La Suerte

Interactions between mantled howling monkeys (Alouatta palliata) and neotropical birds in a fragmented forest habitat on Ometepe Island, Nicaragua *

Falk Huettmann and Julia Linke, Atlantic Cooperative Wildlife Ecology Research Network, Faculty of Forestry and Environmental Management, P.O.Box 44555, University of New Brunswick (UNB), Fredericton NB, Canada E3B 6C2. Email: k9wk@unb.ca

* as presented:
Huettmann, F. (1999).Interactions between mantled howling monkeys (Alouatta palliata) and neotropical birds in a fragmented forest habitat on Ometepe Island, Nicaragua. (Abstract) American Association of Physical Anthropologists, Supplement 28 to the American Association of Physical Anthropology Annual Meeting Issue, p. 156.

Abstract

Interactions across animal taxa and mixed species assemblages are known to improve the survival of the participating species, and can be found throughout the tropics. This study investigates opportunistic ecological interactions between mantled howling monkeys (Alouatta palliata) and some of the most abundant neotropical bird species in the study area, such as banded wren (Thryothorus pleurostictus), white-throated magpie-jay (Calocitta formosa f.) and turkey vulture (Cathartes aura). Forty one hours of bird surveys and monkey contact hours were carried out in two separate fragmented blocks of a seasonal dry forest near the Ometepe Biological Field Station during July and August 1998, in the wet season. The presence, absence, calling frequency and activity between these two animal taxa were analyzed for plots with a 30 m radius, identified as the "viewshed". This radius was choosen since the forest does always allow for oral ("soundscape", 2 km radius), but not for visual observations beyond 30 m. These plots were equally investigated over the whole day, occurrence of wind was identified also. Plots were compared where mantled howling monkeys were present versus control plots where mantled howling monkeys were absent. The masking effect of wind within the "soundscape" proved to be relevant for calls of mantled howling monkeys and birds. Birds were not observed to be feeding on insects or fruits, made available to them by mantled howling monkeys, e.g. by discard feeding of fruits or chasing off insects. Significant results are presented for mantled howling monkeys behavior (howling, moving, feeding, resting) and presence and absence of birds of prey and songbirds. Banded wrens were found to be stimulated to start singing by calling mantled howling monkeys. Except for turkey vultures no other predators (birds of prey, snakes, large mammals) were observed in the "soundscape" when howling monkeys were present. Implications of the observed predator-free "soundscape" for mantled howling monkeys and birds are discussed.

Introduction

Interactions between monkeys and other animals are well known; however, they can be complex and are often not well documented. Most described relationships are food related and are found throughout the whole distribution range of monkey occurrence. For the Old World, Chapin (1939) described associations between long-tailed hornbills (Berenicornis albocristatus) and African monkeys. For the Philippines an association between fairy bluebirds (Irena cyanogaster) and crab-eating macaques (Maccaca fascicularis) was described by Stott (1947); Galetti and McConkey (1998) showed that black hornbills (Anthracoceros malayanus) follow gibbons in central Borneo. For the New World, Fontaine (1980) presented a foraging association of double-toothed kites (Harpagus bidentatus) and white-faced capuchin monkeys (Cebus capuchinus) on Barro Colorado Island in Panama (see Warkentin 1993 for sharp-shinned hawks Accipiter striatus and white-faced Capuchins for the Tivivies Forest Reserve in Costa Rica). Boinski (1988) showed an association of birds with monkeys in Costa Rica, namely double-toothed kites, gray-headed tanagers (Eucometis pencillata), tawny-winged woodcreepers (Dendrocincla anabatina) foraging in association with squirrel monkey (Saimiri oerstedi) troops, and to a lesser degree with capuchin monkeys (kites only), in Parque Nacional Corcovado, Costa Rica.

Agoramoorthy (1997) reports a feeding association between Alouatta seniculus and Odocoileus virginianus (white-tailed deer) in Venezuela, and Glander (1979) reports feeding associations between howling monkeys (Alouatta palliata) and basilisk lizards (Anacardium excelsum). However, relations between howling monkeys and birds are not described, except for Young (1982) on howler monkeys and turkey vultures (Cathartes aura) encounters, and one single observation by Fontaine (1988) of a kite following a rapidly moving troop of howlers. Fontaine (1988) reports that birds "may break off contact with Ateles and Alouatta when these monkeys take their frequent extended rest".

