Abstract
Beyond the unique sound of howler monkey vocalizations, their vigorous loud calling displays are perplexing given the otherwise sedentary lifestyle of these primates. Here we provide potential explanations for this energetic investment by reviewing all available functional studies conducted to date. We highlight the variation among and even within species when we explore whether male loud calls are used in group cohesion, predator avoidance, attraction of females, or competition with other males or other groups over resources. In the competition scenario, we examine strategies of avoidance versus direct competition and whether contests are focused on defense of space, food, mates, or infants. We suggest that much of the debate surrounding the function of loud calls stems from methodological differences among researchers and from the varied levels of analyses used, although we also demonstrate that studies of form and function can be intertwined. We emphasize the need to examine different call types separately and discuss the role of howling in intragroup male relationships. Finally, we address the understudied role of female loud calling and the potential use of hybrid populations to examine the evolution of species-typical loud calls. We conclude with some practical hints for designing field tests to uncover functional significance.
Resumen
Más allá del sonido único de las vocalizaciones de los monos aulladores, estos vigorosos despliegues nos dejan perplejos, dado el sedentario estilo de vida de estos primates. En este capítulo damos explicaciones potenciales a esta inversión de energía, a través de una revisión de los estudios funcionales llevados a cabo hasta la fecha. Remarcamos la variación entre y dentro de las especies cuando exploramos si los aullidos de los machos son utilizados en la cohesión de grupo, evasión de predadores, atracción de hembras o competencia. Sobre este último escenario, examinamos las estrategias de evasión versus la competencia directa y exploramos si la competencia se focaliza en la defensa del espacio, la comida, las parejas o los infantes. Sugerimos que gran parte del debate sobre la función de las vocalizaciones de larga distancia radica en diferencias metodológicas entre investigadores, así como en la variedad de niveles de análisis utilizados, aunque también demostramos que los estudios de forma y función pueden estar entrelazados. Enfatizamos la necesidad de examinar diferentes tipos de llamados separadamente y discutimos el papel de los aullidos en las relaciones intragrupales entre machos. Finalmente, abarcamos el escasamente estudiado papel de las vocalizaciones de larga distancia emitidas por las hembras y la potencial utilización de poblaciones de híbridos para examinar la evolución de las vocalizaciones de larga distancia, típicos de cada especie. Concluimos con consejos prácticos para el diseño de estudios en el campo que permitan descubrir significados funcionales.
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Abbreviations
- %:
-
Percent
- >:
-
Greater than
- A.:
-
Alouatta
- e.g.:
-
For example
- i.e.:
-
In other words
- kHz:
-
Kilohertz
- MA:
-
Massachusetts
- Min:
-
Minutes
- NY:
-
New York
- P.:
-
Pan
- pers. obs.:
-
Personal observation
- RHP:
-
Resource holding potential
- TFT:
-
Tit-for-Tat
- UK:
-
United Kingdom
- unpubl. data:
-
Unpublished data
References
Agostini I, Holzmann I, Di Bitetti MS (2008) Infant hybrids in a newly formed mixed-species group of howler monkeys (Alouatta guariba clamitans and Alouatta caraya) in northeastern Argentina. Primates 49:304–307
Agostini I, Holzmann I, Di Bitetti M (2010a) Are howler monkey species ecologically equivalent? Trophic niche overlap in syntopic Alouatta guariba clamitans and A. caraya. Am J Primatol 72:173–186
