Document Sample
					Journal of Mammalogy, 83(1):159–166, 2002


                                 LESLIE A. CORNICK*   AND   HAL MARKOWITZ

          Department of Biology, San Francisco State University, 1600 Holloway Avenue,
                                     San Francisco, CA 94132
   Present address of LAC: Institute of Marine Science, School of Fisheries and Ocean Sciences,
                           University of Alaska, Fairbanks, AK 99775

The majority of the literature describing howling monkeys (Cebidae) has focused on only
2 of 6 species in the genus. These studies have revealed differences in behavior between
species and differences within species at different locations. One study has been published
describing the vocal patterns of the black howler monkey (Alouatta pigra). This species
appears to differ markedly from previously described Alouatta. In an effort to further dis-
tinguish A. pigra from its congeners, we observed the vocal patterns of an additional
population of black howler monkeys. This population exhibited a bimodal calling pattern
similar to that previously described for A. pigra, but absent in all but one (A. fusca) of the
other species in the genus. The bimodal pattern was evident in both the rainy and dry
seasons, with peaks in the morning and afternoon. Midday and afternoon calling were
significantly reduced in the dry season. We also made a detailed comparison between both
populations to examine the function of the afternoon peak. Contrary to the results of the
previous study, we conclude that there is insufficient evidence to describe either of these
populations as territorial.

Key words:      Alouatta pigra, black howler monkey, howling monkeys, primates, vocalizations

   Neotropical primates exhibit a vast array            complete absence of homologs of all of the
of vocal behaviors within a variety of social           high-pitched patterns of other platyrrhine
contexts, which reflects the diversity of                species. These patterns are present in the
their morphology and social organization.               closest living genera of Alouatta, Aotus and
The howler monkey (Alouatta: Cebidae) is                Callicebus, so it is likely that they were also
no exception, and appears to differ in many             present in the ancestors of Alouatta and
aspects of its vocal behavior from its New              were lost in subsequent evolution (Moyni-
World cousins (Moynihan 1976). Specifi-                  han 1967).
cally, the enlarged hyoid apparatus of howl-               The preponderance of the literature on
er monkeys imposes an upper frequency                   howler monkey vocalizations describes 2
limit on their loud calls. This is an excep-            species in the genus—Alouatta palliata
tion to the typical vocal repertoire of plat-           (Baldwin and Baldwin 1976; Carpenter
yrrhine monkeys, which in other genera in-
                                                        1934; Chivers 1969) and A. seniculus (Bra-
cludes a series of high- and intermediate-
                                                        za et al. 1981; Drubbel and Gautier 1993;
pitched sounds that are emitted to express
                                                        Schon Ybarra 1986; Sekulic 1982a, 1982b,
low-intensity hostility, sexual signals, and
                                                        1983). Only 1 study has been published de-
distress (Moynihan 1967). Howler monkeys
deviate from this repertory and show a                  scribing the vocal patterns of the black
                                                        howler monkey, sometimes referred to as
* Correspondent: lesliec@sfos.uaf.edu                   the Mexican black howler monkey (A. pi-