Mantled howling monkeys are unique in terms of their very prominent call, which can travel several kilometers through the forest. The only other monkey with a comparative call is the orangutan (Pongo pygmaeus) in Asia (Galdikas and Insley 1988, Hohmann and Fruth 1995). Considering the long resting periods for mantled howling monkeys (Milton 1977) lead me to formulate the hypothesis that the presence of howling monkeys do not attract birds, but I predict that their calls act as signals and affect birds.

In order to test this hypothesis I investigated the bird numbers (banded wren Thryothorus pleurostictus, white-throated magpie-jay Calocitta formosa f. and turkey vulture) in relation to the presence, activity and calls of mantled howling monkeys on Ometepe Island in Nicaragua.

Methods

We worked in the two forests, outlined in Map1 and Map2. Fig. 1 shows the "sound-scape", and the data collection scheme. 42 contact hours for monkeys and birds were carried out within 30 m radius plots (viewshed) in two forests on a volcano bottom slope on Ometepe Island. The bird observations were done visual, except for Banded Wrens (song included) (Bibby et al. 1992, Buckland et al. 1993). Plots with monkeys were selected wherever monkeys could be found while walking in the forest randomly. Locations of plots without monkeys were selected randomly within the two forests so that equal sampling effort among habitat strata was guaranteed. Data were processed, analysed and plottted in SPLUS 4.5 release I (Statsci 1995).

Results

We found that abundances of turkey vultures, banded wrens and magpie-jays were significantly higher when mantled howling monkeys howled (Fig. 2, Fig. 3), whereas the simple presence and activity patterns of mantled howling monkeys had no significant impact on the observed numbers of these bird species at all. Figure 4 showed that most turkey vultures appeared two - three minutes after an howling event, visual and oral presence of banded wrens was recognized during the whole 15 minutes peaking at four minutes after howling; magpie-jays were found most often at one minute and at eleven minutes after howling. Figure 5 showed that initially a linear relation existed between howling frequency (howls per hour) and the number of bird observations for turkey vultures and banded wrens, which were mostly observed as single birds. Bird numbers did not increase for > 2 howls per hour but were low for > 9 howls per hour. This data suggested a response peak (threshold) between two and nine howls per hour. This pattern was not obvious for magpie-jays, but could be hidden since magpie-jays were observed in flocks of two - seven birds. I concluded that few howls (signals) were enough to attract these birds. I had no observations for howling frequencies between two and nine howls per hour, which could be related to the metabolism of howling monkeys, or to our sample size. Figure 6 showed a day profile for the animals studied, corrected for sampling effort. Banded wrens could be considered as early morning (8 AM) birds, with a second but smaller peak around noon time; turkey vultures were most active around 8 AM, and 2 PM. Magpie-jays were active in the morning (8 AM, 10 AM), but had their highest peak around 2 PM, and to a lower degree before sun-set (5 PM). I assumed that these activity patterns were related to foraging activities of these birds. The day profile of howls showed an almost regularly spaced pattern with two - three hour intervals, and a higher peak at 4 PM. I found that appr. 60 % of howls were started by wind gusts (graph not shown here). Our data did not detect an early morning peak of howls, as discussed for howling monkeys elsewhere, but we only surveyed during sun light hours (7 AM - 5 PM).

Discussion

Our results showed that the investigated bird species had individual activity patterns, which did not overlap with howling activities as such. However, since bird observations were significantly related with howls, we concluded that birds responded to howling events. In future studies, the specific daily activity patterns of species involved would need to be considered in detail.

The speed of bird responses to howls could be influenced by the bird distribution in the surrounding habitat, and how quickly the birds could approach the location where a howl occurred (viewshed). I did not observe any birds having obvious benefits from joining mantled howling monkeys, such as increased food availability described for other monkeys elsewhere. We assumed that "checking for food" was the case for magpie-jays and turkey vultures when observed after howling since both birds were described as opportunistic feeders (e.g. Howell and Webb 1995). However, banded wrens seem to use the howls as an indication for a predator-free environment; this song bird also gave a relatively far ranging call (appr. 500 m) which potentially could attract predators. Since during our investigations not a single predator (reptile, mammal or raptor) relevant for songbirds was observed in the presence of mantled howling monkeys while howling, and the 15 minutes afterwards, we concluded that howling served as a 'sound umbrella' providing other animals with an indication of a predator-free environment. This could have stimulated banded wrens to become prominent (e.g. start singing). Since appr. 60 % of the howls were wind induced (wind could mask any noise in a forest such as howls), the specific meteorology of the island and the atmospheric interactions between volcano, cloud forest and Lake Nicaragua might have been relevant for this pattern, and would need to be addressed in future studies. The specific island population (Winkler et al. 1999) and set-up of the study area could also explain why our diurnal pattern of howls did not match with studies on howling done elsewhere (e.g. Milton 1977).

