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International Journal of Primatology, Vol. 24, No. 4, August 2003 ( C© 2003)

Foraging Behavior and Activity Patternsof Alouatta caraya in the NortheasternArgentinean Flooded Forest

Susana P. Bravo1 and Ana Sallenave1

Received April 12, 2002; revision October 29, 2002; accepted December 3, 2002

Howling monkeys (Alouatta spp.) are colonizer species, showing a plasticityin behavior that allows them to inhabit different sorts of forests. There is aseries of hypotheses relating demography to behavioral and ecological char-acteristics of howlers: (1) as howler density increases, home range size willdecrease; (2) howler groups occupying small home ranges will have a highproportion of leaves in their diet; and, (3) the proportion of mature leaves inthe diet is negatively correlated with group daily travel distance. To test hy-potheses about howler diet and ranging pattern in relation to food resources,we studied the foraging ecology and general activity patterns of 2 groups ofblack howlers (Alouatta caraya) inhabiting in flooded forest of Parana River(Argentina), the habitat with the highest density recorded for Alouatta. Wefound, in addition to the highest densities, also the smallest home ranges forAlouatta (Group I: 1.7 ha and Group II: 2.2 ha). However, diet was not dom-inated by leaves, and high quality items—flowers, fruits, new leaves—were ahigh proportion of the diet all year. Also, daily travel distance is not correlatedwith the proportion of mature leaves in the diet, but is positively correlatedwith the number of group confrontations. Finally, we propose a model inte-grating and interpreting our results as a function of the spatial and temporaldistribution of high quality food resources in the Argentinean flooded forest.

KEY WORDS: Black howler; diet; behavior; home range; Parana river.

1Museo Argentino de Ciencias Naturales (Conicet), Av. Angel Gallardo 470, 1405 BuenosAires, Argentina. e-mail: sbravo@mastoz.edu.ar.

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INTRODUCTION

Howlers (Alouatta spp.) are folivorous-frugivorous Neotropical pri-mates, which live in unimale and multimale groups (Crockett and Eisenberg,1987). They are considered colonizers, showing a plasticity in behavior thatallows them to inhabit different sorts of forests (Eisenberg et al., 1972).Howlers commonly dwell in middle and upper strata of the forest, though insome environments they also us the lower stratum (Crockett and Eisenberg,1987). Daily, howlers use small areas of their annual home ranges (Chapman,1988; Estrada, 1984; Julliot, 1992; Lucena Mendes, 1989; Milton, 1980;Stoner, 1996; Zunino, 1986), some with high frequency—core areas—Ingeneral, they are related to the distribution of feeding resources.

While howler populations may be influenced by factors such as diseaseor predation, food availability is often assumed to be the critical factor deter-mining their abundance (Chapman et al., 1999; Milton, 1996). Thus, despitethe fact that some primate populations may be severely impacted by hunt-ing, in the absence of human predation, it is reasonable to assume that foodresources may limit howlers densities (Balcomb et al., 2000). Several authorsconcluded that the most important factor determining the habitat quality isthe density of the food species most commonly consumed by howlers (Gaulinet al., 1980; Stoner, 1996).

Comparative howler studies across different sites have shown that thespatial and temporal distribution of resources can influence daily ranges,home range size, and the intensity with which spaces are utilized throughtime (Chapman, 1988; Milton, 1980). There is a series of hypothesis interre-lating these factors. Crocket and Eisenberg (1987) showed that home rangesize is negatively correlated with howler population density (Hypothesis 1).Accordingly, this relationship may not be simply a function of higher fooddensities, permitting the same number of howlers to survive in a small area,it can also be a consequence of the demographic process the populationis under going. Accordingly, at low densities howlers use a bigger areathan they need to survive because the population has not reached carryingcapacity.

Another explanation given for small home ranges, particularly forhowlers, it is that they are associated with a diet dominated by leaves(Estrada, 1984; Julliot and Sabatier, 1993) (Hypothesis 2), assuming auniform distribution of leaves in tropical forest.

Finally, Milton (1980) has suggested that howlers are travel minimizers,energetically constrained because the foliage part of their diet is low in readyenergy (Hypothesis 3). Derived from this hypothesis is the prediction thatthe percentage of leaves in the diet would have to be negatively correlatedwith daily traveled distance.

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The density of black howler in flooded forest of Parana River (Argentina)is higher than densities reported for the other species of Alouatta (Crockett,1998). For example, in the old growing forest of Brasilera Island, Kowaleski(2000) recorded a density of 425 ind/km2. According to the 3 hypotheses andconsidering the high howler density on Brasilera Island, one expects to findblack howler groups using small home ranges, living on a diet dominated bymature leaves, and traveling daily distances negatively correlated with theamount of mature leaves in the diet.

