Abstract
Our knowledge about the perceptual world of howler monkeys is unevenly distributed between the five senses. Whereas there is abundant knowledge about the sense of vision in the genus Alouatta, only limited data on the senses of hearing, smell, taste, and touch are available. The discovery that howler monkeys are the only genus among the New World primates to possess routine trichromacy has important implications for the evolution of color vision and therefore has been studied intensively. Detailed information about the genetic mechanisms and physiological processes underlying color vision in howler monkeys are available. Although the sound production, vocal repertoire, and acoustic communication in the genus Alouatta have been well documented, basic physiological measures of hearing performance such as audiograms are missing. Similarly, despite an increasing number of observational studies on olfactory communication in howler monkeys, there is a complete lack of physiological studies on the efficiency of their sense of smell. Information about the senses of taste and touch is even scarcer and mainly restricted to a description of their anatomical basis. A goal of this chapter is to summarize our current knowledge of the anatomy, physiology, genetics, and behavioral relevance of the different senses in howler monkeys in comparison to other platyrrhines.
Resumen
El conocimiento que tenemos de las percepciones en los monos aulladores no es igual para los cinco sentidos. Mientras que para el género Alouatta existe un vasto conocimiento acerca de la visión, existen datos limitados para el resto de sus sentidos, oído, olfato, gusto y tacto. El hallazgo de que los monos aulladores son el único género entre los primates del Nuevo Mundo que poseen una visión tricrómata, tiene una importante implicación para la evolución de la visión a color y por ello, ha sido ampliamente estudiada. Existe información detallada acerca de los mecanismos genéticos y procesos fisiológicos subyacentes a la visión del color en los aulladores, así como para la producción de sonido, el repertorio vocal y la comunicación acústica, aunque falta información de las medidas fisiológicas básicas de la audición, como son los audiogramas. De manera similar, a pesar del creciente número de estudios observacionales sobre la comunicación olfativa en los monos aulladores, no se cuentan con estudios fisiológicos sobre la eficiencia de su sentido del olfato. La información sobre los sentidos del gusto y el tacto es aún más limitada y, es restringida a su base anatómica. Este capítulo tiene como objetivo resumir el conocimiento actual acerca de la anatomía, fisiología, genética y la relevancia a nivel conductual del uso de los diferentes sentidos en los monos aulladores en comparación con otros platirrinos.
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References
Abee CR (1989) The squirrel monkey in biomedical research. ILAR J 31:11–20
Alport L (2007) A comparative analysis of lingual fungiform papillae and diet in primates. Am J Phys Anthropol 132:62
Alport L (2008) Intraspecific sex differences among primates in the density of lingual fungiform papillae. Am J Phys Anthropol 135:59
Araújo AC Jr, Didonet JJ, Araújo CS, Saletti PG, Borges TRJ, Pessoa VF (2008) Color vision in the black howler monkey (Alouatta caraya). Vis Neurosci 25:243–248
Baldwin JD, Baldwin JI (1976) Vocalizations of howler monkeys (Alouatta palliata) in Southwestern Panama. Folia Primatol 26:81–108
Baltisberger C (2003) Untersuchungen zur geruchlichen Kommunikation bei Brüllaffen (Alouatta palliata)—Eine Freilandstudie. Diploma Thesis, Biology, University of Munich, Germany
