut at 50-m intervals. The study areas completely contained the home ranges of the two focal study groups of Diana monkeys; group W was in the west study area and group E in the east. Primate Species on Tiwai Island Nine species of diurnal non-human primate inhabit Tiwai Island. These include: sooty mangabeys, Cercocebus a. atys; green monkeys, Cercopithecus aethiops sabaeus; Diana monkeys, Cercopithecus d. diana; lesser spot-nose monkeys, Cercopithecus petaurista buettikofiri; Campbell’s monkeys, Cercopithecus c. campbelli; red colobus monkeys, Procolobus 6. badius; olive colobus mon-

37, 5

keys, Procolobus verus; black-and-white colobus monkeys, Colobusp. polykomos; and chimpanzees, Pan troglodytes verus. Green monkeys are found primarily in Savannah habitats, but have colonized the forest zone in regions of extensive human slash-and-burn agriculture; they were seen rarely in the old secondary forest on Tiwai. Chimpanzees were uncommon on Tiwai. Neither of these species was observed near either study group of Diana monkeys during systematic sampling. Long-term systematic studies of three of the above species (olive colobus, red colobus and black-and-white colobus monkeys) on Tiwai Island, in addition to Diana monkeys, provided reliable estimates of species-typical mean group spreads and rates of movement shown in Table I (J. Oates, A. Davies&G. Dasilva, personal communications). Group spread and rate of movement estimates for the other three species (sooty mangabeys, lesser spot-nose monkeys and Campbell’s monkeys) derive from opportunistic observations by myself and other long-term workers on Tiwai Island (J. Oates, A. Davies, G. Dasilva & R. Kluberdanz, personal communications). I use group spread to indicate the average distance between individuals located on opposite sides (extremes) of a social group. Density estimates (Table I) for each of the six species observed in association with Diana monkeys are based on over 200 km of island-wide linetransect surveys. I present both a most representative estimate derived from the Hazard-Rate model (Hayes & Buckland 1983) and a range of density values generated by other techniques (Whitesides et al. 1988). The Focal Species Diana monkeys are frugivore-insectivores spending much of their time in the upper levels of the forest. They apparently require tall forest (e.g. primary or old secondary), because they do not occur in areas devoid of trees over 15-20 m in height (personal observation). In areas such as Tiwai Island where old secondary forest frequently exists next to regenerating farmbush, Diana monkeys rarely use the latter habitat type. Diana monkey groups typically contain 12-30 individuals (most commonly 15-25). All groups whose composition could be reliably determined contained six to eight adult females with only one

Whitesides: Interspecific Table I. Mass, densities,

group

mangabey

Lesser

spot-nose

Campbell’s

Olive

monkey

monkey

Red colobus

monkey

colobus

Black-and-white

monkey colobus

and movement

Mean adult female mass (kg)?

Species Sooty

spreads

monkey

6.2 (N=4) 2.9 (N=7) 2.7 (N=9) 8.2 (N= 14) 4.2 (N= 14) 8.3 (N= IO)

763

associations of C. diana rates of Tiwai

Density (groups/km2)$ 1.1 (1.1-1.1) 3.5 (3.340) 2.8 (2.7 -3.1) 1.4 ’ (142.0) 1.3 (l.lLl.3) 50 (5.0-58)

monkeys*

Mean spread of groups (m)

Mean group movement rate (km/day) 2.0 (1.8-2.5) 1.2 (1.0-1~5) 1.2 (1.0~1~5) 0.6 (0.5-0.7) 1.2 (1.0-1.5) 0.5 (040.6)

(708_qoo) (3OYO) (405060) (708qOO) (202530) (202-530)

* Values for density, mean group spread and mean group movement rate are most representative estimates with mimimum and maximum estimates in parentheses. t Estimates of mean adult female mass with sample sizes in parenthesis are from J. Oates, G. Whitesides, A. Davies, P. Waterman, G. Dasilva & S. Mole (unpublished data). C. diana adult female mass = 3.9 kg (N = 11). $ Density estimates are from Whitesides et al. (1988).

fully adult male. Both study groups contained one adult male and seven adult females throughout the 12-month period reported here; the differences in size between the two study groups resulted entirely from differences in younger age classes.

METHODS I followed group W for 6 days (dawn to dusk) each month from March 1983 through June 1984, and group E for 3 days each month from July 1983 through June 1984. The 6 sample days each month for group W were divided into two blocks of 3 consecutive days with one 3-day block before and one after the mid-point of each month. Sample blocks were separated by a minimum of 7 days. The single sample of 3 consecutive days for group E occurred during the middle (between the 10th and 20th) of each month. During each day of sampling, I conducted scan samples at 20-min intervals, The duration of each scan sample was 7 min or until five individuals were sampled, whichever came first. During a scan, I sampled individual monkeys in the order in which they were seen. Once detected and clearly observed and after 5 s elapsed, a monkey’s behaviour (at that instant), its location, and its spatial relationship to both conspecifics and heterospecifics were