To test these hypotheses and to determine which factors are contribut-ing to high howler densities on Brasilera Island, we studied the floristiccomposition, structure and phenology of the flooded forest and the dietarycomposition, behavior and ranging patterns of 2 groups of black howlersthat inhabit Parana River Islands of Argentina.

METHODS

Study Area

The climate is subtropical with a mean annual temperature of 21.5◦C,and an annual thermal amplitude of 12.2◦C. The annual average precipitationis 1230 mm, rainfall is not strictly seasonal, but monthly averages decreaseduring June–August.

Parana’s hydrological regime is irregular with rains occurring some-where in the watershed and causing periodic floods≤3 times per year. Floodshave variable intensity, covering forest soils with a few cm or several mof water, Duration is also variable, lasting from a few days to several mo(Carignan and Neiff, 1992). Extraordinary floods can last >1 yr, killing ahigh proportion of trees: The last one occurred in 1982–1983 (Neiff, 1999).After an extraordinary flood, new colonization of the flora and fauna inthe islands occurs (Rumiz et al., 1986). Periodic and extraordinary floodsproduce a continuous deposition of sediments and nutrients, favoring vege-tation with a high recovery and resistance to periodic inundation (Eskucheand Fontana 1996).

We studied howlers on Brasilera Island, next to the confluence of Paranaand Paraguay Rivers in Northeastern Argentina (Fig. 1a). The island has asurface of ca. 280 ha; 141 ha are covered with forest. Vegetation followsa typical distribution pattern, forming forests in relatively narrow parallelstrips on elevated old riverbanks—albardones—and grasslands and lagoonsamong forests strips (Fig. 1b). Similarly, different kinds of forests may berecognized depending on the albardon age, there is a more complex one inthe center of island. Our study troops lived in the more complex and old

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Fig. 1. (a) Location of Brasilera Island in South America. (b) Flood forest patches in BrasileraIsland. (c) Black howler groups’ territories, confrontations sites and principal sleeping sites.

forest in the center of the island (Fig. 1b). There is no permanent humanresidence on the island.

Floristic Composition, Vegetation Structure and Phenology

We censused all trees ≥5 cm in diameter at breast height (DBH) in25 plots of 20× 20 m, along the albardon. We recorded tree species, height,DBH and basal area of each tree.

To obtain information about the resource abundance throughout theyear, we performed a phenological analysis for all arboreal species. Everymonth, we selected at random 10 trees from each species, and monitoredthe presence of mature leaves, new leaves, flowers and fruits. We rankedabundance of each phenophase in a relative scale from 0 to 4 (phenolog-ical value), where in 0 is the absence of a particular phenophase and 4 is

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its complete presence. We averaged the individual phenological values foreach species to obtain a Phenological Index of each species (PIsp) for eachmonth and for each phenophase. We quantified monthly variation of eachphenophase (TPIsp) considering all species consumed by black howlers as:

TPIsp = (∑

PIsp) × 100/N,

N = number of species considered.

Foraging Behavior and Activity Patterns

We collected data from 2 groups of black howlers. Group composi-tions at the beginning of the study was: Group I, 16 individuals, 2 adult and1 subadult males, 5 adult females, 5 juveniles (4 females, 1 male) and 3 infants;Group II, 21 individuals, 2 adult and 1 subadult males, 6 adult and 1 subadultfemales, 7 juveniles (4 females, 3 males) and 4 infants. We distinguishedthe individuals by facial features (scars and marks), their variable pelagecolor, relative body size and other individual characteristics, e.g., ringed tail,hairless parts, white spots.

We followed the groups dawn to dusk, from May 1998 to February 2000,in spans of 7–10 continuous days, on a bimonthly basis. We discontinued sam-pling for nearly 2 mo (September–October) in 1998 and 3 mo (January toMarch) in 1999, after floods covered the island. We report data from 1680 hof observations. Each 15 min, we took scan samples (Altmann, 1974; Martinand Bateson, 1993) of all visible monkeys. We recorded: travel, moving, feed-ing, resting, group confrontations, and social interactions. In each scan, werecorded the height above the ground for each individual that was feeding,traveling or resting. Travel is synchronous mobilization of the group fromone area to another in the forest; moving is a change in the relative positionof an individual into the group; resting is an apparent inactivity of individu-als; and social interaction is nonaggressive activity in which ≥2 individualsparticipated, e.g., grooming and play.