Agostini I, Holzmann I, Di Bitetti M (2010b) Ranging patterns of two syntopic howler monkey species (Alouatta guariba and A. caraya) in Northeastern Argentina. Int J Primatol 31:363–381
Aguiar L (2010) Sistema social de grupos mistos de espécies de bugios (Alouatta caraya e Alouatta clamitans) e potenciais híbridos no Alto Rio Paraná, Sul do Brasil. PhD dissertation, Universidade Federal do Paraná
Aguiar LM, Mellek DM, Abreu KC, Boscarato TG, Berbardi IP, Miranda JMD, Passos FC (2007) Sympatry between Alouatta caraya and Alouatta clamitans and the rediscovery of free-ranging potential hybrids in Southern Brazil. Primates 48:245–248
Aguiar LM, Pie MR, Passos FC (2008) Wild mixed groups of howler species (Alouatta caraya and Alouatta clamitans) and new evidence for their hybridization. Primates 49:149–152
Alberts SC, Altmann J (2001) Immigration and hybridization patterns of yellow and anubis baboons in and around Amboseli, Kenya. Am J Primatol 53:139–154
Altmann SA (1959) Field observations on a howling monkey society. J Mammal 40:317–330
August PV, Anderson JGT (1987) Mammal sounds and motivation-structural rules: a test of the hypothesis. J Mammal 68:1–9
Axelrod R, Hamilton WD (1981) The evolution of cooperation. Science 211:1390–1396
Baker MC (2008) Analysis of a cultural trait across an avian hybrid zone: geographic variation in plumage morphology and vocal traits in the Australian ringneck parrot (Platycercus zonarius). Auk 125:651–662
Baldwin JD, Baldwin JI (1976) Vocalizations of howler monkeys (Alouatta palliata) in Southwestern Panama. Folia Primatol 26:81–108
Bee MA, Perrill SA, Owen PC (2000) Male green frogs lower the pitch of acoustic signals in defense of territories: a possible dishonest signal of size? Behav Ecol 11:169–177
Bernstein IS (1964) A field study of the activities of howler monkeys. Anim Behav 12:92–97
Bicca-Marques JC, Mattje Prates H, Cunha R, de Aguiar F, Jones CB (2008) Survey of Alouatta caraya, the black-and-gold howler monkey, and Alouatta guariba clamitans, the brown howler monkey, in a contact zone, State of Rio Grande do Sul, Brazil: evidence for hybridization. Primates 49:246–252
Blair FW (1958) Mating call in the speciation of anuran amphibians. Am Nat 92:27–51
Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, Sunderland
Brockett RC, Horwich RH, Jones CB (1999) Disappearance of infants following male takeovers in the Belizean black howler monkey (Alouatta pigra). Neotrop Primates 7:86–88
Brown WL, Wilson EO (1956) Character displacement. Syst Zool 5:49–64
Bynum EL, Bynum DZ, Suprianta J (1997) Confirmation and location of the hybrid zone between wild populations of Macaca tonkeana and Macaca hecki in Central Sulawesi, Indonesia. Am J Primatol 43:181–209
Camargo CC, Ferrari SF (2007) Interactions between tayras (Eira barbara) and red-handed howlers (Alouatta belzebul) in eastern Amazonia. Primates 48:147–150
Carpenter CR (1934) A field study of the behavior and social relations of howling monkeys Alouatta palliata. Comp Psychol Monogr 10:1–168
Cäsar C, Zuberbühler K (2012) Referential alarm calling behaviour in New World primates. Curr Zool 58:680–697
Charlton BD, Ellis WAH, Brumm J, Nilsson K, Fitch WT (2012) Female koalas prefer bellows in which lower formants indicate larger males. Anim Behav 84:1565–1571
Cheney DL, Seyfarth RM, Palombit RA (1996) The function and mechanisms underlying baboon ‘contact’ barks. Anim Behav 52:507–518
Chiarello AG (1995) Role of loud calls in brown howlers, Alouatta fusca. Am J Primatol 36:213–222
Chivers DJ (1969) On the daily behaviour and spacing of howling monkey groups. Folia Primatol 10:48–102