recorded. If the individual was not visible after the initial 5 s, I made no record. The delay time between initial observation and data recording was an attempt to reduce the bias inherent in scan sampling of overrepresenting conspicuous behaviours. The length of the delay was a compromise between data loss (i.e. animals disappearing from view during the delay period) and bias reduction. Behavioural states of Diana monkeys change rapidly, especially for highly conspicuous behaviour such as vocalization, locomotion and agonistic interactions; therefore, even relatively short delay times are effective in bias reduction. At IO-min intervals (2 min before and 8 min after each scan sample), I recorded the identity of the mapped 50 x 50-m grid cells containing at least one member of the study group; these are termed group samples. During these samples, I also noted the presence of any individual of a heterospecific primate group located within 50 m of any individual member of the study group of Diana monkeys. While a 50-m association criterion is somewhat arbitrary, it represents an upper limit around the study group which I could monitor effectively for groups of other species. In addition, primates almost certainly have the ability to monitor the movements of other groups at distances of at least 50 m, even in dense rain forest.

764

Animal

Behaviour,

I occasionally observed individual primates of other species with no obvious relationship to a social group of their species within 50 m of my study group. Because the potential advantages and disadvantages of interspecific association may be very different for these solitary individuals compared with social groups, I did not include these observations in the analysis. I employed non-parametric statistical tests throughout, except for the use of a three-way loglinear model to test for independence of categorical data among time of day, behaviour, and association status. G-statistics were adjusted using Williams’ correction @okal& Rohlf 1981). A priori, I selected an alpha value of 0.05 as the significance criterion for all statistical tests. However, due to the vagaries of data collection under most field conditions, P-values of less than 0.10 may indicate when biologically important phenomena should be examined further. Thus, I report three ranges of Pvalues in the text: P> 0.10, 0.10 2 P> 0.05, and PGO.05.

The Null Models Perfect gas model Waser (1982, 1984) assumed that groups of monkeys behaved like molecules in a two-dimensional ideal gas with the exception that monkey groups, unlike molecules, are transparent (i.e. capable of passing through each other without interaction). Mitani & Rodman (1979) showed that the mean radius of an ellipse is a robust estimate of the radius of a circle with equivalent area, as long as the axes of the ellipse differ by less than a factor of 10. Primate groups of irregular shape, therefore, may be modelled accurately by a circle whose radius is estimated by one-half the mean group spread. Thus, the validity of neither the gas model nor the following computer simulation model requires that the shape of primate groups in the wild closely approximate a circle. Following Waser (1982, 1984, 1987), if the velocities of two types of groups (species) follow Maxwell-Boltzmann distributions with mean velocities of rJ and fij, then their encounter rate (Z) is Z=2x(fi?++$xP,x(ri+r,+d) where P, equals the density of groups of speciesj per unit area, r equals the estimate of one-half the mean group spread, and d equals the criterion distance for association (50 m).

37, 5

The mean duration of association (K) of a group of species i once it encounters a group of species j is r12xs I K= 4 x (6; x 5;)’ where s=r,+r,+d Therefore, the expected proportion of time (7) spent by a group of species i in association with groups of species j is T=Zx

K=;xP,xs:

Computer simulation model The computer simulation model generated expected association frequencies for a focal group with groups of other species given the random placement of these groups within the focal group’s home range. This iterative model assumes the focal group of Diana monkeys was always present within the home range and that the probability of its centre being located in a particular grid cell was proportional to the observed frequency of use in the field of that grid cell by the focal group. The location of heterospecific groups within the mathematically represented home range also was assigned randomly. The densities of the other species (heterospecific groups) were taken from island-wide estimates (Table I). The number of groups of each species present in the home range during any one iteration was generated by a Poisson distribution with mean of observed density. For comparison, I also ran simulations in which I replaced this Poisson distribution model with both low variance (uniform distribution) and high variance (clumped distribution) models with the same mean densities. For each iteration during the simulations run using the low variance model, the number of groups of a species within the focal group’s home range was the integer value either immediately above or below the mean density for that species; these values were chosen in frequencies that yielded the mean density. The high variance model used either zero or four groups of a species within the study group’s home range; these values also were chosen in frequencies that yielded the mean density for that species. For each iteration the model determined which species, if any, was in association with the focal group by comparing the distance from the centre of the focal group to the centre of each group of

Whitesides: Interspec$c another species. If this distance was less than the radius of the focal group plus the radius of the heterospecific group plus the association criterion (50 m), the model scored an association of that species with the focal group. During any one iteration, if two or more groups of the same species lay within the distance necessary to score an association, only one was scored (i.e. the focal group could be in association with only one group of a particular species, during that iteration). The percentage of time in association of each species with the focal group was then 100 times the number of iterations in which that species was scored as in association divided by the total number of iterations. Throughout this paper, I use percentage of samples in association synonomously with percentage of time in association. Because of uncertainty in estimates of speciestypical group spreads and of densities of groups, I ran three simulations for each study group of Diana monkeys with each other species. One simulation for each study group used the best estimates of island-wide species-specific densities of groups and group spreads; the other simulations used the maximum and minimum estimates for these parameters (Table I). Similarly, when I derived expected association values from Waser’s gas model, I used the same range of parameter values. Each computer simulation for each study group of Diana monkeys with another species was composed of 1000 expected association values; thus a total of 36 000 expected values was generated (three simulations x six species x 1000 values/simulation x two study groups). Each association value for group W was derived from 5000 iterations and for group E from 2500 iterations. The number of iterations per value approximately matched the number of field observations (i.e. group samples) collected for each study group. Thus, each simulation produces a distribution of expected values that can be compared statistically to the field observations. RESULTS Group Spread and Rate of Movement of Study Groups Members of a Diana monkey group were regularly spread over a wide area. At times, individuals belonging to the same social group were separated