When the subjects fed, we registered plant part—mature leaf, new leaf,flower, mature fruit, green fruit and petiole—and species eaten. Becausesome items ingested by black howlers were infestation by arthropods, weevaluated the percentage of units infested by taking samples on specific dates:

— In July 1998, we collected fruits of Ocotea diospyrifolia, 50 fromthe 7 trees with low frequency of use as food by black howlers, and50 fruits from 8 trees with high frequency of use.

— In September 1999, we collected new leaves of Albizia inundatafrom the 2 trees used by black howlers (all trees in the territoryof Group II).

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— In November 1999, we collected flowers of Inga vera, 20 from 6 trees,3 inside Group I and Group II home range. The others 3 trees wereoutside of their home ranges.

— In May 1999, we collected fruits of Banara arguta, 20 from 10 treesused by Group I and Group II. Also, in September 1999, we collected20 new leaves from 10 trees inside Group I and Group II home range.

— In February 2000, we collected fruits of Eugenia punicifolia, 20 from10 trees used by Group I and Group II.

During the rest of study we confirmed the presence of infestation.

Ranging Patterns

We collected data on ranging patterns simultaneously with behavioralobservations. We made a grid of the entire area used by black howler groupsand labeled intersects of the grid with aluminum tags. We labeled all trees≥20 cm DBH within the home ranges of the groups with aluminum identi-fication tags and mapped their coordinates on the grid.

We plotted on maps the positions of trees where black howler groupsrested during the night—sleeping tree—and every place where groups con-fronted one another. We estimated distance traveled daily by plotting ontomaps the center-of-mass of a group at every interval as they moved throughthe habitat and then calculated the distance as the summation of the mostdirect path between successive chronological points.

We classified space used by black howlers as follows:

Territory: following the definition of Jolly (1985), we considered it to be thearea whose boundaries are defended actively by a group. The defense ofan area does not necessarily imply exclusive use (Jolly, 1985). When agroup detected the presence of another group or individual in the area,they started a pursuit, and the opposing group or individual ran to theboundary, where the groups started a howling confrontation.

Overlapping area: areas visited by a group outside their area and inside theterritory defended by another group.

Home range: area comprising territory and overlapping areas.

Because forest grew on an albardon with a width between 20 and 100 mand black howlers groups used all this zone, we measured the distance alongthe albardon that each group used in order to determine the size of areas.Accordingly, we considered the more extreme positions of groups recordedin the maps as limits of the home range, the sites of group confrontations aslimits of territories, and the areas between limits of home range and limitsof territories as overlapping areas.

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We evaluated the relationship between mean distance traveled daily andmean percentage of mature leaves in the diet in each period, and betweenmean distance traveled daily and number of group confrontations recordedad libitum by the Spearman correlation test (Zar, 1996).

RESULTS

Floristic Composition, Vegetation Structure and Phenology

In 1 ha of forest we recorded 1003 trees from 23 species and 10 families(Table I). We determined two tree strata. The low stratum was dominatedby Eugenia punicifolia, Psychotria carthagenensis and juveniles of Ocoteadiospyrifolia. Its height is between 2 and 10 m, though 72.3% of individualheights were between 4 and 8 m, and mean DBH is 11± 7.6 cm. The higherstratum was dominated by Ocotea diospyrifolia and Cecropia pachystachya,

Table I. Species and number of individuals recorded in vegetation plots from low and highstrata in Brasilera Island (Argentina)

Number of Number ofindividuals in individuals in

Family Species low stratum high stratum

Lauraceae Ocotea diospyrifolia 68 65Nectandra angustifolia 4 3Sp 1 4 6

FabaceaeMimosoideae Albizia inundata 8 22

Inga vera 23 7Caesalpinoideae Peltophorum dubium 1 1Papilionoideae Geoffroea striata 1 3

Myrtaceae Eugenia burkartiana 49 17Eugenia punicifolia 217 2Eugenia pyriformis, var. pyriformis 2Sp2 8Sp3 3

Euforbiaceae Croton urucurana 14 6Sapium haematospermum 2

Flacourtiaceae Banara arguta 8 10Sapotaceae Pouteria salicifolia 1Cecropiaceae Cecropia pachystachya 270 87Meliaceae Guarea macrophylla Subsp. spicaeflora 44 10

Trichilia catigua 2Rubiaceae Psychotria carthagenensis 30Salicaceae Salix humboldtiana 1Undetermined

1 12 3

Note. Only individuals with DBH (Diameter Breast Height) taller than 5 cm were counted.