Clark Arcadi A (1996) Phrase structure of wild chimpanzee pant hoots: patterns of production and interpopulation variability. Am J Primatol 39:159–178
Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72
Clutton-Brock TH, Albon SD (1979) The roaring in red deer and the evolution of honest advertisement. Behaviour 60:145–169
Collias NE, Southwick CH (1952) A field study of population density and social organization in howling monkeys. Proc Am Philos Soc 96:144–156
Cortés-Ortiz L, Bermingham E, Rico C, Rodrı́guez-Luna E, Sampaio I, Ruiz-Garcı́a M (2003) Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Mol Phylogenet Evol 26:64–81
Cortés-Ortiz L, Duda TF Jr, Canales-Espinosa D, García-Orduña F, Rodríguez-Luna E, Bermingham E (2007) Hybridization in large bodied New World primates. Genetics 176:2421–2425
Cristóbal-Azkarate J, Dias PAD, Joaquim JV (2004) Causes of intraspecific aggression in Alouatta palliata mexicana: evidence from injuries, demography, and habitat. Int J Primatol 25:939–953
Cristóbal-Azkarate J, Chavira R, Boeck L, Rodrígez-Luna E, Veàl JJ (2006) Testosterone levels of free-ranging resident mantled howler monkey males in relation to the number and density of solitary males: a test of the challenge hypothesis. Horm Behav 49:261–267
Crockett CM (1984) Emigration by female red howler monkeys and the case for female competition. In: Small M (ed) Female primates: studies by women primatologists. Liss, New York
Crockett CM, Eisenberg JF (1987) Howlers: variations in group size and demography. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago
Crockett CM, Sekulic R (1984) Infanticide in red howler monkeys (Alouatta seniculus). In: Hausfater G, Hrdy SB (eds) Infanticide: comparative and evolutionary perspectives. Aldine, Hawthorne
Crockford C, Herbinger I, Vigilant L, Boesch C (2004) Wild chimpanzees produce group-specific calls: a case for vocal learning? Ethology 110:221–243
da Cunha RGT (2004) A functional analysis of vocalisations of black howler monkeys (Alouatta caraya). PhD dissertation, University of St. Andrews
da Cunha RGT, Byrne RW (2006) Roars of black howling monkeys (Alouatta caraya): evidence for a function in inter-group spacing. Behaviour 143:1169–1199
da Cunha RGT, Jalles-Filho E (2007) The roaring of southern brown howler monkeys (Alouatta guariba clamitans) as a mechanism of active defense of borders. Folia Primatol 78:259–271
da Cunha RGT, de Oliveira DAG, Holzmann I, Kitchen DM (2015) Production of loud and quiet calls in howler monkeys. In: Kowalewski M, Garber P, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: Adaptive radiation, systematics, and morphology. Springer, New York
de Boer B (2009) Acoustic analysis of primate air sacs and their effect on vocalization. J Acoust Soc Am 126:3329–3343
de Kort SR, den Hartog PM, ten Cate C (2002) Vocal signals, isolation and hybridization in the vinaceous dove (Streptopelia vinacea) and the ring-necked dove (S. capicola). Behav Ecol Sociobiol 51:378–385
DeGusta D, Milton K (1998) Skeletal pathologies in a population of Alouatta palliata: behavioral, ecological, and evolutionary implications. Int J Primatol 19:615–650
Detwiler KM, Burrell AS, Jolly CJ (2005) Conservation implications of hybridization in African Cercopithecine Monkeys. Int J Primatol 26:661–684
Di Fiore A, Campbell CJ (2007) The Atelines: variation in ecology, behavior, and social organization. In: Campbell CJ, Fuentes A, Mackinnon KC, Panger M (eds) Primates in perspective. Oxford University Press, Oxford
Dias PAD, Rangel-Negrin A, Veà JJ, Canales-Espinosa D (2010) Coalitions and male–male behavior in Alouatta palliata. Primates 51:91–94