associations of C. diana

765

by over 200 m. The two study groups differed in the mean number of grid cells occupied during each group sample (Mann-Whitney U-test: Z= -4.005, PcO.05, Nw=72, NE=36). I estimated the average spread of group W as 100 m and that of group E as 120 m. This difference may be caused by either group size or habitat differences; group W contained 20 individuals which used 41 ha, and group E contained 27 individuals using 29 ha (group sizes as of July 1983). Because group members were spread over a large area, Diana groups rarely moved in organized linear progressions. Instead they tended to move in ameboid-like fashion. Thus, I estimated the rate of group movement by calculating the distance between the geometric centres of the 50 x 50-m grid cells occupied by the study group during consecutive IO-min sampling periods. Group W moved 1019+28.lm/day(8+s~,N=96);groupEmoved 1513 + 63.7 m/day (N= 39). Because these rates were significantly different (Wilcoxon matchedpairs signed-ranks test by month, Z= -3.059, N= 12, P < 0.05), I generated separate expected values from the gas model for the two study groups. Observed Associations of Diana Monkeys Table II displays the mean percentage of IO-min intervals each month in which I observed each study group of Diana monkeys in association with each heterospecific species (N= 12 months for each species; total number of IO-min intervals: N= 5309 for group W, N=2647 for group E). Results showed relatively low levels of association by other species with group W. Only olive colobus (11.8%) and black-and-white colobus monkeys (14.4%) occurred with group W in more than 10% of the samples, although at least one species was within 50 m of group W during 36.6% of the samples. For group E, four of six species were in association for more than 10% of the samples (lesser spot-nose monkeys: 10.1%; red colobus monkeys: 13.4%; black-and-white colobus monkeys: 15.1%; and olive colobus monkeys: 86.2%). Overall, group E was within 50 m of another species during nearly 90% of the samples. Rankings of observed percentage of time in association by species with group W were identical to the rankings of species-specific densities of groups except for olive colobus. This pattern also held for the percentage of time other species were in association with group E, except that red colobus

766

Animal Behaviour, Table II. Mean in heterospecific

percentage of samples association

(k

SE)

37, 5

two groups

Diana

Species Sooty mangabey Lesser spot-nose monkey Campbell’s monkey Red colobus monkey Olive colobus monkey Black-and-whitecolobus Any species?

Group

monkey

study

W

1.18&0.28 7,34+1,28 5.06+0.85 3.71 Ifr 1.66 11.78k3.99 14.38 k3.69 36.59k3.18 (28.32k3.35)

of Diana

group

Group

monkeys

were

Wilcoxon test* E

0.99 kO.37 10.14$-3.83 2.41 kO.64 13.37k3.02 86.20 k 2.50 15.07*3.21 89.51 * 1.85 (35.21 k4.88)

T

P

22.5 38 9 8 0 37.5 0 10

NS NS

< 0.05 < 0.05 < 0.05 NS

i 0.05 < 0.05

* Wilcoxon matched-pairs signed-ranks test by month (PI= 12) for differences between the two study groups with respect to the percentage of samples in association for each heterospecific species. t All associations containing a study group of Diana monkeys; values in parentheses are for all associations excluding those with only olive colobus.

joined olive colobus by having a higher ranking than expected from the rankings of densities of groups. The percentage of time most species were in association with the two study groups exhibited marked fluctuations among months (Fig. 1). These fluctuations occurred for both study groups of Diana monkeys, and thus, apparently were not an effect of the number of days sampled within a month. Group E occurred in association with other species more frequently than group W even when associations with olive colobus were not included (Table II). Campbell’s monkeys were in association with group W more frequently than with group E (5 1% versus 2.4%, Wilcoxon matched-pairs signed-ranks test by month, Pi 0.05; Table II), while groups of red colobus and groups of olive colobus monkeys both were in association with group E more frequently (3.7% versus 13.4% and 11.8% versus 86.2%, Wilcoxon matched-pairs signed-ranks tests by month, both Ps < 0.05; Table II). The two study groups of Diana monkeys did not differ significantly in their association percentages with respect to the other three species (sooty mangabeys, lesser spot-nose monkeys and blackand-white colobus monkeys). I used the runs test (Siegel 1956) to examine potential clumping of monthly levels of association for each heterospecific species with each study group of Diana monkeys. No significant clumping or patterning was found (all rs between 4 and 9,