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the height was between 11 and 23 m, with 89.6% of individuals between 11and 16 m, and mean DBH is 30± 18 cm.

Phenological records showed the lowest level for resources used byblack howlers during winter (June, July and August, Fig. 2a). Consumedspecies did not flower then, and only some individuals of Ocotea diospyrifo-lia, Banara arguta and Psychotria carthagenensis bore fruits (Fig. 2b). Con-sumed species showed a basal level of new leaves of ca. 20%, producedby leaf renewals in perennial species, and mature leaves showed a mini-mum because deciduous species, as fabaceas, lost their leaves. During spring(September, October and November), phenological records showed a higherlevel of food resources (Fig. 2a), with a high level of new leaves, flowers andfruits.

Among fruits, species consumed by black howlers form two sets. Oneoffered fruits in greater or lesser quantities throughout the year—Banaraarguta, Psychotria carthagenensis and Ocotea diospyrifolia (Fig. 2b)—whilethe other concentrated fruit production only in 1 or 2 mo: Cecropia pachys-tachya and Euguenia punicifolia (Fig. 2c).

Foraging Behavior

As foraging behavior of the two groups were very similar, we present themean percentage of both groups. Annually black howlers consumed plantparts of 22 species from 15 families (Table II). Tree species represented63.6% of them. Fruits of tree species consumed by black howlers (Table II)represent 76.9% of the total individuals recorded in the vegetation plots.Also, black howlers consumed fruits of 2 species of vines (Table II), and≥1 epiphytic plant. Fruits of Psychotria carthagenensis were generally onlyeaten by juvenile black howlers. The month with fruit consumption of thegreatest number of species was May 1999, with 4 species. Annually, maturefruits represented 17.6% of black howler diet (Fig. 3a), but in some monthsthey represented>60% of the diet (Fig. 3b). We recorded the highest percentof feeding on mature fruit by Group II during July 1998 (71%).

Yearly, flowers represented 12% of howler diet (Fig. 3a), though in somemonths they could represent 44% of the diet (Fig. 3b), and they were eatenin a similar proportion as fruits when fruits were not available (Fig. 3b).Howlers ate flowers of Geofroea striatta (24.3%; 32.5%; 29.5%), Inga vera(42.2%) and Species 1 (Papilionaceae) (12.7%) each time they were avail-able. In some months, black howlers ingested flowers of 2 species from whichthey commonly ate fruits (Ocotea diospyrifolia 10.2% of feeding records ofGroup II in November 1999, and Banara arguta 10.2% of feeding records ofGroup I in February 2000).

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Fig. 2. (a) TPIsp = Total Phenological index (See methods). (b) Pisp =Partial Phenological index, abundance of fruits from species ingested byblack howlers that were available all year. (c) Abundance of fruits fromspecies available only in some months.

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Table II. Species used by black howlers as food resources in Brasilera Island (Argentina)

Life history Family Species Fl Fr Nl Ml P

Trees Lauraceae Ocotea diospyrifolia X X X XNectandra angustifolia X X

Mimosaceae Albizia inundata X XInga vera X X

Papilionaceas Geofroea striatta X X X XSp1 X X X

Mirtaceae Euguenia punicifolia X X X XPsidium guajaba XEuguenia pyriformis XVar. pyriformis

Flacurtiaceae Banara arguta X X X XSapotaceae Pouteria salicifolia X XMoraceae Cecropia pachystachya X X X X XRubiaceae Psychotria carthagenensis X

Vines Bignoniaceae Clytostoma callistegioides X X XConvolvulaceae Ipomoe alba X X

Ipomoea indica X XIpomoea cairica X X

Vitaceae Cissus palmata X X XSapindaceae Paullinia sp. X X

Shrubs Urticaceae Urera aurantiaca XFlia 1 Sp 2 X X

Aquatic plants Pontederiaceae Eichhornia crassipes X

Note. The X indicates the item used. Fl = Flowers, Fr = Fruits, Nl = New leaves, Ml =Matureleaves, P = Petiole.

When high quality food, i.e., fruits, flowers, and new leaves, was notavailable both groups used the same strategy. They consumed only matureleaves, and the groups divided into two subgroups, which foraged in theextreme sites of the group home ranges. At sunset they grouped again for afinal foraging period and rested together during the night. Subgroup com-position changed every day. During the day some individuals changed fromone subgroup to another.

Black howlers ingested animal protein indirectly when they fed on newleaves, fruits and flowers. Each month one of the principal items in the dietwas heavily infested by arthropods (Table III). Consumption of infesteditems represented 25.5% of the total feeding records. The greatest percent-age recorded during the month of July 1998 is 66.7% for Group II.