160                               JOURNAL OF MAMMALOGY                              Vol. 83, No. 1

gra—Horwich and Gebhard 1983), which             is a perceptible incursion into a consistently
suggests patterns that differ markedly from      shifting area of about 150 yards surround-
those described for the other 2 species.         ing a group, which is defined as ‘‘group
   Horwich and Gebhard (1983) described          space.’’ Altmann (1959) described A. pal-
the seasonal variation in daily vocalization     liata as territorial within a subportion of the
patterns of a population of A. pigra at the      home range but did not report any behav-
Community Baboon Sanctuary in Bermu-             iors (e.g., active patrolling) that have been
dian Landing, Belize. Vocalizations dis-         shown as necessary for territorial defense
played a distinct bimodality in the dry sea-     (Grant et al. 1992; Mitani and Rodman
son (early morning and late afternoon            1979).
peaks) and a dampened bimodality in the             The purpose of this study was to char-
rainy season (morning and afternoon peaks        acterize the daily vocal patterns of an ad-
reduced, with increased midday calling).         ditional population of A. pigra, to better
Within the genus, this bimodal pattern has       distinguish them from other species in the
been reported only for A. fusca (Mendes          genus, and elucidate further the evolution-
1985; Young 1983) and anecdotally for A.         ary significance of the variation across plat-
seniculus (Braza et al. 1981).                   yrrhine genera. Specific objectives were to
   Based on their findings, Horwich and           determine the mean duration of vocal bouts,
Gebhard (1983) described A. pigra at this        to assess diurnal and seasonal variation in
location as territorial. They suggested that     vocal patterns, and to determine the degree
in howler monkeys and colobine monkeys,          of correlation between vocal bouts and ter-
which produce long-range calls, the bimod-       ritorial defense.
al pattern of howling typically occurs in
species that exhibit territorial defense. Ad-             MATERIALS    AND   METHODS
ditionally, they observed 3 incidents of ad-        Study area.—The study was conducted in the
jacent troops being actively chased across       Lamanai archaeological reserve, a popular tour-
home range boundaries, followed by in-           ist destination, in the Orange Walk District of
creased howling by both troops. Finally,         Belize. Lamanai (17 46 N, 88 39 W) is estimat-
they reported a high percentage of vocali-       ed to be 3.76 km2 in area (Gavazzi 1995). It has
zations occurring at or near home range          a concentrated area of excavated Spanish, Brit-
boundaries.                                      ish, and Mayan ruins in the southern portion and
                                                 unexcavated mounds enveloped by secondary
   There is a lack of consensus as to the
                                                 semideciduous forest in the northern portion.
existence of territoriality in Alouatta. Howl-   The southern portion also consists of secondary
er monkeys do not appear to be strictly ter-     semideciduous forest, with concentrations of
ritorial, as home ranges tend to have a great    preferred howler food trees (Ficus, Brosimum
deal of overlap. However, it is clear that       alicastrum) in and around excavated areas. La-
neighboring troops avoid using areas of          manai is bounded to the east by the New River
overlap simultaneously. Carpenter (1965)         Lagoon, to the west by milpas (plantations) and
has argued that they merely defend their         forest, to the north by forest and swamp, and to
current location. This is supported by Chiv-     the south by the village of Indian Church. Daily
ers (1969), who noted that vocal confron-        temperature ranges from 18 to 35 C, with a
tations by A. palliata can occur in any part     mean of 27 C (Lambert and Arnason 1978).
                                                 Mean annual precipitation is about 1,500 mm,
of the home range, rather than only at
                                                 with the primary wet season from June through
boundaries, and by Klein (1974), who de-         November (Gavazzi 1995).
termined that the considerable overlap in           A population of about 22–25 troops of A. pi-
range patterns between adjacent groups is        gra resides at Lamanai. Troops range in size
ephemeral in time and space. Klein (1974)        from 2 to 12 animals. Density was estimated to
suggested that what appears to provoke an        be 45.21 animals/km2. This population has been
immediately mutual active vocal response         the subject of an ongoing behavioral ecology
February 2002         CORNICK AND MARKOWITZ—CALLS OF BLACK HOWLER MONKEY                             161