Ps > 0.05, N, = Nz = 6), and only one of 14 tests displayed such a trend (sooty mangebeys with group W; r=4, PGO.10, N,=N2=6). Struhsaker (1981) suggested that association levels of an habituated study group with relatively unhabituated groups of other species might be abnormally low, because the unhabituated primates would avoid the observer and thus the habituated study group. However, this hypothesis would predict increasing association levels throughout a study as these other groups gradually become habituated to the observer. As these animals become habituated, they should tolerate the presence of the observer for longer periods, and hence, spend more time in association with the group under study. Therefore, I examined the correlation between monthly percentage of samples each species was in association with the Diana study groups and the cumulative month of study. The only significant correlation of the 14 calculated was for association levels of groups of black-andwhite colobus monkeys with group E (Kendall rank correlation; z=O.454, PC 0.05, N= 12). In addition, trends (0.102 P> 0.05) of association levels with month of study occurred for groups of sooty mangabeys and groups of black-and-white colobus monkeys with group W (Kendall rank correlations: sooty mangabeys, 7 =0.424; blackand-white colobus, z = 0.424; 0.10 2 Ps > 0.05, Ns = 12). Thus, degree of habituation to a human observer might be an important factor affecting the observed level of association only for black-and-

Whitesides: InterspeciJic associations of C. diana

767

Procolobus _ vefus 94-, ;:

98-

I: :: 0

74 70

“““o”“’

a

1983

1984

of study

Figure 1. Monthly was in association

fluctuations with other

in the percentage species. 0: group

of time (percentage W; 0: group E.

white colobus monkeys, although the possibility that seasonal factors produced the observed correlations cannot be discounted.

Versus Predictions

of the Gas Model

Expected association values calculated from the gas model for both study groups of Diana monkeys

each study

group

of Diana

monkeys

along with the values derived from field observations are shown in Table III. Encounter

Observations

of samples)

rates

For three of six species (sooty mangabeys, red colobus monkeys and black-and-white colobus monkeys) the observed encounter rate with group W was below the range of expected values (Table III). For two species (lesser spot-nose monkeys and

mangabey

Species

III. Expected

0.69 (0.74-0.66) 1.31 (1.80-1.07) 1.09 (1.45-0.92) 0.46 (0.73-0.42) 0.46 (0.54-0.34) 1.26 (1.56-1.18)

study

0.74

0.58

0.25

0.97

1.13

0.28

Observed

W

0.82 (I ,0330.75) 1.75 (2.29-1.49) 1.45 (1.84-1.27) 0.68 (1.06-0.64) 0.61 (0.69-0.48) 1.94 (2.34-1.86)

Expected

Group

groups

Encounter rate (encounters/day)

for both

1.25

1.06

0.88

0.80

1.27

0.36

Observed

E

of Diana

Group

111 (129989) 136 (1577113) 142 (1633118) 213 (238-196) 128 (144108) 179 (189-168)

W

146

149

109

39

48

32

107 (121-88) 120 (133-105) 125 (138-109) 165 (180-156) 113 (1233100) 138 (143-132)

Expected

Group

association duration (min/association)

W and E) generated

Observed

Mean

(groups

Expected

monkeys

89

601

110

22

59

20

Observed

E

(363745)

(ElO)

(Z625)

(232530)

(2s2-96)

(1 Fl4)

Expected

Group

15

86

13

2

10

1

(303l38)

(7-i)

(A-422)

(192-226)

(22%)

(ldll2)

Expected

Group

E

14

12

4

5

7

1

Observed

of time in association Diana monkeys

Observed

W

Percentage with

by the gas model*

* The expected values for each parameter derived using best estimates of density, group spread and movement rate (Table I). Numbers in parentheses represent expected values calculated from combinations of extreme parameter estimates from Table 1. Values from Diana study groups used for calculation of expected values are: group W: mean movement rate = 1.0 km/day, mean group spread= 100 m; group E: mean movement rate= 1.5 km/day, mean group spread = 120 m.

Black-and-white monkey

colobus

monkey

Olive

colobus

monkey

monkey

Group

values

Expected

association

monkey

Red colobus

Campbell’s

Lesser spot-nose

Sooty

Table

.? b

b 1. 3 e B Sk 8 F’ F

769

Whitesides: InterspeciJic associations of C. diana Campbell’s monkeys) observed encounter rates fell within the range of expected values. Only groups of olive colobus monkeys had an observed encounter rate which exceeded the expected values. Four of six species (sooty mangebeys, lesser spot-nose monkeys, Campbell’s monkeys and black-and-white colobus monkeys) had observed encounter rates with group E that were below the range of expected values (Table III). The observed encounter rate for groups of red colobus monkeys was within the expected value range. Only groups of olive colobus monkeys had an observed encounter rate with group E that exceeded the range of expected values. Mean duration of association Only olive colobus groups had an observed mean duration of association that exceeded the range of expected values for both group W and group E (Table III). While observed mean duration of associations between olive colobus groups and group W barely exceeded the maximum value calculated by the gas model (149 min observed versus 144 min expected), the mean duration of olive colobus groups with group E was nearly five times the maximum expected level (601 min versus 123 min). For both study groups of Diana monkeys, the observed mean durations of association with each of the remaining five species were below the range of expected values. Percentage of time in association The observed values of the percentage of time most other species spent in association with the two study groups of Diana monkeys were below the range of expected values calculated from the gas model (Table III). Only groups of olive colobus monkeys were observed in association for a greater percentage of time than expected. As with the observed mean duration of association values, the percentage of time olive colobus groups were in association with both group W and group E exceeded the maximum calculated value by the gas model. Observations Versus Predictions of the Computer Simulation Model The computer-generated expected values for the percentage of time groups of other species were in association with the study groups of Diana monkeys are shown in Fig. 2. The results of these

g ‘;;

7 24.(b’

(86.2%).