Trees of Ocotea diospyrifolia were in high abundance in the old growthforest; however, black howlers ingested their fruits only from some of them.For example, during July 1998 Group I used more frequently the trees thatwere in the territory of Group II, and thus generated confrontations. Whenwe evaluated the infestation of Ocotea diospyrifolia, we found that trees interritory of Group I had 35% of their seeds infested, while trees in territory

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Fig. 3. (a) Annual percentage of feeding records for the different items used by blackhowlers on Brasilera Island. (b) Percentage of feeding records for the different items ineach period sampled. Values are the mean of two groups. Ml = mature leaves, Nl = newleaves, Frm = mature fruits, Frg = green fruits, Fl = Flowers, B = Buds.

of Group II had >80% of infestation. We detected larvae of two species ofHeilipus. (Curculionidae) infesting seeds of Ocotea diospyrifolia.

Ingestion by howlers of honey, moss, and lichens on branches and trunkswas very rare, but their consumption of free water was common. When it

Table III. Plant items infested by insects and ingested by black howlers in Brasilera island(Argentina)

Infested Infestation Frequency in the diet perSpecies item (mean % ± SD) Period period (mean % ± SD)

Eugenia punicifolia Fruit Nov. 98 20.28 ± 0.0480.42 ± 12.28 Feb. 00 10.68 ± 14.29

Ocotea diospyrifolia Seed May 99 29.16 ± 0.1182.00 ± 10.30 Jul. 98 58.78 ± 11.15

Jul. 99 1.63 ± 2.31Feb. 00 0.29 ± 0.40

Inga vera Flower Nov. 98 22.23 ± 28.1989.81 ± 11.36 Nov. 99 0.61 ± 0.86

Albizia inundata New leaves 100 Sept. 99 11.84 ± 2.82Nov. 98 10.81 ± 3.51Nov. 99 15.43 ± 7.10

Banara arguta Fruit 100 May 99 11.44 ± 2.53Jul. 98 0.73 ± 1.03Nov. 98 0.26 ± 0.4

B. arguta New leaves 100 Sept. 99 11.62 ± 9.21Nov. 99 11.41 ± 7.98

Note. Infestation values are the mean percentage of units infested by trees in each species. Thelast row shows the frequency of each item in the diet during the periods in which it was ingestedby black howlers (mean of both groups under observation).

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Fig. 4. (a) Annual mean percentage recorded for each behavior. (b) Percentage of recordsfor each behavior shown by black howlers during each period sampled. Values are the meanof two groups.

was not available, black howlers ate petioles of aquatic plants that persist inthe mud.

Activity Patterns

The two black howler groups had very similar activity patterns, so wepresent common mean percentages for the different foraging activities.

Annual mean percentage of rest is 56.5%, while annual mean of feed-ing and travel a 18.9% and 10.5%, respectively (Fig. 4a). In some months,howlers spent ca. 50% of the day engaged in activity (Fig. 4b). We noted nopattern in the rhythms of activity and rest of black howlers, because theyhad a low activity during the mid morning and mid afternoon, but someindividuals fed while others played or allogroomed. Also, the periods oflow activity were interrupted because individuals detected the presence ofanother group near or in their territory.

Social interactions included principally allogrooming and play. Blackhowlers had long sessions of allogrooming during the low activity periodsand after confrontations. Usually a pair of monkeys spent around 15 mininteracting in an allogroming session, but we recorded sessions that lasted>45 min. Play occurred mainly (>70%) between juveniles or between adults(males or females) and an infant or juvenile; however, adult males also playedtogether. Alloparental care was common, including males carrying infantsor helping juveniles that were recently independent of the mother’s bodyFemales suckled infants and independent juveniles, which were not theirown offspring. Adoption also occurred an ill female with a young infant(2–3 mo old) could not travel with the group, and her infant was seen with

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Fig. 5. Feeding, resting and travel height for black howler groups. (I) = Group I,(II) = Group II.

another female that had an infant of the same age. The ill female died, butthe 2 infants survived at least up to the end of our study, when they were ca.15 mo old.

For each group, the mean heights above ground where they fed, rested,and traveled were similar (Fig. 5). The 2 black howler groups had similarforaging behavior and activity patterns, though the levels of activity and themean height of activity of Group II were higher. In general, the territoryof Group II had taller trees than that of Group I. Therefore, the averageheight of resting of Group I is lower. Difference in feeding height is relatedto the consumption of vines. Group I mainly fed on vines in shrubs, whileGroup II foraged in tall trees. Travel height differences occurred becauseGroup I used the ground to travel between patches of forest in the extremeof albardon, while Group II never travelled on the ground.