Baltisberger C, Laska M, Rodríguez-Luna E (2003) Olfactory communication in mantled howler monkeys (Alouatta palliata)—a field study. Folia Primatol 74:183–184
Bezanson M (2009) Life history and locomotion in Cebus capucinus and Alouatta palliata. Am J Phys Anthropol 140:508–517
Bicca-Marques JC (1992) Drinking behavior in the black howler monkey (Alouatta caraya). Folia Primatol 58:107–111
Bicca-Marques JC, Calegaro-Marques C (1995) Locomotion of black howlers in a habitat with discontinuous canopy. Folia Primatol 64:55–61
Bicca-Marques JC, Calegaro-Marques C (1998) Behavioral thermoregulation in a sexually and developmentally dichromatic neotropical primate, the black-and-gold howling monkey (Alouatta caraya). Am J Phys Anthropol 196:533–546
Bilgener M (1995) Chemical factors influencing food choice of howler monkeys (Alouatta palliata). Turk J Zool 19:291–303
Boissinot S, Zhou Y-H, Qiu L, Dulai KS, Neiswanger K, Schneider H, Sampaio I, Hunt DM, Hewett-Emmett D, Li W-H (1997) Origin and molecular evolution of the X-linked duplicate color vision genes in howler monkeys. Zool Stud 36:360–369
Boissinot S, Tan Y, Shyue S-K, Schneider H, Sampaio I, Neiswanger K, Hewett-Emmett D, Li W-H (1998) Origins and antiquity of X-linked triallelic color vision systems in New World monkeys. Proc Natl Acad Sci U S A 95:13749–13754
Bopp P (1954) Schwanzfunktionen bei Wirbeltieren. Rev Suisse Zool 61:83–100
Boscarol G, Falcone I, Fiore R, Gamba M, Giacoma C, Martinoli L, Piazza S, Pizzigalli C, Luna R (2004) Vocal repertoire of Alouatta palliata mexicana in Agaltepec. Folia Primatol 75:410–411
Brady AG (2000) Research techniques for the squirrel monkey (Saimiri sp). ILAR J 41:10–18
Brockett RC, Horwich RH, Jones CB (2005) Hand-holding by Belizean black howler monkeys: intentional communication in a neotropical primate. Folia Primatol 76:227–230
Bustos CA, Corkum LD, Slater KY, Mennill DJ (2008) Acoustic characteristics of the vocalizations of mantled howler monkeys (Alouatta palliata) in the fragmented low-land forests of Honduras. Am J Primatol 70:68
Caine NG, Mundy NI (2000) Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proc R Soc Lond B 267:439–444
Caine NG, Osorio D, Mundy NI (2010) A foraging advantage for dichromatic marmosets (Callithrix geoffroyi) at low light intensity. Biol Lett 6:36–38
Calegaro-Marques C, Bicca-Marques JC (1993) Reprodução de Alouatta caraya Humboldt, 1812 (Primates, Cebidar). A Primatologia Brasil 4:51–66
Cant JGH (1986) Locomotion and feeding postures of spider and howling monkeys. Field study and evolutionary interpretation. Folia Primatol 46:1–14
Carpenter CR (1934) A field study of the behavior and social relations of howling monkeys. Comp Psychol Monogr 10:1–168
Chiarello AG (1994) Diet of the brown howler monkey, Alouatta fusca, in a semi-deciduous forest fragment of southeastern Brazil. Primates 35:25–34
Chiarello AG (1995) Role of loud calls in brown howlers, Alouatta fusca. Am J Primatol 36:213–222
Chiarello AG (2005) Grooming in brown howler monkeys, Alouatta fusca. Am J Primatol 35:73–81
Chivers DJ (1969) On the daily behavior and spacing of howling monkey groups. Folia Primatol 10:48–102
Coleman MN (2009) What do primates hear? A meta-analysis of all known nonhuman primate behavioral audiograms. Int J Primatol 30:55–91
Coleman MN, Ross CF (2004) Primate auditory diversity and its influence on hearing performance. Anat Rec 281A:1123–1137
Cornick LA, Markowitz H (2002) Diurnal vocal patterns of the black howler monkey (Alouatta pigra) at Lamanai, Belize. J Mammal 83:159–166
