دورية أكاديمية

Direct links between resource availability and activity budget better reveal ecological patterns of endangered Coimbra-Filho's titi monkey.

التفاصيل البيبلوغرافية
العنوان: Direct links between resource availability and activity budget better reveal ecological patterns of endangered Coimbra-Filho's titi monkey.
المؤلفون: Souza-Alves JP; Programa de Pós-graduação em Ciências Biológicas, Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, João Pessoa, Paraíba, Brazil. souzaalves1982@gmail.com.; Programa de Pós-graduação em Biologia Animal, Centro de Biociências, Departamento de Zoologia, Universidade Federal de Pernambuco, Recife, Pernambuco, Brazil. souzaalves1982@gmail.com.; Centro de Biociências, Departamento de Zoologia, Universidade Federal de Pernambuco, Recife, Pernambuco, Brazil. souzaalves1982@gmail.com.; Laboratório de Ecologia, Centro de Biociências, Comportamento e Conservação (LECC), Universidade Federal de Pernambuco, Recife, Brazil. souzaalves1982@gmail.com., Hilário RR; Departamento de Meio Ambiente e Desenvolvimento, Universidade Federal de Amapá, Macapá, Brazil., Fontes IP; Secretaria Municipal de Meio Ambiente, Aracaju, Sergipe, Brazil., Thomas WW; The New York Botanical Garden, Bronx, NY, USA., de Vasconcellos Barbosa MR; Programa de Pós-graduação em Ciências Biológicas, Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, João Pessoa, Paraíba, Brazil.
المصدر: Primates; journal of primatology [Primates] 2024 Jan; Vol. 65 (1), pp. 49-59. Date of Electronic Publication: 2023 Oct 08.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Springer Tokyo Country of Publication: Japan NLM ID: 0401152 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1610-7365 (Electronic) Linking ISSN: 00328332 NLM ISO Abbreviation: Primates Subsets: MEDLINE
أسماء مطبوعة: Publication: 2003- : Tokyo : Springer Tokyo
Original Publication: Inuyama, Japan, Japan Monkey Centre.
مواضيع طبية MeSH: Callicebus* , Pitheciidae*, Animals ; Haplorhini ; Diet ; Fruit ; Primates ; Seasons ; Feeding Behavior
مستخلص: Many primatological studies do not assess direct indexes of food availability to make inferences about behavioral strategies. We related the diet and behavior of a group of Callicebus coimbrai in northeastern Brazil to fruit availability indexes and compared this pattern between seasons (direct and indirect assessment of food availability) to assess whether direct and indirect approaches detect similar ecological patterns. We monitored the study group for 33 months (5 days/month) via scan sampling. The monthly availability of fruits and new leaves was recorded in phenological transects. Fruit availability varied across years based on fruit prevalence, and timing and duration of the abundant seasons. We did not find evidence of a time-minimizing strategy, since C. coimbrai did not change its activity levels according to food availability. However, the negative relationship between foraging and fruit availability indicates that C. coimbrai can compensate for the lower fruit availability by increasing the search for alternative food sources. Monthly fruit consumption was positively correlated to fruit availability and negatively related to the consumption of other food items. However, the behavioral and feeding profiles did not vary between seasons and were not related to rainfall levels. Primate studies should directly relate behavioral and feeding profiles to fruit availability indices, thus avoiding using seasons as proxies of food availability.
(© 2023. The Author(s), under exclusive licence to Japan Monkey Centre.)
References: Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267. (PMID: 459740510.1163/156853974X00534)
Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121. (PMID: 10.1111/j.1095-8339.2009.00996.x)
Arseneau-Robar TJM, Changasi AH, Turner E, Teichroeb JA (2021) Diet and activity budget in Colobus angolensis ruwenzorii at Nabugabo, Uganda: are they energy maximizers? Folia Primatol 92(1):35–48. (PMID: 10.1159/000511046)
Babweteera F, Plumptre AJ, Adamescu GS et al (2018) The ecology of tree reproduction in an African medium altitude rain forest. Biotropica 50(3):405–417. (PMID: 10.1111/btp.12563)
Bicca-Marques JC, Heymann EW (2013) Ecology and behaviour of titi monkey (genus Callicebus). In: Veiga LM, Barnett AA, Ferrari SF, Norconk MA (eds) Evolutionary Biology and Conservation of Titis, Sakis, and Uacaris. Cambridge University Press, Cambridge, pp 196–207. (PMID: 10.1017/CBO9781139034210.023)
Boyer D, Ramos-Fernández G, Miramontes O et al (2006) Scale-free foraging by primates emerges from their interaction with a complex environment. Proc Royal Soc B: Biol Sci 273(1595):1743–1750. (PMID: 10.1098/rspb.2005.3462)
Caselli CB, Setz ES (2011) Feeding ecology and activity pattern of black-fronted titi monkeys (Callicebus nigrifrons) in a semideciduous tropical forest of southern Brazil. Primates 52:351–359. (PMID: 2186111510.1007/s10329-011-0266-2)
Chagas RRD, Ferrari SF (2010) Habitat use by Callicebus coimbrai (Primates: Pitheciidae) and sympatric species in the fragmented landscape of the Atlantic Forest of southern Sergipe, Brazil. Zoologia (Curitiba) 27:853–860. (PMID: 10.1590/S1984-46702010000600003)
Chapman CA, Naughton L, Lawes ML, Wasserman MD (2004) Conservation value of forest fragments: explanations for population declines of Colobus in Western Uganda. Folia Primatol 75:30–31.