Ranging Pattern

More than 70% of behavioral records are from territories. Territoriesdefended by black howler groups were 1.3 ha for Group I and 1.8 ha forGroup II (Fig. 1c). During February 2000, Group II displaced Group I, thusthe area defended in this period was 0.92 ha for Group I and 2.76 ha forGroup II.

Howlers used overlapping areas at low frequency, and they ran to theterritory limits when detected and pursued by the resident group. At the

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territorial perimeter, black howler groups howled within a few meters ofone another. In general, confrontations finished suddenly, some individualsof the groups began to eat, juveniles of the two groups played together, andadult males rested and some females allogroomed them. However, in somecases confrontations terminated with physical aggression. The overlappingarea of Group I over Group II territory was 0.44 ha, and we did not detectoverlapping with any other group. The overlapping area of Group II overGroup I territory and over a third group’s territory was 0.4 ha.

Home range was 1.7 ha for Group I and 2.2 ha for Group II. During theday, as howler groups used all their territories, they had visual contact withneighboring groups or dispersing individuals, thus we recorded ≤6 howlingconfrontations by the Group II in a single day (February 2000).

Mean daily distances traveled is 513± 253 m for Group I and 602±350 m for Group II. The maximum (GROUP II, 1,515 m) and minimum(GROUP I, 85 m) daily distances traveled occurred in February 2000, whenGroup I was displaced by Group II. Mean distance traveled daily is positivelycorrelated with number of confrontations (Group I: rs = 0.77, P< 0.05, n=7; Group II: rs = 0.75, P< 0.05, n= 7; Fig 6a), but is not correlated with thepercentage of mature leaves in the diet (Group I: rs = −0.21, P = 0.64, n =7; Group II: rs = −0.18; P = 0.70, n = 7; Fig 6b).

The howlers used sleeping trees with different frequencies (Table IV);both groups had a principal sleeping tree. Group I used theirs to rest during47.4% of the nights, and Group II used theirs 52.7% of the nights. Group Iused 6 other sleeping trees, one which is a small patch of forest (Fig. 1c), andGroup II used 7 other sleeping trees.

DISCUSSION

The mean home range of black howlers in Argentinean flooded forestis the smallest of the genus in a natural environment (Table V). Our resultssupport Hypothesis 1—that home range is inversely related to howler pop-ulation density (Crockett and Eisenberg, 1987)—because the island has thehighest known howler density (Crockett, 1998; Rumiz, 1990; Zunino et al.,2001; Zunino and Rumiz, 1986). In southern Brazil, a group of black howlerslived in a forest patch of 2 ha (Bicca-Marquez, 1994), but it was not a naturalforest and the black howlers used commercial fruits species (Citrus sinenesis)as food resources.

Contrary to Hypothesis 2, despite the extremely small home ranges thatwe found for black howlers on Brasilera Island, their diet was not dominatedby leaves. On the mainland, where home ranges average 5.5 ha, leaves rep-resented 70% of howler diet (Zunino and Rumiz, 1986), while in Brasilera

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Fig. 6. (a) Correlation between number of confrontations and mean daily distance trav-eled (DTD) of each black howler group during each period of observation. (b) Correla-tion between percentage of mature leaves in black howlers diet and DTD of each blackhowler group during each observational period. ◦ = Values of Group I. • = Values ofGroup II.

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Table IV. Percentage of nights that each blackhowler group used each sleeping site

Sleeping site Group I (%) Group II (%)

1 47.4 52.72 18.4 14.53 13.2 12.74 10.5 7.35 5.3 7.36 2.6 1.87 2.6 1.88 1.8

Island where the focal groups have around 2-ha home ranges, leaves repre-sented only 51% of their diet. Our Analysis of monthly consumption showedthat in July 1999, the percentage of leaves in the diet was extremely high be-cause during the week observed there was no fruits or flower in the homeranges of the 2 groups. If we recalculate the annual percentage of matureleaves in the diet without considering July 1999, the average percentage ofmature leaves in the diet is <40%. In Los Tuxtlas, Mexico, exactly the op-posite occurred for Alouatta palliata, with an unusually large home rangeand a diet dominated by leaves. Estrada (1984) explained this by consid-ering the leaves like fruits, because their availability was unpredictable intime and space. Conversely, we explain the unusually small home rangein Argentinean flooded forest, considering the fruits like leaves, because

Table V. Home range in hectares reported for different Alouatta spp.