Crockett CM (2003) Re evaluating the sexual selection hypothesis for infanticide by Alouatta males. In: Jones CB (ed) Sexual selection and reproductive competition in primates: new perspectives and directions, vol 3, Special topics in primatology. American Society of Primatology, Norman, pp 327–365
Da Cunha RGT, Byrne RW (2006) Roars of black howler 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
Daniel E (2007) Noise and hearing loss: a review. J Sch Health 77:225–231
Darian-Smith I (1982) Touch in primates. Annu Rev Psychol 33:155–194
De Boer B (2009) Acoustic analysis of primate air sacs and their effect on vocalization. J Acoust Soc Am 126:3329–3343
Delgado RA (2006) Sexual selection in the loud calls of male primates: signal content and function. Int J Primatol 27:5–25
Dias PAD, Rangel-Negrín A (2014) Diets in Howler Monkeys. In: Kowalewski M, Garber P, Cortes-Ortíz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology and conservation. Springer, New York
Dominy NJ, Lucas PW (2001) Ecological importance of trichromatic vision to primates. Nature 410:363–366
Dominy NJ, Lucas PW (2004) Significance of color, calories, and climate to the visual ecology of catarrhines. Am J Primatol 62:189–207
Dominy NJ, Garber PA, Bicca-Marques JC, de Azevedo-Lopes MA (2003a) Do female tamarins use visual cues to detect fruit rewards more successfully than do males? Anim Behav 66:829–837
Dominy NJ, Svenning JC, Li WH (2003b) Historical contingency in the evolution of primate color vision. J Hum Evol 44:25–45
Drubbel RV, Gatier 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
Dulai KS, von Dornum M, Mollon JD, Hunt DM (1999) The evolution of trichromatic color vision by opsin gene duplication in New World and Old World primates. Genome Res 9:629–638
Endler JA, Basolo AL (1998) Sensory ecology, receiver biases and sexual selection. Trends Ecol Evol 13:415–420
Epple G, Lorenz R (1967) Vorkommen, Morphologie und Funktion der Sternaldrüse bei den Platyrrhini. Folia Primatol 7:98–126
Espinosa-Gómez FC, Gómez-Rosales S, Wallis IR, Canales-Espinosa D, Hernández-Salazar LT (2013) Digestive strategies and food choice in mantled howler monkeys Alouatta palliata mexicana: bases of their dietary flexibility. J Comp Physiol B. doi:10.1007/s00360-013-0769-9
Estrada A (1984) Resource use by howler monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas, Veracruz, Mexico. Int J Primatol 5:105–131
Finlay BL, Franco ECS, Yamada ES, Crowley JC, Parsons M, Muniz JAPC, Silveira LCL (2008) Number and topography of cones, rods and optic nerve axons in New and Old World primates. Vis Neurosci 25:289–299
Franco ECS, Finlay BL, Silveira LCL, Yamada ES, Crowley JC (2000) Conservation of absolute foveal area in New World monkeys: a constraint on eye size and conformation. Brain Behav Evol 56:276–286
Galetti M, Pedroni F, Morellato LP (1994) Diet of the brown howler monkey Alouatta fusca in a forest fragment in southeastern Brazil. Mammalia 57:111–118
Garber PA, Kowalewski M (2012) Collective action and male affiliation in howler monkeys (Alouatta caraya). In: Sussman RW, Cloninger CR (eds) Origins of altruism and cooperation, developments in primatology: progress and prospects. Springer, New York
Gilad Y, Wiebe V, Przeworski M, Lancet D, Pääbo S (2004) Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol 2:120–125
Gilad Y, Wiebe V, Przeworski M, Lancet D, Pääbo S (2007) Correction: Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol 5:e148
Gil-da-Costa R, Palleroni A, Hauser MD, Touchton J, Kelley P (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 (1977) Poison in a monkey’s Garden of Eden. Nat Hist 86(3):35–41
Glander KE (1980) Reproduction and population growth in free-ranging mantled howling monkeys. Am J Phys Anthropol 53:25–36