Chapman CA, Valenta K, Bonnell TR et al (2018) Solar radiation and ENSO predict fruiting phenology patterns in a 15-year record from Kibale National Park. Uganda Biotropica 50(3):384–395. (PMID: 10.1111/btp.12559)
Chaves ÓM, Stoner KE, Arroyo-Rodríguez V (2011) Seasonal differences in activity patterns of geoffroyis’ spider monkeys (Ateles geoffroyi) living in continuous and fragmented forests in Southern Mexico. Int J Primatol 32:960–973. (PMID: 10.1007/s10764-011-9515-x)
Di Bitetti MS, Janson CH (2000) When will the stork arrive? patterns of birth seasonality in neotropical primates. Am J Primatol 50(2):109–130. (PMID: 1067670810.1002/(SICI)1098-2345(200002)50:2<109::AID-AJP2>3.0.CO;2-W)
Dinsmore MP, Strier KB, Louis EE Jr (2021) The influence of seasonality, anthropogenic disturbances, and cyclonic activity on the behavior of northern sportive lemurs (Lepilemur septentrionalis) at Montagne des Français Madagascar. Am J Primatol 83(12):e23333. (PMID: 3467919410.1002/ajp.23333)
Dunham AE, Razafindratsima OH, Rakotonirina P, Wright PC (2018) Fruiting phenology is linked to rainfall variability in a tropical rain forest. Biotropica 50(3):396–404. (PMID: 10.1111/btp.12564)
Dunn JC, Asensio N, Arroyo-Rodríguez V et al (2012) The ranging costs of a fallback food: liana consumption supplements diet but increases foraging effort in howler monkeys. Biotropica 44(5):705–714. (PMID: 10.1111/j.1744-7429.2012.00856.x)
Erhart EM, Overdorff DJ (2008) Spatial memory during foraging in prosimian primates: Propithecus edwardsi and Eulemur fulvus rufus. Folia Primatol 79(4):185–196. (PMID: 10.1159/000112911)
Estrada A, Garber PA, Rylands AB et al (2017) Impending extinction crisis of the world’s primates: why primates matter. Sci Adv 3(1):e1600946. (PMID: 28116351524255710.1126/sciadv.1600946)
Estrada A, Garber PA, Mittermeier RA et al (2018) Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation. PeerJ 6:e4869. (PMID: 29922508600516710.7717/peerj.4869)
Estrada A, Garber PA, Gouveia S et al (2022) Global importance of Indigenous Peoples, their lands, and knowledge systems for saving the world’s primates from extinction. Sci Adv 8(31):eabn2927. (PMID: 35947670936528410.1126/sciadv.abn2927)
Ferrari SF, Hilário RR (2014) Seasonal variation in the length of the daily activity period in buffy-headed marmosets (Callithrix flaviceps): an important consideration for the analysis of foraging strategies in observational field studies of primates. Am J Primatol 76:385–392. (PMID: 2432349510.1002/ajp.22242)
Frankie GW, Baker HG, Opler PA (1974) Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. J Ecol 62:881–919. (PMID: 10.2307/2258961)
Ganzhorn JU, Klaus S, Ortmann S, Schmid J (2003) Adaptations to seasonality: some primates and nonprimate examples. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. The University of Chicago Press, Chicago and London, pp 132–148.
Grueter CC, Li D, Ren B, Li M (2013) Overwintering strategy of Yunnan snub-nosed monkeys: adjustments in activity scheduling and foraging patterns. Primates 54:125–135. (PMID: 2316094310.1007/s10329-012-0333-3)
Hilário RR, Moraes B, Souza-Alves JP, Ferrari SF (2022) The density of Callicebus coimbrai is better predicted by vegetation structure variables than by surrounding landscape. Int J Primatol. https://doi.org/10.1007/s10764-022-00278-y. (PMID: 10.1007/s10764-022-00278-y)
Hilty SL (1980) Flowering and fruiting periodicity in a premontane rain forest in Pacific Colombia. Biotropica 12:292–306. (PMID: 10.2307/2387701)
Janzen DH (1967) Synchronization of sexual reproduction of trees within the dry season in Central America. Evolution 21(3):620–637. (PMID: 2856368510.2307/2406621)
Jenik J, Longman KA. 1987. Tropical forest and its environment. 2nd ed. Longman Scientific & Technical.