E

.

0’ S’M

LSNM

CM

RCM

OCM

BWCM

Figure 2. Computer simulation of null model for expected percentage of time (percentage of samples) study groups of Diana monkeys (a: group W; b: group E) were in association with other species. Three simulations were run for each species.SM: Sooty mangahey; LSNM: lesser spot-nose monkey; CM: Campbell’s monkey; RCM: red colobus monkey; OCM: olive colobus monkey; BWCM; black-and-white colobus monkey. Vertical bars indicate the range of 1000 expected values generated for each simulation. Boxes contain 95% of expected values. The central vertical bar for each species represents the simulation using the most representative group density and group spread for that species. The other two simulations for each species were generated using extreme values of group density and group spread. 0: observed values. In (b), olive colobus, P. wrus, were observed in association with group E during 86.2% of samples.

simulations were quantitatively similar to those produced by the gas model. The computer simulation model, however, consistently generated expected values that were lower than those calculated from the gas model. Nonetheless, only groups of olive colobus monkeys were in association with both Diana study groups for a significantly greater percentage of time than expected by chance. The values for observed percentage of time in association for all other species were either within or significantly less than the computer simulation values. Thus, despite some disagreement in the magnitude of the expected values generated by the gas model versus the computer simulation model, the predictions were qualitatively similar. In all cases

770

Animal

Behaviour,

the two models agreed as to whether observed associations formed by the study groups exceeded predictions. The computer simulations run using the low variance model (uniform distribution of groups for generating the number of groups of each species within a Diana study group’s home range during each iteration) produced slightly greater (ca. 4%) mean values for percentage of time in association than the simulations run using the Poisson distribution. The values generated using this low variance model did not alter the acceptance or rejection of the null hypothesis for any of the 12 comparisons. Computer simulations also were run using a high variance model (clumped distributions of groups). The values generated using this model were approximately 10% lower than those generated using the Poisson distribution. Use of these values for testing the null hypothesis altered acceptance or rejection in only one of 12 comparisons (red colobus associations with group E). These results indicate that the computer simulations are relatively robust with respect to the distributional model used to generate the number of groups of each species used in each iteration.

Effects of Association viour and Ranging

Status on Patterns of Beha-

Interspecific association could still be biologically relevant for one or more of the species involved even though they occurred no more frequently than expected by chance, if the associations resulted in alteration of behaviour. I compared the relative frequencies of occurrence of six behavioural categories (feed-forage, inactive, locomotion, social behaviour, vocalization, and other) for Diana monkeys within 50 m of an individual of another species (i.e. in association) versus those more than 50 m from a heterospecific (Tables IV and V). Members of both study groups of Diana monkeys always were observed within 50 m of a conspecific group member. Behaviour was not independent of association state for group W (Gtest, Gadj = 11.58, df= 5, P < 0.05) but was independent of association state for group E (Gad, = 3.51, df = 5, P> 0.10). However, behaviour was not independent of time of day for either study group (group W: Gad,= 21964, df = 65, P < 0.05; group E: Gad,= 124.40, df = 65, P < 0.05). In addition, association state was also not independent of time of day

37.5

for either study group (group W: Gad,= 123.57, df= 13, PO.lO; group E: x:=65.60, df=65, P~0.10). Tests for independence among pairs of factors while holding the third factor constant showed significant nonindependence between association state and time of day (group W: xi= 366.80, df= 78, P < 0.05; group E: ~;=27344, df=78, PO.lO; group E: ~;=67.27, df=70, P>O.lO). The frequency of individual 50 x 50-m grid cells used by members of each study group while in association was significantly different from the frequency of use while not in association (group W: G,, = 1843.70, df = 136, P < 0.05; group E: Gad,=479.97, df= 88, P-zO.05). The frequency of individual grid cell use, however, was neither uniform nor random throughout either study group’s home range (test for coefficient of dispersion; group W: x2 = 30 977.14, df= 165, P< 0.05; group E: x2=8330.13, df=l27, P-cO.05). The difference in use while in association, therefore, could result either from the study groups’ differential use of grid cells with time of day or the probable non-uniform habitat use by groups of other species. A difference in the rate of movement of a group when in association, in comparison with when the group was not in association, could indicate the biological importance (either in a positive or negative sense) of interspecific association. I therefore compared group movement rate when a study group was in association versus when it was not by computing the average distance moved per IO-min interval per day. For a IO-min interval to be included in either category, the group samples both