Glander KE (1982) The impact of plant secondary compounds on primate feeding behavior. Yearb Phys Anthropol 25:1–18
Glaser D (1979) Gustatory preference behavior in primates. In: Kroeze JHA (ed) Preference behavior and chemoreception. IRL Press, London
Guillotin M, Dubost G, Sabatier D (1994) Food choice and food composition among the three major primate species of French Guiana. J Zool 233:551–579
Heffner RS (2004) Primate hearing from a mammalian perspective. Anat Rec 281A:1111–1122
Hickman GC (1979) The mammalian tail: a review of functions. Mammal Rev 9:143–157
Hiramatsu C, Melin AD, Aureli F, Schaffner CM, Vorobyev M, Matsumoto Y, Kawamura S (2008) Importance of achromatic contrast in short-range fruit foraging of primates. PLoS One 3:e3356
Hirano ZMB, Tramonte R, Silva ARM, Braga RR, dos Santos WF (2003) Morphology of epidermal glands responsible for the release of colored secretions in Alouatta guariba clamitans. Lab Primate Newslett 42:4–7
Hirano ZMB, Correa IC, de Oliveira DAG (2008) Contexts of rubbing behavior in Alouatta guariba clamitans: a scent-marking role? Am J Primatol 70:575–583
Hiwatashi T, Okabe Y, Tsutsui T, Hiramatsu C, Melin AD, Oota H, Schaffner CM, Aureli F, Fedigan LM, Innan H, Kawamura S (2010) An explicit signature of balancing selection for color-vision variation in New World monkeys. Mol Biol Evol 27:453–464
Hladik CM, Simmen B (1996) Taste perception and feeding behavior in nonhuman primates and human populations. Evol Anthropol 2:58–71
Hofer H (1977) Taste areas of the Plica sublingualis of Alouatta and Aotus (Primates, Platyrrhini). Cell Tissue Res 177:415–429
Hofer H, Meinel W, Rommel C (1979) Taste buds in the epithelium of the Plica sublingualis of New World monkeys. Anat Anz 145:17–31
Horwich RH (1983) Breeding behaviors in the black howler monkey (Alouatta pigra) of Belize. Primates 24:222–230
Hunt DM, Dulai KS, Cowing JA, Julliot C, Mollon JD, Bowmaker JK, Li W-H, Hewett-Emmett D (1998) Molecular evolution of trichromacy in primates. Vision Res 38:3299–3306
Jacobs GH, Deegan JF (2005) Polymorphic New World monkeys with more than three M/L cone types. J Opt Soc Am A 22:2072–2080
Jacobs GH, Neitz M, Deegan JF, Neitz J (1996) Trichromatic colour vision in New World monkeys. Nature 382:156–158
Joganic JL, Perry GH, Cunningham AJ, Dominy NJ, Verrelli BC (2009) Molecular evolution of color vision genes in howling monkeys (Alouatta). Am J Phys Anthropol 48(suppl):159–160
Jones CB (1979) Grooming in the mantled howler monkey, Alouatta palliata. Primates 20:289–292
Jones CB (2002) How important are urinary signals in Alouatta? Lab Primate Newslett 41:15–17
Jones CB (2003) Urine-washing behaviors as condition-dependent signals of quality by adult mantled howler monkeys (Alouatta palliata). Lab Primate Newslett 42:12–14
Jones CB, van Cantfort TE (2007) Multimodal communication by male mantled howler monkeys (Alouatta palliata) in sexual contexts: a descriptive analysis. Folia Primatol 78:166–185
Kaas JH (2004) Evolution of somatosensory and motor cortex in primates. Anat Rec 281A:1148–1156
Kainz PM, Neitz J, Neitz M (1998) Recent evolution of uniform trichromacy in a New World monkey. Vision Res 38:3315–3320
Kelemen G, Sade J (1960) The vocal organ of the howling monkey (Alouatta palliata). J Morphol 107:123–140
Kitchen DM (2004) Alpha male black howler monkeys 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 131:73–83
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
Laska M, Hernández-Salazar LT (2004) Gustatory responsiveness to monosodium glutamate and sodium chloride in four species of nonhuman primates. J Exp Zool 301A:898–905