study since 1993. A. pigra in the southern por-       sex and age class of vocalizing monkey(s), prox-
tion of the reserve, which is the area of highest     imity to other troops, and vocal response to ob-
visitor activity, exhibits behaviors that suggest a   server.
strong level of habituation to humans (e.g., lack        Age classes were estimated by the size of the
of apparent disturbance of feeding, resting and       individual in relation to that of an adult female,
grooming, lack of troop movement upon en-             as originally defined by Carpenter (1934), and
counter, and juvenile animals coming to the           follows the same criteria as reported by previous
ground to investigate researchers). Conversely,       researchers on this project (Gavazzi 1995). In-
few people enter the northern portion of the re-      fants and juveniles do not typically emit loud
serve, and in that area A. pigra does not appear      calls and were therefore not examined in this
to be habituated to humans, as evidenced by           study.
movement into higher areas in the canopy and             At certain times during each field season vol-
increased alertness upon approach.                    unteer research assistants were available and
   Research protocol.—We collected data during        data collection methods varied slightly. When
2 field seasons, encompassing 1 rainy season           assistants were available, research sessions var-
(September–November 1996) and 1 dry season            ied in length and may not have started and ended
(January–April 1997). We walked transects on          at precise times, because of constraints of meal-
the existing trail system from 0600 to 1200 h         times, etc. At the beginning of each session, start
and from 1200 to 1800 h on alternating days, 6        and end times of sessions and transects were re-
days a week. We surveyed the southern and             corded. The same data as mentioned earlier were
northern portions of the reserve every 2 days,        collected with respect to vocalizations, and
so that the 12-h diurnal period was covered for       troops were located whenever possible. When
each portion of the reserve.                          troops were located, the researcher and assis-
   We noted temperature, humidity, and cloud          tants remained with the troop for up to 1 h, col-
cover (sunny, partly cloudy, cloudy, and rainy)       lecting detailed behavioral data in 5-min scan
at the beginning of each session. We recorded         samples for other portions of the study (see Gav-
the following information on data sheets for all      azzi 1995). A total of 397 h was spent in the
loud calls heard during transects: start time, end    field in the rainy season and 417 h in the dry
time, observer location, compass bearing from         season, with 201 and 301 total vocal bouts doc-
observer to vocalization (to determine the ap-        umented, respectively.
proximate location of the howling monkey or
troop within the reserve), and approximate rel-                      Statistical Analysis
ative distance (close, medium, far), with the as-       Calling rate.—We assigned vocal bouts to an
sumed maximum distance within the 1-km range          hour of the day by the midpoint between the
of howler monkey vocalizations (Carpenter             beginning and ending time of the bout. We as-
1965). Distance approximations were based on          signed bouts with an unknown ending time (e.g.,
the relative intensity of vocalization (Gavazzi       ending time was not recorded because of ob-
1995).                                                server error or the vocalizing troop moving out
   We examined only the loud calls, which are         of range) to the hour in which they began so
the primary means of communication in Alouat-         that they could be counted. We then calculated
ta (Carpenter 1965). For a complete description       the calling rate for each hour by dividing the
of the vocal repertoire of Alouatta and a sono-       number of vocal bouts in a given hour by the
gram of A. pigra, see Whitehead (1995). A vocal       amount of time spent in the field during that
bout was defined as continuous howling, with no        hour, for each field session and each season in-
interruptions lasting longer than 30 s. Each bout     dependently. To ensure that observations could
may have contained as few as 1 or as many as          be considered independent, we calculated the
several individual loud calls, sometimes inter-       hourly mean calling rate by taking the mean for
spersed with other types of vocalizations (e.g.,      each hour corrected by hours of effort, within
barks, grunts—Carpenter 1934). Duration of in-        each season. We pooled the hours of the day into
dividual loud calls was not measured. Bouts last-     3 categories (morning: 0600–0900 h, midday:
ing less than 1 min were recorded as beginning        0900–1400 h, and afternoon: 1400–1800 h)
and ending in the same minute. When we were           based upon the graphical examination of the
able to locate the vocalizing troop, we recorded      data. To determine whether calling rate varied
162                                  JOURNAL OF MAMMALOGY                                 Vol. 83, No. 1