Jerusalinsky L, Souza-Alves JP, Ferrari SF (2020) Callicebus coimbrai. The IUCN Red List of Threatened Species 2020: e.T39954A17972422. https://doi.org/10.2305/IUCN.UK.2020-3.RLTS.T39954A17972422.en . Accessed on 24 April 2023.
Kinap NM, Nagy-Reis M, Bobrowiec PED et al (2021) Influence of topography gradient and seasonality on primate habitat use in Central Amazonia. Mamm Biol 101:251–259. (PMID: 10.1007/s42991-021-00108-3)
Kobayashi S, Langguth A (1999) A new species of titi monkey, Callicebus Thomas, from north-eastern Brazil (Primates, Cebidae). Rev Brasil Zool 16:531–551. (PMID: 10.1590/S0101-81751999000200018)
Martinez J, Wallace RB, Domic E, López L, Nekaris KAI (2022) Seasonal ecological flexibility of a threatened Bolivian endemic: Olalla’s titi monkey (Plecturocebus olallae). Int J Primatol. https://doi.org/10.1007/s10764-021-00276-6. (PMID: 10.1007/s10764-021-00276-6)
Mendoza I, Peres CA, Morellato LPC (2017) Continental-scale patterns and climatic drivers of fruiting phenology: a quantitative neotropical review. Glob Planet Change 148:227–241. (PMID: 10.1016/j.gloplacha.2016.12.001)
Monasterio M, Sarmiento G (1976) Phenological strategies of plant species in the tropical savanna and the semi-deciduous forest of the Venezuelan Llanos. J Biogeog 3:325–355. (PMID: 10.2307/3037976)
Mourthé I (2014) Response of frugivorous primates to changes in fruit supply in a northern Amazonian forest. Braz J Biol 74:720–727. (PMID: 2529622410.1590/bjb.2014.0088)
Nagy-Reis MB, Setz EZ (2017) Foraging strategies of black-fronted titi monkeys (Callicebus nigrifrons) in relation to food availability in a seasonal tropical forest. Primates 58:149–158. (PMID: 2748574610.1007/s10329-016-0556-9)
Ni Q, Xie M, Grueter CC et al (2015) Effects of food availability and climate on activity patterns of western black-crested gibbons in an isolated forest fragment in southern Yunnan, China. Primates 56:351–363. (PMID: 2627566410.1007/s10329-015-0481-3)
Njoku E (1963) Seasonal periodicity in the growth and development of some forest trees in Nigeria I observations on mature Trees. J Ecol 51:617–624. (PMID: 10.2307/2257750)
Norberg RA (1977) An ecological theory on foraging time and energetics and choice of optimal food-searching method. J Anim Ecol 46:511–529. https://doi.org/10.2307/3827. (PMID: 10.2307/3827)
Pinheiro J, Bates D, R Core Team (2023) nlme: linear and nonlinear mixed effects models. R Packag Version 3:1–162.
R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Richards PW (1996) The tropical rain forest: an ecological study. Cambridge University Press, Cambridge, England.
Rímoli J, dos Santos NR, Júnior AÉL (2012) Diet and activity patterns of black howler monkeys Alouatta caraya (Humboldt, 1812, Primates, Atelidae) in ecotone Cerrado-Pantanal in the left bank of Aquidauana River, Mato Grosso do Sul. Brazil Oecol Aust 16(4):933–948. (PMID: 10.4257/oeco.2012.1604.15)
Santana MM, Souza-Alves JP, Ferrari SF (2014) Twinning in titis (Callicebus coimbrai): stretching the limits of biparental infant caregiving? Neotrop Primates 21(2):189–191. (PMID: 10.1896/044.021.0205)
Santos GP, Galvão C, Young RJ (2012) The diet of wild black-fronted titi monkeys Callicebus nigrifrons during a bamboo masting year. Primates 53:265–272. (PMID: 2231107210.1007/s10329-012-0295-5)
Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2(1):369–404. (PMID: 10.1146/annurev.es.02.110171.002101)
Sefczek TM, Hagenson RA, Randimbiharinirina DR et al (2020) Home range size and seasonal variation in habitat use of aye-ayes (Daubentonia madagascariensis) in Torotorofotsy Madagascar. Folia Primatol 91(6):558–574. (PMID: 10.1159/000508620)
Sengupta A, Radhakrishna S (2016) Influence of fruit availability on fruit consumption in a generalist primate, the rhesus macaque Macaca mulatta. Int J Primatol 37:703–717. (PMID: 10.1007/s10764-016-9933-x)
Silva LP, Santana LM, de Melo FR (2021) Effect of seasonality on the feeding behavior of martins’ bare-faced tamarin Saguinus martinsi martinsi (Primates: Callitrichidae) in the Brazilian Amazon. Primate Conserv 35:1–9.