Laska M, Tutsch M (2000) Laterality of tail resting posture in three species of New World primates. Neuropsychologia 38:1040–1046
Laska M, Scheuber HP, Hernández-Salazar LT, Rodriguez-Luna E (2003) Sour-taste tolerance in four species of nonhuman primates. J Chem Ecol 29:2637–2649
Laska M, Rivas-Bautista RM, Hernández-Salazar LT (2009) Gustatory responsiveness to six bitter tastants in three species of nonhuman primates. J Chem Ecol 35:560–571
Lucas PW, Darvell BW, Lee PKD, Yuen TDB, Choong MF (1998) Colour cues for leaf food selection by long-tailed macaques (Macaca fascicularis) with a new suggestion for the evolution of trichromatic colour vision. Folia Primatol 69:139–154
Lucas PW, Dominy NJ, Riba-Hernandez P, Stoner KE, Yamashita N, Lorí-Calderön E, Petersen-Pereira W, Rojas-Durán Y, Salas-Pena R, Solis-Madrigal S, Osorio D, Darvell WB (2003) Evolution and function of routine trichromatic vision in primates. Evolution 57:2636–2643
Machida H, Giacometti L (1967) The anatomical and histochemical properties of the skin of the external genitalia of the primates. Folia Primatol 6:48–69
Machida H, Giacometti L (1968) The skin. In: Malinow MR (ed) Biology of the howler monkey. Karger, New York, pp 126–140
Machida H, Perkins E, Giacometti L (1967) The anatomical and histochemical properties of the tongue of primates. Folia Primatol 5:264–279
Matsui A, Go Y, Niimura Y (2010) Degeneration of olfactory receptor gene repertoires in primates: no direct link to full trichromatic vision. Mol Biol Evol 27:1192–1200
Matsushita Y, Oota H, Welker BJ, Pavelka MS, Kawamura S (2013) Color vision variation as evidenced by hybrid L/M opsin genes in wild populations of trichromatic Alouatta New World monkeys. Int J Primatol. doi:10.1007/s10764-013-9705-9
McComb K, Semple S (2005) Coevolution of vocal communication and sociality in primates. Biol Lett 1:381–385
Melin AD, Fedigan LM, Hiramatsu C, Sendall CL, Kawamura S (2007) Effects of colour vision phenotype on insect capture by a free-ranging population of white-faced capuchins, Cebus capucinus. Anim Behav 73:205–214
Mendel F (1976) Postural and locomotor behavior of Alouatta palliata on various substrates. Folia Primatol 26:36–53
Milton K (1975) Urine-rubbing behavior in the mantled howler monkey, Alouatta palliata. Folia Primatol 23:105–112
Milton K (1979) Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. Am Nat 114:362–378
Milton K (1980) The foraging strategy of howler monkeys. Columbia University Press, New York
Osorio D, Smith AC, Vorobyev M, Buchanan-Smith HM (2004) Detection of fruit and the selection of primate visual pigments for color vision. Am Nat 164:696–708
Paterson JD (1981) Postural-positional thermoregulatory behavior and ecological factors in primates. Can Rev Phys Anthropol 3:3–11
Perkins EM (1975) Phylogenetic significance of the skin of New World monkeys (order Primates, infraorder Platyrrhini). Am J Phys Anthropol 42:395–424
Piazza S, Boscarol G, Falcone I, Fiore R, Gamba M, Giacoma C, Martinoli L, Pizzigalli C (2004) Acoustic features of loud calls in a group of Alouatta palliata mexicana: individual differences and connections with age. Folia Primatol 75:405–406
Pinto L, Setz E (2004) Diet of Alouatta belzebul discolor in an Amazonian rain forest of Northern Mato Grosso State, Brazil. Int J Primatol 25:1197–1211
Pubols LM (1968) Somatic sensory representation in the thalamic ventrobasal complex of the spider monkey (Ateles). Brain Behav Evol 1:305–323
Pubols BH, Pubols LM (1969) Forelimb, hindlimb, and tail dermatomes in the spider monkey (Ateles). Brain Behav Evol 2:132–159
Pubols BH, Pubols LM (1971) Somatotopic organization of spider monkey somatic sensory cortex. J Comp Neurol 141:63–76