significantly among the 3 time periods, we made
pairwise comparisons of the weighted means
(Cimeani) for each time period using the F dis-
tribution. F values were calculated for each
comparison by F             [(C1)(mean1)       (C2)
(mean2)]2/[(C1)2/n1    (C2)2/n2](MSE) with 1 and
(n1    n2)     2 degrees of freedom, where C1
1 and C2         1 for pairwise comparisons, and
MSE       within cell variation from the primary
analysis of variance. We calculated 3 compari-
sons—morning versus midday, midday versus
afternoon, and morning versus afternoon. Con-
trasts were planned a priori. Alpha levels for
each contrast ( c) were calculated using the Si-
dak inequality (Jones 1984) and set at P
0.035. We made 7 pairwise contrasts in the same
manner to determine the effects of cloud cover
on calling rate, with c set at P 0.017. Finally,
we made 3 comparisons to determine if calling
rates for each time period varied between the
rainy season and the dry season, with c set at
P     0.035.
   Duration of bouts.—We determined bout du-
ration by subtracting beginning time from end-
ing time. Bouts beginning and ending in the
same min were defined as lasting 30 s. Bouts
with an unknown ending time were not used to
calculate the mean duration. One aberrant case           FIG. 1.—Calling rate and bout duration in Al-
(114 min) was omitted from the autumn 1996            ouatta pigra at Lamanai, Belize, for rainy versus
data set, as it was not representative of a typical   dry seasons. a) Mean number of bouts/h for 3
bout. Unfortunately the calling troop(s) were not     daily time periods in each season and b) mean
located visually to allow this bout to be exam-       duration of vocal bouts for 3 daily time periods
ined within its social context. We calculated the     during each season. Autumn is the rainy season,
mean duration for each hour by the same method        spring is the dry season. Morning 0600–0900
as for calling rate. Differences across the 3 time    h; midday      0900–1400 h; afternoon      1400–
periods, effects of cloud cover on bout duration,     1800 h.
and differences in bout duration between sea-
sons were also examined, as earlier.                  were significantly reduced compared with
                                                      that of the rainy season (F     24.53, d.f.
                    RESULTS                           1, 293, P     0.0001 and F      11.80, d.f.
  Calling rate.—A distinct bimodal calling            1, 87, P 0.0009, respectively), and morn-
pattern was evident in both rainy (autumn             ing and afternoon peaks were significantly
1996) and dry (spring 1997) seasons, with             higher than midday calling rate (F      7.46,
peaks in morning and afternoon (Fig. 1a).             d.f.    1, 166, P    0.007 and F       21.10,
Morning calling rate was nearly the same              d.f.    1, 153, P     0.0001, respectively).
for both rainy and dry seasons. During the            The overall calling rate (mean      SE) was
rainy season, morning and afternoon calling           1.73     0.20 bouts/h in the rainy season (n
rates were significantly higher than midday                201 bouts) and 1.14      0.11 bouts/h in
calling rates (F   7.46, d.f.  1, 166, P              the dry season (n 301 bouts). Cloud cov-
0.007 and F      21.10, d.f.    1, 15, P              er had no effect on calling rate in either
0.0001, respectively). During the dry sea-            season. Temperature and humidity effects
son, midday and afternoon calling rates               were inconclusive.
February 2002      CORNICK AND MARKOWITZ—CALLS OF BLACK HOWLER MONKEY                     163