Drubbel RV, Gautier JP (1993) On the occurrence of nocturnal and diurnal loud calls, differing in structure and duration, in red howlers (Alouatta seniculus) of French Guyana. Folia Primatol 60:195–209
Eason P (1989) Harpy eagle attempts predation on adult howler monkeys. Condor 91:469–470
Eisenberg JF (1976) Communication mechanisms and social integration in the black spider monkey, Ateles fusciceps robustus, and related species. Smithson Contrib Zool 213:1–108
Elowson AM, Snowdon CT (1994) Pygmy marmosets, Cebuella pygmaea, modify vocal structure in response to changed social environment. Anim Behav 47:1267–1277
Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223
Farmer HL, Plowman AB, Leaver LA (2011) Role of vocalisations and social housing in breeding in captive howler monkeys (Alouatta caraya). Appl Anim Behav Sci 134:177–183
Fashing PJ (2001) Male and female strategies during inter-group encounters in guerezas (Colobus guereza): evidence for resource defense mediated through males and a comparison with other primates. Behav Ecol Sociobiol 50:219–230
Fialho MS, Setz EZF (2007) Extragroup copulations among brown howler monkeys in southern Brazil. Neotrop Primates 14:28–30
Fichtel C (2004) Reciprocal recognition of Sifaka (Propithecus verreauxi verreauxi) and red-fronted lemur (Eulemur fulvus rufus) alarm calls. Anim Cogn 7:45–52
Ficken MS, Ficken RW (1967) Singing behaviour of blue-winged and golden-winged warblers and their hybrid. Behaviour 28:149–181
Fischer J, Kitchen DM, Seyfarth RM, Cheney DL (2004) Baboon loud calls advertise male quality: acoustic features and their relation to rank, age and exhaustion. Behav Ecol Sociobiol 56:140–148
Fisher J, Hammerschmidt K, Todt D (1998) Local variation in Barbary macaque shrill barks. Anim Behav 56:623–629
Fitch WT, Hauser MD (1995) Vocal production in nonhuman primates—acoustics, physiology, and functional constraints on honest advertisement. Am J Primatol 37:191–219
FitzGibbon CD, Fanshawe JH (1988) Stotting in Thomson’s gazelles: an honest signal of condition. Behav Ecol Sociobiol 23:69–74
Frey R, Gebler A (2010) Mechanisms and evolution of roaring-like vocalization in mammals. In: Brudzynski SM (ed) Handbook of mammalian vocalization: an integrative neuroscience approach. Academic, London
Gabow SA (1975) Behavioral stabilization of a baboon hybrid zone. Am Nat 109:701–712
Geissman T, Mutschler T (2006) Diurnal distribution of loud calls in sympatric wild Indris (Indri indri) and ruffed lemurs (Varecia variegata): implications for call function. Primates 47:393–396
Gerhardt HC (1974) The vocalizations of some hybrid treefrogs: acoustic and behavioral analyses. Behaviour 49:130–151
Gil-da-Costa R, Palleroni A, Hauser MD, Touchton J, Kelley JP (2003) Rapid acquisition of an alarm response by a neotropical primate to a newly introduced avian predator. Proc R Soc Lond B 270:605–610
Glander KE (1978) Howling monkey feeding behavior and plant secondary compounds: a study of strategies. In: Montgomery GG (ed) The ecology of arboreal folivores. Smithsonian Institution Press, Washington, DC
Hauser MD (1993) The evolution of nonhuman primate vocalizations: effects of phylogeny, body weight, and social context. Am Nat 142:528–542
Hewitt GH (1988) Hybrid zones—natural laboratories for evolutionary studies. Trends Ecol Evol 3:158–167
Hill CM (1994) The role of female diana monkeys, Cercopithecus diana, in territorial defence. Anim Behav 47:425–431
Holzmann I, Agostini I, Di Bitetti M (2012) Roaring behavior of two syntopic howler species (A. caraya and A. guariba clamitans): evidence supports the mate defense hypothesis. Int J Primatol 33:338–355
Horwich RH, Gebhard K (1983) Roaring rhythms in black howler monkeys (Alouatta pigra) of Belize. Primates 24:290–296