Raguet-Schofield M (2010) The role of dietary toughness in the ontogeny of Nicaraguan mantled howler monkeys (Alouatta palliata) feeding behavior. Am J Phys Anthropol 141:193
Ramsier MA, Glander KE, Finneran JJ, Cunningham AJ, Dominy NJ (2009) Hearing, howling, and Hollywood: auditory sensitivity in Alouatta palliata is attuned to high-frequency infant distress calls. Am J Primatol 71:69
Ramsier M, Cunningham AJ, Patiño M, Villanea FA, Spoor F, Demes B, Larson S, Glander KE, Talebi M, Dominy NJ (2012) Hearing sensitivity and the evolution of acoustic communication in platyrrhine monkeys. Am J Phys Anthropol 147[suppl]:243
Regan BC, Julliot C, Simmen B, Viénot F, Charles-Dominique P, Mollon JD (1998) Frugivory and colour vision in Alouatta seniculus, a trichromatic platyrrhine monkey. Vision Res 38:3321–3327
Regan BC, Julliot C, Simmen B, Viénot F, Charles-Dominique P, Mollon JD (2001) Fruits, foliage and the evolution of primate colour vision. Philos Trans R Soc Lond B 356:229–283
Richter CP, Campbell KH (1940) Taste thresholds and taste preferences of rats for five common sugars. J Nutr 20:31–46
Rolls ET (2007) Sensory processing in the brain related to the control of food intake. Proc Nutr Soc 66:96–112
Rommel C (1981) Die sublingualen Strukturen der Primaten. Teil 1: Prosimiae, Platyrrhini und Cercophitecinae. Gegenbaurs Morph Jb 127:153–175
Sanchez-Villagra MR, Pope TR, Salas V (1998) Relation of intergroup variation in allogrooming to group social structure and ectoparasite loads in red howlers (Alouatta seniculus). Int J Primatol 19:473–491
Schmitt D, Larson SG (1995) Heel contact as a function of substrate type and speed in primates. Am J Phys Anthropol 96:39–50
Schön MA (1970) On the mechanism of modulating the volume of the voice in howling monkeys. Acta Oto Laryngol 70:443–447
Schön MA (1971) The anatomy of the resonating mechanism in howling monkeys. Folia Primatol 15:117–132
Schön Ybarra MA (1986) Loud calls of adult male red howling monkeys (Alouatta seniculus). Folia Primatol 47:204–216
Schön Ybarra MA (1988) Morphological adaptation for loud phonations in the vocal organ of howling monkeys. Primate Rep 22:19–24
Scott TR, Plata-Salaman CR (1999) Taste in the monkey cortex. Physiol Behav 67:489–511
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). Behavior 81:38–54
Sekulic R (1983) The effect of female call on male howling in red howler monkeys (Alouatta seniculus). Int J Primatol 4:291–305
Sekulic R, Chivers JR (1986) The significance of call duration in howler monkeys. Int J Primatol 7:183–190
Sekulic R, Eisenberg JF (1983) Throat-rubbing in red howler monkeys (Alouatta seniculus). In: Müller-Schwarze D, Silverstein M (eds) Chemical signals in vertebrates III. Plenum, New York, pp 347–350
Silveira LCL, Saito CA, Da Silva Filho M, Bowmaker JK, Kremers J, Lee BB (2007) Physiological properties of photoreceptors and retinal ganglion cells from a trichromatic platyrrhine: the howler monkey, Alouatta sp. In: Silveira LCL, Ventura DF, Lee BB (eds) 19th Symposium of the international colour vision society abstracts book EDUFPA, Belém, Brazil, pp 69–70
Simmen B, Sabatier D (1996) Diets of some French Guianan primates: food composition and food choices. Int J Primatol 17:661–693
Smith TD, Rossie JB (2006) Primate olfaction: anatomy and evolution. In: Brewer W, Castle D, Pantelis C (eds) Olfaction and the brain: window to the mind. Cambridge University Press, Cambridge, pp 135–166
Smith TD, Bhatnagar KP, Shimp KL, Kinzinger JH, Bonar CJ, Burrows AM, Mooney MP, Siegel MI (2002) Histological definition of the vomeronasal organ in human and chimpanzees, with a comparison to other primates. Anat Rec 267:166–176