                                               and Bermudian Landing is typical across
                                               the genus and is consistent with long resting
                                               periods following morning foraging bouts
                                               (Milton 1980).
                                                  In other aspects of the diurnal calling pat-
                                               tern, however, there is substantial variation
                                               within the genus (Table 1). Both popula-
                                               tions of A. pigra that have been studied thus
                                               far (Lamanai—present study; Bermudian
                                               Landing, Belize—Horwich and Gebhard
                                               1983) have an afternoon peak in howling,
                                               which is reported for 2 other congeners—
  FIG. 2.—Frequency of bout duration in Al-    A. seniculus and A. fusca. A distinct after-
ouatta pigra at Lamanai, Belize. Duration      noon peak occurring throughout the year
ranged from 1 min to 55 min.                   has been observed in 1 population of A.
                                               seniculus (Braza et al. 1981), although
                                               small afternoon peaks were observed in the
   Duration of bouts.—Duration of vocal        dry season in 2 others (Drubbel and Gautier
bouts (mean      SE, 10.5    0.73 min) did     1993; Sekulic 1982a). An afternoon peak is
not vary significantly with time of day in      consistently reported for A. fusca (Mendes
either season (Fig. 1b). However, the range    1985; Young 1983).
of bout lengths was extensive—from 1              According to Horwich and Gebhard
min to as long as 39 min in the autumn and     (1983), the afternoon peak is indicative of
to 55 min in the spring. For both seasons      territoriality. However, this conclusion is
combined, 91% of the bouts lasted 20 min       not supported in the literature or by findings
(Fig. 2). Cloud cover had no effect on bout    from Lamanai. Historically, neither A. sen-
duration in either season.                     iculus nor A. palliata has been described as
                                               territorial (but see Altmann 1959). Nor is
                DISCUSSION                     A. fusca considered territorial by current re-
   Calling rate.—The early morning peak        searchers (S. L. Mendes, in litt.). Gavazzi
and low midday calling rate exhibited by A.    (1995) did not consider A. pigra at Lamanai
pigra at Lamanai is consistently reported      to be territorial because of the degree of
for all other members of Alouatta and for      overlap in home ranges. This conclusion is
other Cebid monkeys (Carpenter 1940; Ull-      supported both by the preponderance of lit-
rich 1961). The early morning peak has         erature describing primate ranging patterns
been described as a dawn chorus, during        and by our observations during the present
which nearly all troops in relatively close    study. Mitani and Rodman (1979) deter-
proximity howl simultaneously, often for       mined that primates will defend a home
lengthy periods (Baldwin and Baldwin           range only if their foraging regime allows
1976; Carpenter 1934; Chivers 1969; Hor-       them to do so. If costs of defending re-
wich and Gebhard 1983; Sekulic 1982a). It      sources exceed benefits gained by active
is generally accepted that this serves as a    patrolling required defending them, then
spacing mechanism to minimize the likeli-      territorial defense behavior will not evolve
hood of encounters between neighboring         (Brown 1964). In a general study of home
troops during the course of the day, partic-   range defense, Grant et al. (1992) found
ularly in areas where the home ranges over-    that primates who are primary folivores,
lap (Carpenter 1934, 1965; Chivers 1969;       such as A. pigra, do not defend their home
Sekulic 1982a). The reduced rate of midday     range, as their lack of mobility makes the
calling throughout the year at both Lamanai    cost of defense prohibitive. Grant et al.
164                                                                                                                                       JOURNAL OF MAMMALOGY                                                                                                                                                             Vol. 83, No. 1

                                                                                                                                                                                                                                                                                          (1992) also noted that leaves are not a de-
                                                                        Density (ind/km2)                                                                                                                                                                                                 pressible food resource, making the benefits
                                                                                                                                                                                                                                                                                          of excluding competitors low, hence the ob-

                                                                                                                                                                                                                                                                                          served overlap in home ranges throughout



                                                                                                                                                                                                                                                                                          the genus. We saw no evidence of active
                                                                                                                                                                                                                                                                                          patrolling during over 800 h in the field.
                                                                                                                                                                                                                                                                                          Rather, troops often spent several hours
                                                                                                                                                                                                                                                                                          sleeping in the same tree, without even a
                                                                                                                                                                                                                                                                                          single animal alert to intruders.
                                                                                                                                                                                                                                                                                             Milton (1980) suggested that ranging
                                                                        Afternoon peak

                                                                                                                                                                                                                                                                                          patterns of howler monkeys could be best
                                                                                                                                                                                                                                                                                          described as the semiexclusive use of core





                                                                                                                                                                                                                                                                                          areas within the home range, given the in-
  TABLE 1.—Calling patterns and population density in genus Alouatta.

                                                                                                                                                    Both studies reported slight increases in afternoon calling during the dry season, not considered an afternoon peak as defined here.   ability to successfully defend an entire
                                                                                                                                                                                                                                                                                          home range against conspecifics, particular-
                                                                                                                                                                                                                                                                                          ly in areas of overlap. Howling, particularly
                                                                                                                                                                                                                                                                                          the dawn chorus and the howls upon first
                                                                                                                                                                                                                                                                                          arriving in a food tree, allows the monkeys
                                                                        Midday calling