Species Home range (ha) Reference

A. caraya 1.7–2.2a This studyA. caraya 2 Bicca-Marques (1994)A. caraya 5–6a Zunino (1986)A. seniculus 4–7b Sekulic (1982)A. palliata 9.9 Glander (1980)A. seniculus 10–20b Terborgh in Crockett and Eisenberg (1987)A. seniculus 13–24a Defler in Crockett and Eisenberg (1987)A. seniculus 22 Gaulin and Gaulin (1982)A. palliata 31 Milton (1980)A. pigra 25–50a Silver et al. (1998)A. seniculus 45 Julliot (1992)A. palliata 54 Stoner (1996)A. palliata 60 Estrada (1984)A. palliata 108 Chapman (1988)A. pigra 125 Schlichte in Crockett and Eisenberg (1987)A. seniculus 182 Palacios and Rodriguez (2001)

aTwo groups home range.bRange over 4 groups.

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fruiting trees in flooded forest represent>70% of trees in the forest, and are,they always available during the year. So, we could reformulate Hypothesis 2as follows: howlers have small home range in areas where their diet is domi-nated by resources with high abundance and uniform distribution in time andspace.

There is no correlation between the percentage of leaves in the diet anddaily travel distance (Hypothesis 3). Therefore, black howlers in BrasileraIsland appear not to be energetically constrained. In contrast, distance trav-eled daily is correlated with confrontations, a positive relationship that couldbe an indirect effect of high densities. Accordingly, home range may not bethe only parameter affected by high population density. Additional evidenceagainst energetic constraints in black howlers inhabiting Brasilera Island arethe hours dedicated to rest. They spent 63–80% of daytime resting (Crockettand Eisenberg, 1987; Estrada et al., 1999), and in Argentine mainland forestblack howlers spent 77.4% of daytime resting (Zunino, 1989). The lowestrest percentage is in Brasilera Island. It is similar to the rest time of Atelesgeoffroyi (40–54%), a monkey of similar size but with a more energetic diet(Crockett and Eisenberg, 1987).

What would be the factors explaining this lack of energetic constraint?We consider the contributing factors to be temporal and spatial distributionof resources.

Seasonal food availability on Brasilera Island was higher than in main-land patch forest of similar latitude and altitude (Zunino, 1989). From theend of autumn (June) to the beginning of spring (October) the mainlandforest had low food abundance (Zunino, 1989; Zunino et al., 2001), and inwinter, Ficus luschnachtiana is the only species that offers fruits: few itemsat any given time because it fruits asynchronously (Bravo and Zunino, 2000;Zunino, 1989).

Throughout the year, high quality items in the diet may be supple-mented energetically by a high level of infestation by insects. Infested itemsrepresent >25% of the black howler diet over the year. Others species ofhowlers incorporate indirectly few insects in their diets, generally from figs(Crockett and Eisenberg, 1987; Prates et al., 1990). New leaves of Albiziainundata had ≥2 aphids in each foliole, and the entire surface was coveredwith honeydew secreted by them. Dry weight honeydew is 90–95% carbo-hydrate and could contain amino acids (Holldobler and Wilson, 1990). Allinfested items represent an ingestion of sugar—fruits, honeydew or nectar—and protein: larvae or adult insects. Proteins eaten with carbohydrates areused for vital functions, while proteins consumed without carbohydrates aremetabolized for energy. This is one of the reasons why some omnivorousspecies, e.g., Cebus capucinus, Pan paniscus, search for infested fruits: to ob-tain high quality items more easily than insect consumption alone (Redford

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et al., 1984). Another possible reason for ingestion of infested items is thatinfestation is a signal used by black howlers to evaluate secondary compoundconcentrations. However, in Costa Rica protein content is the principal fac-tor in food selection by Alouatta palliata, and astringency and tannin concen-trations are a secondary factor in their evaluation of food items (Bilgener,1995). In order to understand the role of insects in howler diet, it will benecessary to determine the digestive efficiency of howlers that eat them.

The trees of 9 species whose parts were commonly consumed by blackhowlers in 2-ha home ranges represented 89% of trees recorded in the floris-tic plots, indicating a uniform spatial distribution of resources. The low treespecies diversity in Brasilera Island is correlated with low diversity in the dietof black howlers, compared to the diet of other species of howlers (Table VI).According to Gaulin et al. (1980) and Stoner (1996) an important factor de-termining habitat quality is the density of the food species most commonlyconsumed. Accordingly, we could consider flooded forest to be a high-qualityhabitat for the black howlers, which could help to explain the lack of ener-getic constraints.