771

Whitesides: InterspeciJic associations of C. diana Table IV. Distribution of behavioural categories of Diana group W as a function of association state and time of day* Behavioural category Time interval (hours) 0600-0700 0700-0800 0800-0900 0900-1000

1000~1100 1100~1200 1200-1300 1300~1400 1400~1500 1500-1600 1600-1700 1700-1800 1800-1900 1900-2000

Totals

Association state? A NA A NA A NA A NA A NA A NA A NA A NA A NA A NA A NA A NA A NA A NA

Inactive

Forage

Social behaviour

Locomote

0 0

8 102

0 3

4 49

0 0

88 545

1 7

31 167

0

1

118 561

0 12

35 146

2 0

188 499

5

10

3 0

218 469

0

Vocalize 0

1 0 1 0

Other 0 1

Totalf 12 162

(6.9%)

2 21

122 (14.1%) 741

3 18

156 746

(17.3%)

2

54 124

0 3

3 18

252 654

(27.8%)

6 19

56 108

0

6 19

295 611

(32.6%)

242 429

14 12

56 96

8 13

320 552

(36.7%)

189 464

9 23

55 104

6

6 20

262 628

(29.4%)

11 7 18

142 453

6 23

111

0 0

8 23

198 (24.0%) 628

5 14

164

8 24

44 104

2

5 26

228 597

(27.6%)

428

5 17

147 452

7 17

40 112

5 21

204 620

(24.8%)

2 6

130

I 22

33 137

11

500

23

184 (21.1%) 689

0 5

81 556

8 19

24 133

1 29

745

0 6

100

11

449

23

32 129

5 21

149 (17.0%) 628

0 4

20

3 2

3 30

2

0 5

26 (19.5%) 107

109

7812

28

327

1 2

64

302

35

2052

1 0 1 1

1 0 1 1 1 0 3

1 0 0

114 (13.3%)

10 630

* Numbers are occurrences of individuals in behavioural categories determined from scan samples. t A: association, i.e. within SOm of member of a group of another species; NA: not in association. 1:Values in parentheses are percentage of hourly total which are in association.

preceding and succeeding the interval must agree as to association state. Group W moved 14.0 f0.66 m/interval (~&SE, N = 71 days) when in association and 14.2 k 0.5 1 m/ interval (N=71 days) when not in association. Group E moved 21.OkO.87 m/interval (N=36 days) when in association and 22.9k2.78 m/ interval (N=26 days) when not in association. For both study groups, the mean distance moved per interval per day when in association was not different from the distance moved when not in

association (Wilcoxon matched-pairs signed-ranks tests; group W: z = - 0.609, N = 70, P > 0.10; group E: z= -0.216, N=26, P>O.lO).

Associations of Diana Monkeys with Olive Colobus Monkeys Olive colobus was the only species that occurred in association with either study group of Diana monkeys for more than 20% of the samples (Table

772 Table

Animal Behaviour, V. Distribution

of behavioural

categories

of Diana

group

E as a function

Behavioural

interval

Time (hours)

0600-0700 0700-0800 0800-0900 0900-1000 1000-l

100

1100-1200 1200-1300 1300-1400 1400-1500 1500-1600 1600-1700 1700-1800 1800-1900 1900-2000 Totals

Association state? A NA A NA A NA A NA A NA A NA A NA A NA A NA A NA A NA A NA A NA A NA

Inactive

Forage

0 0

27 32 169 151 197 121 209 130 242 112 236 86 229 102 238 52 194 103 226 100 217 91 221 90 131 120 20 10

3 0 0 2 0 0 2 I 2 1 6 1 2 1 10 3 10 3 2 3 0 1 I 0 3 0 57

3856

Social behaviour 0 0 7 5 9 13 3 6 11 1 11 2 9 0 17 2 12 5 9 3 14 0 12 9 8 7 0 0 175

37, 5 of association

state and time of day*

category

Locomote I1 12 70 69 90 42 97 38 96 40 98 34 83 44 106 18 81 33 89 41 92 26 94 36 68 73 20 9 1610

Vocalize

Other

0 1 0 0 I 0 0 0 0 0 2 0 0 1 1 0 1 0 I 1 1 0 2 0 0 0 0 0 12

4 1 5 8 7 3 9 1 11 8 8 5 9 3 13 3 9 4 7 4 8 3 3 3 3 6 0 0 148

Total: 42 46 254 233 304 181 318 175 362 162 357 128 336 151 377 76 307 148 342 152 334 123 332 139 211 206 43 19

(47.7%) (52.2%) (62.7%) (64.5%) (69.1%) (73.6%) (69.0%) (83.2%) (67.5%) (69.2%) (73.1%) (70.5%) (50.6%) (69.4%)

5858

* Numbers are occurrences of individuals in behavioural categories determined from scan samples. t A: association, i.e. within 50 m of member of a group of another species; NA: not in association. $ Values in parentheses are percentage of hourly total which are in association.