Smith AC, Buchanan-Smith HM, Surridge AK, Osorio D, Mundy NI (2003) The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinus spp.). J Exp Biol 206:3159–3165
Smith AC, Surridge AK, Prescott MJ, Osorio D, Mundy NI, Buchanan-Smith HM (2012) Effect of colour vision status on insect prey capture efficiency of captive and wild tamarins (Saguinus spp.). Anim Behav 83:479–486
Stephan H, Baron G, Frahm HD (1982) Comparison of brain structure volumes in insectivora and primates. II. Accessory olfactory bulb (AOB). J Hirnforsch 23:575–591
Stephan H, Baron G, Frahm HD (1988) Comparative size of brains and brain components. In: Steklis H, Erwin J (eds) Comparative primate biology, vol 4. Alan R. Liss, New York
Stoner KE, Riba-Hernández P, Lucas PW (2005) Comparative use of color vision for frugivory by sympatric species of platyrrhines. Am J Primatol 67:399–409
Sumner P, Mollon JD (2000) Catarrhine photopigments are optimized for detecting targets against a foliage background. J Exp Biol 203:1963–1986
Talebi MG, Pope TR, Vogel ER, Neitz M, Dominy NJ (2006) Polymorphism of visual pigment genes in the muriqui (Primates, Atelidae). Mol Ecol 15:551–558
Teaford MF, Lucas PW, Ungar PS, Glander KE (2006) Mechanical defenses in leaves eaten by Costa Rican howling monkeys (Alouatta palliata). Am J Phys Anthropol 129:99–104
Urbani B (2002) A field observation on color selection by new world sympatric primates, Pithecia pithecia and Alouatta seniculus. Primates 43:95–101
Van Belle S, Bicca-Marques JC (2014) Insights into Reproductive Strategies and Sexual Selection in Howler Monkeys. In: Kowalewski M, Garber P, Cortes-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: Behavior, ecology and conservation. Springer, New York
Van Belle S, Estrada A, Ziegler TE, Strier KB (2009) 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
Vogel ER, Neitz M, Dominy NJ (2007) Effect of color vision phenotype on the foraging of wild white-faced capuchins, Cebus capucinus. Behav Ecol 18:292–297
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. 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: Thierry B, Roeder JJ, Anderson JR, Herrenschmidt N (eds) Current primatology, vol 2. University Louis Pasteur, Strasbourg, pp 221–226
Whitehead JM (1996) Vox Alouattinae: a preliminary survey of the acoustic characteristics of long-distance calls of howling monkeys. Int J Primatol 16:121–144
Youlatos D, Gasc JP (2011) Gait and kinematics of arboreal quadrupedal walk of free-ranging red howler in French Guiana. In: D’Août K, Vereecke EE (eds) Primate locomotion. Springer, New York
Youlatos D, Kowalewski M, Garber PA, Cortés-Ortiz L (2014) New challenges in the study of howler monkey anatomy, physiology, sensory ecology, and evolution: where we are and where we need to go? In: Kowalewski MM, Garber PA, Cortés-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: adaptive radiation, systematics, and morphology. Springer, New York
Young OP (1982) Tree-rubbing behavior of a solitary male howler monkey. Primates 23:303–306
Acknowledgments
We thank the editors of this volume for their invitation to contribute to the present volume. Many thanks go to Greg Willis for providing photographs of A. palliata. This chapter benefited from the comments of three anonymous referees whose input shaped its final form. We are greatly indebted to them and their effort.
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Salazar, L.T.H., Dominy, N.J., Laska, M. (2015). The Sensory Systems of Alouatta: Evolution with an Eye to Ecology. 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_12
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