Horwich RH, Lyon J (1990) A Belizean rain forest: the Community Baboon Sanctuary. Orangutan Press, Gays Mills
Horwich RH, Brockett RC, Jones CB (2000) Alternative male reproductive behaviors in the Belizean black howler monkey (Alouatta pigra). Neotrop Primates 8:95–98
Hughes M (2000) Deception with honest signals: signal residuals and signal function in snapping shrimp. Behav Ecol 11:614–623
Jones CB (1980) The functions of status in the mantled howler monkey, Alouatta palliata Gray: intraspecific competition for group membership in a folivorous Neotropical primate. Primates 21:389–405
Julliot C (1994) Predation of a young spider monkey (Ateles paniscus) by a crested eagle (Morphnus guianensis). Folia Primatol 63:75–77
Kelaita MA, Cortés-Ortiz L (2013) Morphological variation of genetically-confirmed Alouatta pigra × A. palliata hybrids from a natural hybrid zone in Tabasco, Mexico. Am J Phys Anthropol 150:223–234
Kirschel ANG, Blumstein DT, Smith TB (2009) Character displacement of song and morphology in African tinkerbirds. Proc Natl Acad Sci USA 106:8256–8261
Kitchen DM (2000) Aggression and assessment among social groups of Belizean black howler monkeys (Alouatta pigra). PhD dissertation, University of Minnesota
Kitchen DM (2004) Alpha male black howler monkey responses to loud calls: effect of numeric odds, male companion behaviour and reproductive investment. Anim Behav 67:125–139
Kitchen DM (2006) Experimental test of female black howler monkey (Alouatta pigra) responses to loud calls from potentially infanticidal males: effects of numeric odds, vulnerable offspring, and companion behavior. Am J Phys Anthropol 131:73–78
Kitchen DM, Beehner JC (2007) Factors affecting individual participation in group-level aggression in non-human primates. Behaviour 144:1551–1581
Kitchen DM, Seyfarth RM, Fischer J, Cheney DL (2003) Loud calls as indicators of dominance in male baboons (Papio cynocephalus ursinus). Behav Ecol Sociobiol 53:374–384
Kitchen DM, Horwich RH, James RA (2004) Subordinate male black howler monkey (Alouatta pigra) responses to loud calls: experimental evidence for the effects of intra-group male relationships and age. Behaviour 141:703–723
Lemaire F (1977) Mixed song, interspecific competition and hybridisation in the reed and marsh warblers (Acrocephalus scirpaceus and palustris). Behaviour 63:215–240
Lichtenberg SJ, Simmons J, Benefit B, McCrossin F, Kautz T, Arney I, Diaz LC, Diaz M, Diaz R, Milne R, Shendo B (2012) Differences between black howler (Alouatta pigra) group size and pattern of vocalizations in two ecologically different populations in northern Belize. Am J Phys Anthropol 147(suppl 54):193–194 (Abstract)
Marler P (1973) A comparison of vocalizations of red-tailed monkeys and blue monkeys, Cercopithecus ascanius and C. mitis, in Uganda. Z Tierpsychol 33:223–247
Maynard Smith J (1974) The theory of games and the evolution of animal conflicts. Theor Biol 47:208–221
Maynard Smith J, Parker GA (1976) The logic of asymmetric contests. Anim Behav 24:159–175
Maynard Smith J, Price GR (1973) The logic of animal conflict. Nature 246:15–18
McComb K, Packer C, Pusey A (1994) Roaring and numerical assessment in contests between groups of female lions, Panthera leo. Anim Behav 47:379–387
McKinney T (2009) Anthropogenic change and primate predation risk: crested caracaras (Caracara plancus) attempt predation on mantled howler monkeys (Alouatta palliata). Neotrop Primates 16:24–27
Milton K (1980) The foraging strategy of howler monkeys: a study in primates economics. Columbia University Press, New York