II). In addition, this was the only species observed in association with both study groups for more samples than expected by either null model (Table III, Fig. 2). The group of olive colobus monkeys that associated with group E and those forming associations with group W in the absence of other Cercopithecus species appeared to maintain the associations by closely following or tracking the Diana monkeys. I observed no overt interspecific interaction other than several instances of play between small juve-

niles. No other species formed associations of similar duration or frequency with either study group of Diana monkeys. DISCUSSION Many authors have attempted to attribute functional significance to observed interspecific associations without first rejecting the null hypothesis that these associations could be caused by chance encounters between social groups or individuals of

Whitesides: Interspecl@ different species (but see Waser 1982, 1984, 1987 and Cords 1987 for exceptions). No studies on interspecific associations among either fishes or birds have tested this hypothesis. Most authors have failed even to described clearly their criteria for the definition of association. Without quantification of observations, not only is the testing of the null hypothesis impossible, but the rigorous differentiation among competing functional explanations is also precluded. The methods described in this paper can be applied easily to species belonging to taxa other than primates, even those with very different social organizations. The importance of null models in the study of interspecific associations is demonstrated here by the fact that the percentage of samples groups of olive colobus monkeys were in association with Diana group W was less than that for groups of black-and-white colobus monkeys with either study group and less than olive colobus with group E; however, observed associations of olive colobus with Diana monkeys occurred significantly more often than null model predictions while those of all other species did not. Accuracy of Null Models In all 12 cases (six species with each study group of Diana monkeys), both the gas model and the computer simulation model agreed as to which associations occurred more frequently than predicted. Thus, qualitative agreement between the models was high. The major limitation of both null models concerns the accuracy of the field data used to generate predictions. For example, the data on speciesspecific density of groups was derived from islandwide line-transect samples. Not only does some uncertainty exist in the overall density estimates (hence the use of a range of density values during the generation of null model values), but primate densities are probably spatially heterogeneous. Such heterogeneity has at least two closely related causes. The first involves the lack of saturation of the habitat by a species. For some species (e.g. olive colobus monkeys) population density may be low enough so that not all apparently suitable habitat is used. For other species, all appropriate habitat (e,g, old secondary forest) may be included within some social group’s range. However, even for these species habitat heterogeneity may cause nonrandom and non-uniform patterns of habitat use.

associations of C. diana

773

The non-random and non-uniform habitat use found for Diana monkeys indicates that heterogeneity of habitat use also may occur for other species. Such heterogeneity of use will result in both temporal and spatial heterogeneity of the density of groups. Because home range sizes, group densities, and ranging patterns vary among species, patterns of heterogeneity of densities will differ in a speciesspecific manner. The effect of such heterogeneity on null model predictions, therefore, depends both on the focal species chosen and the particular associated species under consideration. Interactions among conspecific groups could affect such heterogeneity by affecting the relative distributions of groups. Whitesides et al. (1988) found that while all seven species on Tiwai Island had coefficients of dispersion less than 1.0 (i.e. repulsed or uniform distribution), the values for only two species (Campbell’s monkeys and blackand-white colobus monkeys) indicated distributions significantly different from random. However, the effect of a highly repulsed distribution of groups on the predicted values generated by the computer simulation model was small. Simulations run using highly clumped distributions of groups (biologically unlikely) also had relatively little effect on the predictions generated. These results indicate the robustness of the computer simulation model to assumptions of the distribution of groups. Monthly Variation of Associations The relatively large monthly fluctuations in the percentage of time the Diana study groups were in association with other species (Fig. 1) is probably a reflection of non-random range use by all species as discussed above. For species whose annual percentage of time in association with the Diana study groups did not exceed that predicted from the null models, a monthly value greater than predicted may indicate aggregation at common resources (Struhsaker 1981) the spatial clumping of resources used by one species with different resources used by another, or merely random fluctuations. The observed temporal fluctuation in associations emphasizes the necessity of long-term field studies in the investigation of interspecific associations. Behavioural Changes in Associations Interspecific associations of both birds and primates examined previously appear significantly

774

Animal

Behaviour,

different from those reported here for Diana monkeys. Neither study group showed alteration of behaviour or change in rate of movement when in association. In contrast, Cords (1987) found that blue monkeys, Cercopithecus mitis, travelled farther per hour when in association with redtails, Cercopithecus ascanius, than when alone. In addition, Terborgh (1983) found that Saguinus imperator and Saguinus fuscicollis seemed to alter their rate of travel when the two species were together. He also found that Saimiri sciureus slowed their rate of travel and Cebus appella increased theirs when in association. Birds frequently alter their behaviour when in mixed-species flocks. Such changes involve decreased rates of scanning for predators (Barnard et al. 1982; Thompson & Barnard 1983; Sullivan 1984; Beveridge & Deag 1987), shifts in sizes or types of prey taken (Barnard & Stephens 1981, 1983; Thompson & Barnard 1984) and alteration of foraging efficiency/energy intake rates (Barnard et al. 1982; Barnard & Stephens 1983). Many of these changes are dependent not only on the size, but also the species composition, of the mixed-species flocks (Barnard et al. 1982; Barnard & Stephens 1983; Beveridge & Deag 1987). Association Between Colobus Monkeys