Abundance and distribution of high quality items also could be respon-sible for big groups using small areas, because during brief periods in whichonly mature leaves were available, black howler groups divided in 2 sub-groups. During a brief study in Guascara Island (Parana River, Argentina),Zunino and Rumiz (1986) also observed this behavior when the only foodavailable was mature leaves. Black howler diet in the Argentine mainland isdominated by mature leaves and group division was not reported by Zunino(1987). However, one must consider that groups Argentine mainland forestare smaller than those in flooded forest and sometimes even smaller floodedforest subgroups. In general, howler groups are cohesive and stable (Chivers,1969; Estrada, 1984; Gaulin et al., 1980; Gaulin and Gaulin, 1982; Glander,

Table VI. Species richness of diet for different species of howlers

Species Number of species Reference

Alouatta caraya 18 Zunino (1987)Alouatta caraya 22 This studyAlouatta palliata 22 Chapman (1988)Alouatta fusca 27 Prates et al. (1990)Alouatta fusca 52 Galetti et al. (1994)Alouatta palliata 73 Milton (1980)Alouatta pigra 74 Silver et al. (1998)Alouatta palliata 95–65b Stoner (1996)Alouatta palliata 96a Glander (1980)Alouatta seniculus 195 Julliot (1994)

aOnly arboreal species.bThe two groups studied used differnt number of species.

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1980; Julliot, 1992; Milton, 1980). Division into subgroups is not exclusiveto black howlers, because it occurs among Alouatta palliata in Costa Rica,where subgroups may have no contact for ≤4 weeks (Chapman, 1988).

In Figure 7, we present a model to summarize and integrate our results,showing how spatial and temporal abundance of high quality resources couldbe favoring high population density, while minimizing energetic constraintsover individuals. High density promotes a small home range, while the lackof energetic constraints on individuals increases their activity. High levels ofactivity together with small home ranges increase the encounter probability,

Fig. 7. Model that integrates our results of resource availability, behavior and spatial use ofblack howlers in Argentinean flooded forest. Arrows indicate the directionality of the relationbetween variables. + sign indicates a positive relation between the variables contacted by thearrow. − indicates a negative relation between the variables contacted by the arrow.

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844 Bravo and Sallenave

and if the good nutritional condition of individuals is taken into account, theencounter probability produces a high frequency of confrontations. There isa positive feedback between activity level and encounter probability becausewhen an individual from a group detects the presence of a strange individualor another group, it vocalizes and the group travels to the area? Accordingly,daily travel distance is correlated with number of confrontations. Finally,high density and activity decreases the areas of flooded forest used at lowfrequency by black howler groups. The only factor that we know that candisrupt this situation in the island is extraordinary floods, because they killa high proportion of trees and thus drastically decrease the resources avail-ability and consequently diminish black howler density. Thus, the floodedforest has variable quality because it depends on river flood dynamics. Assuggested by Van Horne (1983), using only density as an indicator of habitatquality could be misleading.

Black howler persistence in the islands could depend on mainland pop-ulations. Therefore, we consider the island-mainland system for black howlerto be a metapopulation, where in the mainland is a source, helping in therapid restoration of island populations after an extraordinary flood. There isno significant genetic difference between black howler populations inhabit-ing the flooded forest and the mainland (Szapkievich, 2001).

Flooded forest on islands of the Parana River is one of the least knownwetland regions, and it is one of those most threatened and altered by theconstruction of dams and canals (Neiff, 1999). If a conservation plan is de-veloped, it will be necessary to consider not only a protected corridor ofislands along Parana River but also protected areas on the mainland.

ACKNOWLEDGMENTS

We thank the 15 students who helped us with fieldwork, especiallyLuciana, Silvana, Sebastian, Boris, Sonia and Candelaria, and hope thatthey enjoyed howlers. Susana Bravo gratefully acknowledges her adviserGabriel Zunino. Special thanks to Victor Cueto, Olga Vaccaro, Ana LıaVanzato, Carolyn Crockett and two anonymous reviewers for comments onthe manuscript and assistance with the English language. We also to thankCentro de Capacitacion Comunitario from Cerrito Island, and people fromCerrito community including Mr. Gallo, his wife Titina and Cencio for theirhelp when problem arose. We thank Guillermo Cao and his family for re-ceiving us in their home every time it was necessary, Martin Kowalewskiand Julian Faivovich for assistance with the bibliography. The research waspartially supported by Consejo Nacional de Investigaciones Cientıficas yTecnicas and by International Foundation for Science (research grantD/2686-1).

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