Outlook

This study covered only two months (July - August) during the wet season. It is likely that the avifauna changes when wintering neotropical migrants enter the region. Further research would be needed throughout the year to investigate how such a scenario would affect the results shown and discussed here.

Acknowledgements

F.H .is very grateful to L. Winkler, the Molina Family, the TA colleagues (M.Bezanson & C. Travers), and certainly all the students of the Ometepe Advanced Primatology Field Course July-August 1998 for the help and support carrying out this work. An oral version of this paper was given at the Northeast Graduate Student Wildlife Conference at the University of Orono, Wildlife Department, in Maine/U.S.

LITERATURE

Agoramoorty, G. 1997. Apparent feeding associations between Alouatta seniculus and Odocoileus virginianus in Venezuela. Mammalia 61 (2): 271-273.

Bibby, C.J., N.D. Burgess, and D.A. Hill. 1992. Bird census techniques. Academic Press, Hartcourt Brace & Company Publishers.

Boinski, S. and R. M. Timm. 1985. Predation by squirrel monkeys and double-toothed kites on tent-making bats. American Journal of Primatology 9 (2): 121 - 127.

Boinski, S., P. E. Scott. 1988. Association of birds with monkeys in Costa Rica. Biotropica 20 (2): 136 - 143.

Buckland, S.T., D.R. Anderson, K.P. Burnham, and J.P. Laake. 1993. Distance sampling. Chapman and Hall, New York, N.Y.

Fontaine, R. 1980. Observations on the foraging association of double-toothed kites and white-faced capuchin monkeys. Auk 97: 94 - 98.

Galdikas, B. M. F. and S. I. Insley. 1988. The fast call of the adult male orangutan. Journal of Mammalogy 69 (2): 371 - 375.

Galetti, M. and K. McConkey. 1998. Black Hornbill Anthracoceros malayanus following Gibbons in central Borneo. Ibis 140 (4): 686 - 687.

Glander, K. E. 1979. Feeding associations between howling monkeys and basilisk lizards. Biotropica 11: 235 - 236.

Hohmann, G. and B. Fruth. 1995. Loud calls in great apes: Sex difference and social correlates. Pp. 161 - 184 in Current Topics in Primate Vocal Communication by E Zimmermann (ed.), New York, Plenum Press.

Howell, S. N. and S. Webb. 1995. A guide to the birds of Mexico and Northern Central America. Oxford University Press, Oxford. 851 pp.

Huettmann, F. and J. Bowman. (eds.) (1999). Investigation of Animal Movement. Workshop Proceedings, 12 - 14 November 1998 Fredericton. Supported by the Sir James Dunn Wildlife Research Centre, Atlantic Cooperative Wildlife Ecology Research Network, Biology Dept. of the University of New Brunswick.

Milton, K. 1977. The Foraging strategy of the howler monkey in the tropical forest of Barro Colorado Island, Panama. Unpublished Ph.D. dissertation, New York, New York University.

Statsci 1995. SPLUS Guide to Statistical and Mathematical Analysis, Version 4.5, Mathsoft Inc. Seattle.

Warkentin, I. G. 1993. Presumptive foraging association between sharp-shinned hawks (Accipiter striatus) and white-faced capuchin monkeys (Cebus capuchinus). Journal of Raptor Research 27 (1): 46 -47.

Whitehead, G. M. 1990. Comparison of the loud calls of howling monkeys. American Journal of Primatology 20 (3): 244.

Winkler, L., G. Peter and R. Sohn. (1999). Monitoring health, genetic diversity, movement, and fission-fusion social patterns in a New World monkey (Alouatta palliata): an interdisciplinary project. Pages 79 -84. In: Huettmann, F., Bowman, F. (1999). Investigation of Animal Movement. Workshop Proceedings, 12 - 14 November 1998 Fredericton. Supported by the Sir James Dunn Wildlife Research Centre, Atlantic Cooperative Wildlife Ecology Research Network, Biology Dept. of the University of New Brunswick.

Young, O. P. 1982. Aggressive interaction between howler monkeys and turkey vultures: The need to thermoregulate behaviorally. Biotropica 14 (3)

Sketch of study area and data collection scheme

Sonogram of a howl from a Howling Monkey

Howling and Bird Numbers

Howling Frequency and Bird Observations

Day profile of howling and bird observations (corrected for sampling effort)

Write to La Suerte | La Suerte Home Page