Diana

Monkeys

and Olive

The only species which was in association with both study groups of Diana monkeys more frequently than expected was olive colobus. However, the lack of alteration in behaviour of Diana monkeys while in association reinforces the observation that the olive colobus-Diana monkey associations are maintained unilaterally by the olive colobus. Because dietary overlap is probably negligible between olive colobus monkeys and any of the Cercopithecus species (no overlap was detected between olive colobus and Diana monkeys: Whitesides, unpublished data; J. Oates, personal communication), the cost to a Cercopithecus species group of proximity of a group of olive colobus is probably minimal. This cost neutrality of the association with respect to Diana monkeys may explain why Diana groups do not actively avoid olive colobus groups, but it leaves unexplained why olive colobus maintain association with Diana groups. The absence of dietary overlap between olive colobus and Diana monkeys, in addition to the

37,5

largely folivorous diet of the olive colobus, eliminates most of the food/foraging-related explanations for the biological significance of these observed associations. Certainly, reduction of duplication of effort, increased insect disturbance, and increased resource detection can all be rejected as possible explanations. The other two proposed foraging advantages (availability of food items otherwise unavailable, and increased intraspecific competitive ability) seem highly unlikely given the olive colobus’ diet and interactions among conspecific groups. Social groups of olive colobus monkeys were typically smaller (2-10 individuals) than those of other diurnal primate species resident on Tiwai. However, olive colobus may reduce the predator detection, avoidance, and/or defence disadvantages of small group size by engaging in interspecific associations. Association with a Cercopithecus species might increase effective group size with respect to predator avoidance, while not increasing the competitive interactions normally correlated with an increase in conspecific group size. Functional

Significance

of Associations

Some authors have attempted to assign a single evolutionary cause not only to one type of association, but to the entire phenomenon of interspecific association. Other authors have realized that associations involving different species even within the same geographical area may have different causes (e.g. Saimiri sciureus with Cebus species versus Saguinus imperator with Saguinus fuscicollis in Peru; Terborgh 1983). Still others have even suggested that some associations may have multiple causes (e.g. Struhsaker 1981 and Cords 1987 for blue monkeys and redtails; Barnard et al. 1982 and Thompson & Barnard 1983 for lapwings, plovers and gulls). To date, observations indicate that probably no single evolutionary cause explains the general phenomenon of interspecific associations in primates, much less those involving other taxa; each case much be assessed individually. This does not mean that the other instances of interspecific even those involving taxonomic associations, orders or classes of organisms different from those under consideration, might not provide important insights into the evolutionary causality of observed associations, only that they need not. In addition, we must not automatically assume that observed associations are the result of some evolutionary

Whitesides:

Interspecific

cause; this assumption must be tested carefully before we attempt to assign significance or function to such associations. ACKNOWLEDGMENTS

I thank John Oates and Steve Green for their advice and assistance during all stages of this research. G. L. Dasilva, A. G. Davies, R. P. Kluberdanz and J. F. Oates provided both personal insights and access to their unpublished data. I owe special thanks to P. T. White, N. Wakeham, R. Wakeham, the Paramount Chief of Barri, the people of Kambama and the University of Sierra Leone for assistance in Sierra Leone. I also thank R. J. Breitwisch, M. Cords, T. H. Fleming, S. M. Green, D. P. Janos, C. M. Nelson, J. F. Oates, C. T. Snowdon, K. D. Waddington and P. M. Waser for comments on various versions of the manuscript. D. S. Houston and W. G. LeBlanc provided assistance with computer analysis, and J. T. Vance gave important technical help with the computer simulations. The work was supported by NSF grant No. BNS 8120206 to J. F. Oates and S. M. Green and by a Robert E. Maytag Fellowship. This is contribution No. 301 in Behavior, Ecology and Tropical Biology from the Department of Biology, University of Miami. REFERENCES Altmann, S. A. & Altmann, J. 1970. Baboon Ecology. Chicago: University of Chicago Press. Barlow, G. W. 1974. Extraspecific imposition of social grouping among surgeon-fishes (Pisces: Acanthuridae). .I. Zoo/. Lond., 174, 333-340. Barnard, C. J. & Stephens, H. 1981. Prey size selection by lapwings in lapwing/gull associations. Behaviour, 77,l~ 22. Barnard, C. J. & Stephens, H. 1983. Costs and benefits of single and mixed species flocking in fieldfares (Turdus pilaris) and redwings (T. iliacus). Behaviour, 84, 91123. Barnard, C. J., Thompson, D. B. A. & Stephens, H. 1982. Time budgets, feeding efficiency and flock dynamics in mixed species flocks of lapwings, golden plovers and gulls. Behaviour, 80, 4469. Bates, H. W. 1864. The Naturalist on the River Amazon. London: John Murray. Belt, T. 1874. The Naturalist in Nicaragua. London: John Murray. Berner, T. 0. & Grubb, T. C., Jr. 1985. An experimental analysis of mixed-species flocking in birds of deciduous woodland. Ecology, 66, 1229-1236. Bernstein, I. S. 1967. Intertaxa association in a Malayan primate community. Folia primatol., 7, 198-207.

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