                                                                                                                                                                                                                                                                                          to maximize the benefits of semiexclusive




                                                                                                                                                                                                                                                                                          use of an area without incurring costs of
                                                                                                                                                                                                                                                                                          territorial defense (Milton 1980). No other
                                                                                                                                                                                                                                                                                          function for an afternoon peak in howling
                                                                                                                                                                                                                                                                                          has been suggested, and we were unable to
                                                                                                                                                                                                                                                                                          correlate this behavior with any other ob-
                                                                                                                                                                                                                                                                                          served behavior when howling troops were
                                                                        Dawn chorus

                                                                                                                                                                                                                                                                                          located. Further examination of this phe-
                                                                                                                                                                                                                                                                                          nomenon is warranted in those species for




                                                                                                                                                                                                                                                                                          which it has been reported.
                                                                                                                                                                                                                                                                                             The overall roaring rate (mean          SE,
                                                                                                                                                                                                                                                                                          1.37      0.11 bouts/h) was slightly lower
                                                                                                                                                                                                                                                                                          than that found by Horwich and Gebhard
                                                                                                                                                                                                                                                                                          (1983) at Bermudian Landing (1.78 bouts/
                                                                                               pigra, Bermudian Landing, Belize (Horwich and Geb-

                                                                                                                                                                                                                                                                                          h), and our population differed strikingly
                                                                                                                                                                                                                                                                                          from the Bermudian Landing population in
                                                                                               palliata, Barro Colorado Island (Carpenter 1965)
                                                                                               palliata, Barro Colorado Island (Chivers 1969)

                                                                                               seniculus, Guyana (Drubbel and Gautier 1993)
                                                                                               palliata, Panama (Baldwin and Baldwin 1972)

                                                                                                                                                                                                                                                                                          seasonal differences in morning and after-
                                                                                                                                                                                                                                                                                          noon calling rates. At Bermudian Landing,
                                                                                               seniculus, Venezuela (Braza et al. 1981)

                                                                                                                                                                                                                                                                                          the morning and afternoon peaks were
                                                                                               seniculus, Venezuela (Sekulic 1982a)

                                                                                                                                                    157 individuals utilizing 37 acres (15 ha).

                                                                                                                                                                                                                                                                                          greater during the dry season (Horwich and
                                                                                                                                                                                                                                                                                          Gebhard 1983). At Lamanai, the reverse
                                                                                            A. pigra, Lamanai (Gavazzi 1995)
                                                                                            A. pigra, Lamanai (present study)

                                                                                                                                                                                                                                                                                          was true, with morning and afternoon peaks
                                                                                               fusca, Brazil (Mendes 1985)
                                                                                               fusca, Brazil (Young 1983)

                                                                                                                                                                                                                                                                                          being greater in the rainy season. This may
                                                                                                                                                                                                                                                                                          be a result of differing data collection and
                                                                                                                                                                                                                                                                                          analysis methods between the two studies,
                                                                                                                                                                                                                                                                                          habitat differences between the 2 sites, and
                                                                                                                                                                                                                                                                                          or differences in the seasonal activity of hu-
                                                                                              hard 1983)

                                                                                                                                                                                                                                                                                          mans in the area.
                                                                                                                                                                                                                                                                                            Duration of bouts.—The duration of vo-
                                                                                                                                                                                                                                                                                          cal bouts did not vary significantly with

                                                                                                                                                                                                                                                                                          time of day, season, or cloud cover. Hor-
February 2002         CORNICK AND MARKOWITZ—CALLS OF BLACK HOWLER MONKEY                                 165