Miranda JMD, Bernardi IP, Moro-Rios RF, Aguiar LM, Ludwig G, Passos FC (2004) Social structure of Alouatta guariba clamitans: a group with a dominant female. Neotrop Primates 12:135–138
Miranda JMD, Bernardi IP, Moro-Rios RF, Passos FC (2006) Antipredator behavior of brown howlers attacked by black hawk-eagle in Southern Brazil. Int J Primatol 27:1097–1101
Mitani JC, Rodman PS (1979) Territoriality: the relation of ranging pattern and home range size to defendability, with an analysis of territoriality among primate species. Behav Ecol Sociobiol 5:241–251
Mitani JC, Hunley KL, Murdoch ME (1999) Geographic variation in the calls of wild chimpanzees: a reassessment. Am J Primatol 47:133–151
Morton ES (1977) On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. Am Nat 111:855–869
Moynihan M (1967) Comparative aspects of communication in New World primates. In: Morris D (ed) Primate ethology. Aldine, Chicago
Newman JD, Symmes D (1982) Inheritance and experience in the acquisition of primate acoustic behavior. Primate communication. Cambridge University Press, New York, p 259–278
Nunn CL (2000) Collective benefits, free-riders, and male extra-group conflict. In: Kappeler P (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge
Nunn CL, Lewis RJ (2001) Cooperation and collective action in animal behaviour. In: Noë R, van Hooff JARAM, Hammerstein P (eds) Economics in nature: social dilemmas, mate choice and biological markets. Cambridge University Press, Cambridge
Oliveira DAG (2002) Vocalizações de longo alcance de Alouatta fusca clamitans e Alouatta belzebul belzebul: estrutura e contexto. PhD dissertation, Universidade de São Paulo
Oliveira DAG, Ades C (2004) Long-distance calls in Neotropical primates. An Acad Bras Cienc 76:393–398
Owings DH, Morton ES (1998) Animal vocal communication: a new approach. Cambridge University Press, Cambridge
Owren MJ, Linker CD (1995) Some analysis methods that may be useful to acoustic primatologists. In: Zimmermann E, Newman JD, Jürgens U (eds) Current topics in primate vocal communication. Plenum Press, New York
Owren MJ, Dieter JA, Seyfarth RM, Cheney DL (1993) Vocalizations of rhesus (Macaca mulatta) and Japanese (M. fuscata) macaques cross-fostered between species show evidence of only limited modification. Dev Psychobiol 26:389–406
Parker GA (1974) Assessment strategy and the evolution of fighting behaviour. J Theor Biol 47:223–243
Payne RJH (1998) Gradually escalating fights and displays: the cumulative assessment model. Anim Behav 56:651–662
Peres CA (1990) A harpy eagle successfully captures an adult male red howler monkey. Wilson Bull 102:560–561
Poole JH (1989) Announcing intent: the aggressive state of musth in African elephants. Anim Behav 37:140–152
Rangel-Negrín A, Dias PAD, Chavira R, Canales-Espinosa D (2011) Social modulation of testosterone levels in male black howlers (Alouatta pigra). Horm Behav 59:159–166
Riede T, Tokuda IT, Munger JB, Thomson SL (2008) Mammalian laryngeal air sacs add variability to the vocal tract impedance: physical and computational modeling. J Acoust Soc Am 124:634–647
Schön Ybarra MA (1986) Loud calls of adult male red howling monkeys (Alouatta seniculus). Folia Primatol 47:204–216
Schön Ybarra MA (1988) Morphological adaptations for loud phonations in the vocal organ of howling monkeys. Primate Rep 22:19–24
Schön Ybarra MA (1995) A comparative approach to the non-human primate vocal tract: implications for sound production. In: Zimmermann E, Newman JD, Jürgens U (eds) Current topics in primate vocal communication. Plenum Press, New York
Scroggie MP, LittleJohn MJ (2005) Territorial vocal behavior in hybrid smooth froglets Geocrinia laevis complex (Anura: Myobatrachidae). Behav Ecol Sociobiol 58:72–79