Souza-Alves JP, Fontes IP, Ferrari SF (2011a) Use of sleeping sites by a titi group (Callicebus coimbrai) in the Brazilian Atlantic Forest. Primates 52:155–161. (PMID: 2131194910.1007/s10329-011-0235-9)
Souza-Alves JP, Fontes IP, Chagas RR, Ferrari SF (2011b) Seasonal versatility in the feeding ecology of a group of titis (Callicebus coimbrai) in the northern Brazilian Atlantic Forest. Am J Primatol 73(12):1199–1209. (PMID: 2189851310.1002/ajp.20990)
Souza-Alves JP, Thomas WW, Barbosa MRV (2018) Phytosociology of angiosperms in a highly-fragmented landscape of Coastal Atlantic Forest in Northeastern Brazil. Rev Nord Biol 26(1):124–137.
Souza-Alves JP, Caselli CB, Gestich CC, Nagy-Reis MB (2019a) Should I store, or should I sync? The breeding strategy of two small Neotropical primates under predictable resource availability. Primates 60(2):113–118. (PMID: 3078862410.1007/s10329-019-00716-1)
Souza-Alves JP, Mourthe I, Hilário RR et al (2019b) Terrestrial behavior in titi monkeys (Callicebus, Cheracebus, and Plecturocebus): Potential correlates, patterns, and differences between genera. Int J Primatol 40:553–572. (PMID: 10.1007/s10764-019-00105-x)
Souza-Alves JP, Chagas RR, Santana MM et al (2021a) Food availability, plant diversity, and vegetation structure drive behavioral and ecological variation in endangered Coimbra-Filho’s titi monkeys. Am J Primatol 83(3):e23237. (PMID: 3352887210.1002/ajp.23237)
Souza-Alves JP, Baccaro FB, Fontes IP et al (2021b) For emergency only: terrestrial feeding in Coimbra-Filho’s titis reflects seasonal arboreal resource availability. Primates 62(1):199–206. (PMID: 3286237310.1007/s10329-020-00859-6)
Stevenson PR, Link A (2010) Fruit preferences of Ateles belzebuth in Tinigua Park, northwestern Amazonia. Int J Primatol 31:393–407. (PMID: 10.1007/s10764-010-9392-8)
Stevenson PR, Quiñones MJ, Ahumada JA (2000) Influence of fruit availability on ecological overlap among four neotropical primates at Tinagua National Park, Colombia. Biotropica 32:533–544. (PMID: 10.1111/j.1744-7429.2000.tb00499.x)
Trapanese C, Meunier H, Masi S (2019) What, where and when: spatial foraging decisions in primates. Biol Rev 94(2):483–502. (PMID: 3021197110.1111/brv.12462)
Van Schaik CP, Terborgh JW, Wright SJ (1993) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annu Rev Ecol Syst 24(1):353–377. (PMID: 10.1146/annurev.es.24.110193.002033)
Wright SJ, Calderon O (1995) Phylogenetic patterns among tropical flowering phenologies. J Ecol 83:937–948. (PMID: 10.2307/2261176)
Wright SJ, Calderón O (2018) Solar irradiance as the proximate cue for flowering in a tropical moist forest. Biotropica 50(3):374–383. (PMID: 10.1111/btp.12522)
Zhou J, Li WB, Wang X, Li JH (2022) Seasonal change in activity rhythms and time budgets of Tibetan macaques. Biology 11(9):1260. (PMID: 36138739949546710.3390/biology11091260)
معلومات مُعتمدة: 307648/2010-9 Conselho Nacional de Desenvolvimento Científico e Tecnológico; 562310/2010-0 Conselho Nacional de Desenvolvimento Científico e Tecnológico; 0846_20092 Fundação Grupo Boticário de Proteção à Natureza
فهرسة مساهمة: Keywords: Adaptability; Availability of resources; Behavioral patterns; Coimbra-Filho’s titi monkey; Feeding ecology; Seasonality
SCR Organism: Callicebus coimbrai
تواريخ الأحداث: Date Created: 20231008 Date Completed: 20240119 Latest Revision: 20240123
رمز التحديث: 20240123
DOI: 10.1007/s10329-023-01095-4
PMID: 37805969
قاعدة البيانات: MEDLINE
الوصف
تدمد:1610-7365
DOI:10.1007/s10329-023-01095-4