wich and Gebhard (1983) did not measure               Support was provided by Oceanic Society Ex-
duration of calling bouts or individual loud          peditions, a National Institutes of Health Field
calls at Bermudian Landing, so no compa-              Training Grant and a Graduate Assistance in Ar-
rable data are available for A. pigra. Studies        eas of National Need Fellowship.
conducted on A. palliata (Altmann 1959;
                                                                      LITERATURE CITED
Baldwin and Baldwin 1976; Carpenter
1934; Chivers 1969) and A. seniculus                  ALTMANN, S. A. 1959. Field observations on a howling
                                                        monkey society. Journal of Mammalogy 40:317–
(Drubbel and Gautier 1993; Schon Ybarra                 330.
1986; Sekulic 1982a; Sekulic and Chivers              BALDWIN, J. D., AND J. I. BALDWIN. 1976. Vocalizations
1986) typically examined characteristics of             of howler monkeys (Alouatta palliata) in western
                                                        Panama. Folia Primatologica 26:81–108.
individual vocalizations, rather than those           BRAZA, F., F. ALVAREZ, AND T. AZCARATE. 1981. Be-
of entire calling bouts, with the exception             havior of the red howler monkey (Alouatta senicu-
of Chivers (1969).                                      lus) in the Llanos of Venezuela. Primates 22:459–
   The range of duration for all vocal bouts          BROWN, J. L. 1964. The evolution of diversity in avian
between Chivers (1969) and the present                  territorial systems. Wilson Bulletin 76:160–169.
study at Lamanai are comparable (9–62                 CARPENTER, C. R. 1934. A field study of the behavior
                                                        and social relations of howling monkeys (Alouatta
min and 1–55 min, respectively). Mean du-               palliata). Pp. 3–92 in Naturalistic behavior of non-
ration in Chivers’ study (22.6 min), how-               human primates (C. R. Carpenter, ed.). Pennsylvania
ever, was twice that of the present study               State University Press, University Park.
                                                      CARPENTER, C. R. 1940. A field study in Siam of the
(10.5 min). Density at Barro Colorado Is-               behavior and social relations of the gibbon (Hylo-
land at the time of Chivers’ study was al-              bates lar). Comparative Psychological Monographs
most double that of density at Lamanai (Ta-             16:1–212.
                                                      CARPENTER, C. R. 1965. The howler monkeys of Barro
ble 1), indicating that bout duration may in-           Colorado Island. Pp. 250–291 in Primate behavior:
crease with population density.                         field studies of monkeys and apes (I. DeVore, ed.).
   The variation in vocal behaviors across              Holt, Rinehart, and Winston, New York.
                                                      CHIVERS, D. J. 1969. On the daily behavior and spacing
the genus and between populations of A.                 of howling monkey groups. Folia Primatologica 10:
pigra warrants continued examination. It                48–102.
was not until 1970 that A. pigra was given            DRUBBEL, R. V., AND J. P. GAUTIER. 1993. On the oc-
                                                        currence of nocturnal and diurnal loud calls, differ-
specific recognition. A more complete un-                ing in structure and duration, in red howler monkeys
derstanding of variation within and between             (Alouatta seniculus) of French Guyana. Folia Pri-
species of Alouatta is needed to clarify evo-           matologica 60:195–209.
                                                      GAVAZZI, A. J. 1995. Ecology of the black howler
lutionary relationships within the genus and            monkey (Alouatta pigra) at Lamanai, Belize. M.A.
the way these threatened primates are re-               thesis, San Francisco State University, San Francis-
sponding to continuing habitat fragmenta-               co, California.
                                                      GRANT, J. W. A., C. A. CHAPMAN, AND K. S. RICHARD-
tion and human encroachment.                            SON. 1992. Defended versus undefended home range
                                                        size of carnivores, ungulates and primates. Behav-
              ACKNOWLEDGMENTS                           ioral Ecology and Sociobiology 31:149–161.
                                                      HORWICH, R. H., AND K. GEBHARD. 1983. Roaring
   We wish to thank the Government of Belize
                                                        rhythms in black howler monkeys (Alouatta pigra)
and the Lamanai Archaeological Reserve for              in Central America. Primates 24:290–296.
permission to conduct this study. We also thank       JONES, D. 1984. The use, misuse, and role of multiple-
the Howells family and the Lamanai Outpost              comparison procedures in ecological and agricultur-
Lodge for their support and accommodations,             al entomology. Environmental Entomology 13:635–
and volunteer research assistants for their enthu-    KLEIN, L. L. 1974. Agonistic behavior in neotropical
siasm and willingness to spend long hours in the        primates. Pp 77–122 in Primate aggression, territo-
field. We thank A. Gavazzi and the Markowitz             riality, and xenophobia (R. L. Hooloway, ed.). Ac-
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