Sekulic R (1982a) Daily and seasonal patterns of roaring and spacing in four red howler Alouatta seniculus troops. Folia Primatol 39:22–48
Sekulic R (1982b) The function of howling in red howler monkeys (Alouatta seniculus). Behaviour 81:38–54
Sekulic R (1982c) Behavior and ranging patterns of a solitary female red howler (Alouatta seniculus). Folia Primatol 38:217–232
Sekulic R (1982d) Male relationships and infant deaths in red howler monkeys (Alouatta seniculus). Z Tierpsychol 61:185–202
Sekulic R (1983) The effect of female calls on male howling in red howler monkeys (Alouatta seniculus). Int J Primatol 4:291–305
Sekulic R, Chivers DJ (1986) The significance of call duration in howler monkeys. Int J Primatol 7:183–190
Seyfarth RM, Cheney DL (1984) Grooming, alliances and reciprocal altruism in vervet monkeys. Nature 308:541–543
Seyfarth RM, Cheney DL (2010) Production, usage, and comprehension in animal vocalizations. Brain Lang 115:92–100
Širović A, Hildebrand JA, Wiggins SM (2007) Blue and fin whale call source levels and propagation range in the Southern Ocean. J Acoust Soc Am 122:1208–1215
Snowdon CT (1989) Vocal communication in New World monkeys. J Hum Evol 18:611–633
Snowdon CT (2004) Sexual selection and communication. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge
Southwick CH (1962) Patterns of intergroup social behavior in primates, with special reference to rhesus and howling monkeys. Ann N Y Acad Sci 102:436–454
Steenbeek R, Assink PR (1998) Individual differences long distance calls of male wild Thomas langurs (Presbytis thomasi). Folia Primatol 69:77–80
Steenbeek R, Piek RC, van Buul M, van Hooff JARM (1999) Vigilance in wild Thomas’s langurs (Presbytis thomasi): the importance of infanticide risk. Behav Ecol Sociobiol 45:137–150
Steinmetz S (2005) Vocalizações de longo alcance como comunicação intra-grupal nos bugios (Alouatta guariba). Neotrop Primates 13:11–15
Stevens JR, Hauser MD (2004) Why be nice? Psychological constraints on the evolution of cooperation. Trends Cogn Sci 8:60–65
Stevens JR, Volstor J, Schooler LJ, Rieskam J (2011) Forgetting constrains the emergence of cooperative decision strategies. Front Psychol Cogn Sci 1:1–12
Sun GZ, Huang B, Guan ZH, Geissmann T, Jiang XL (2011) Individuality in male songs of wild black crested gibbons (Nomascus concolor). Am J Primatol 73:431–438
Tenaza R (1985) Songs of hybrid gibbons (Hylobates lar × H. muelleri). Am J Primatol 8:249–253
Tinbergen N (1963) On aims and methods of ethology. Z Tierpsychol 20:410–433
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago
Van Belle S, Estrada A, Strier KB (2008) Social relationships among male Alouatta pigra. Int J Primatol 29:1481–1498
Van Belle S, Estrada A, Ziegler TE, Strier KB (2009a) Sexual behavior across ovarian cycles in wild black howler monkeys (Alouatta pigra): male mate guarding and female mate choice. Am J Primatol 71:153–164
Van Belle S, Estrada A, Ziegler TE, Strier KB (2009b) Social and hormonal mechanisms underlying male reproductive strategies in black howler monkeys (Alouatta pigra). Horm Behav 56:355–363
Van Belle S, Kulp AE, Thiessen-Bock R, Garcia M, Estrada A (2010) Observed infanticides following a male immigration event in black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. Primates 51:79–284
Waser P (1977) Individual recognition, intragroup cohesion and intergroup spacing: evidence from sound playback to forest monkeys. Behaviour 60:28–74
West SA, Griffin AS, Gardner A (2007) Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol 20:415–432
Whitehead JM (1985) Long distance vocalizations and spacing in mantled howling monkeys Alouatta palliata. PhD thesis, University of North Carolina, Chapel Hill
Whitehead JM (1987) Vocally mediated reciprocity between neighbouring groups of mantled howling monkeys, Alouatta palliata palliata. Anim Behav 35:1615–1627
Whitehead JM (1989) The effect of the location of a simulated intruder on responses to long-distance vocalizations of mantled howling monkeys, Alouatta palliata palliata. Behaviour 108:73–103
Whitehead JM (1994) Acoustic correlates of internal states in free-ranging primates: The example of the mantled howling monkey Alouatta palliata. In: Roeder JJ, Thierry B, Anderson JR, Herrenschmidt N (eds) Current primatology, vol II. Social development, learning and behaviour. Université Louis Pasteur, Strasbourg
Wich SA, Nunn CL (2002) Do male “long-distance calls” function in mate defense? A comparative study of long-distance calls in primates. Behav Ecol Sociobiol 52:47–484
Wich SA, Assink PR, Becher F, Sterck EHM (2002) Playbacks of loud calls to wild Thomas langurs (Primates; Presbytis thomasi): the effect of familiarity. Behaviour 139:79–87
Wiley RH, Poston J (1996) Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution 50:1371–1381
Wilson ML, Hauser MD, Wrangham RW (2001) Does participation in intergroup conflict depend on numerical assessment, range location, or rank for wild chimpanzees? Anim Behav 61:1203–1206
Wrangham RW, Rubenstein DI (1986) Social evolution in birds and mammals. In: Rubenstein DI, Wrangham RW (eds) Ecological determinants of social evolution. Princeton University Press, Princeton
Ydenberg RC, Giraldeau L-A, Falls JB (1988) Neighbours, strangers, and the asymmetric war of attrition. Anim Behav 36:343–347
Zahavi A (1977) The cost of honesty. J Theor Biol 67:603–605
Zucker EL, Clarke MR (1986) Male-male interactions in a group of free-ranging howling monkeys. Am J Primatol 10:443 (Abstract)
Acknowledgments
The coauthors are grateful to the anonymous reviewers and to the editors for constructive comments and for the opportunity to be involved in this book. RGTC is grateful to EMBRAPA, Richard Byrne, Marcelo Oliveira Maciel, Emiko Kawakami de Resende, José Anibal Comastri Filho, Gentil Cavalcanti, Marcos Tadeu, Sandra Santos, CAPES (studentship #1373/99 4), and St. Leonard’s College at University of St. Andrews (for Russell Trust Award). IH wishes to thank Mario Di Bitetti, Nacho Areta, Ilaria Agostini, and Daphne Colcombet, as well as The National Research Council from Argentina (CONICET) for funding. DMK is indebted to University of Minnesota (UMN), The Ohio State University (OSU), and NSF (grants # BCS-0962807 and 0962755) for funding. She is also grateful to UMN colleagues, advisors, and field assistants; L Cortes-Ortiz, T Bergman, PAD Dias, D Canales Espinosa, A Rangel-Negrin, C Rodriguez Muldonado, A Gomez Martinez, and A Coyohua; OSU colleagues, administrators, and students; and, most importantly, Jim, Dylan, and Nash Nicholson. DAGO wishes to thank César Ades (in memoriam), Zelinda Hirano, Júlio César de Souza Jr., Fernando Déscio, Simone Porfírio, Marcelo Marcelino, Isabel Coelho, Israel Quintani, and Esmeralda da Silva, for funding from CNPq, CAPES, FAPESP, and FINEP, as well as the following institutions: University of São Paulo, Instituto Florestal—P.E. da Cantareira, CEPESBI, FURB, Municipality of Indaial, and IBAMA/PB, RPPN Fazenda Pacatuba.
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Kitchen, D.M., da Cunha, R.G.T., Holzmann, I., de Oliveira, D.A.G. (2015). Function of Loud Calls in Howler Monkeys. In: Kowalewski, M., Garber, P., Cortés-Ortiz, L., Urbani, B., Youlatos, D. (eds) Howler Monkeys. Developments in Primatology: Progress and Prospects. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1957-4_14
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