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Nocturnal primate social systems

Types of social system Dispersed pairs: Phaner Gregarious pairs: Aotus Dispersed multi-male: Mirza. Significance of nocturnal primates Special features of lemurs Reconstructing primate social evolution. Slow loris!. Nocturnal primate social systems. The nocturnal primates

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Nocturnal primate social systems

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  1. Types of social system Dispersed pairs: Phaner Gregarious pairs: Aotus Dispersed multi-male: Mirza Significance of nocturnal primates Special features of lemurs Reconstructing primate social evolution Slow loris! Nocturnal primate social systems The nocturnal primates Features Diversity

  2. Daubentoniidae Daubentonia Ayeaye Galagidae Nocturnal primates 18 genera > 60 spp (approx 25% of all primates) Daubentonia Lepilemur Microcebus, Allocebus, Mirza, Cheirogaleus, Phaner Avahi Galago, Galagoides, Otolemur, Euoticus Loris, Nycticebus, Arctocebus, Perodicticus Tarsius Aotus

  3. Galago spp Nocturnal primates: diversity still unknown and underestimated (see Table 3.1 in “Primates in Perspective 2007) E.g. Galago 8 species (Bearder 1987) 17 species (Bearder 1999, Primates) Questions: - How do people classify species? - On which criteria? Galago crassicaudatus

  4. Tapetum shows nocturnal adaptation. (= small layer behind the retina to reflect light back to the retina) All strepsirhines have it. Activity patterns NOCTURNAL DIURNAL CREPUSCULAR: activity peaks at dawn and dusk (no primates) CATHEMERAL: activity peaks occur both night and day e.g. Owl monkey Aotus Argentina: 5 h night, 4 h day Eulemur, Hapalemur, Varecia

  5. Nocturnal primates: social systems not well known Mostly solitary, hard to follow Sleeping groups have been wrongly interpreted as social groups Social networks can be complex Few studies of marked individuals, genetic parentage

  6. Why are most Nocturnal Primates solitary? Maybe a combination of: Small body size (Jarman-Bell principle) Insectivory (scramble competition) Predation pressure (crypsis) Nocturnality (coordination difficulty)

  7. Angwantibo Galago senegalensis “Parked” baby Mothers feed without infants

  8. Daubentoniidae Galagidae Some nocturnal primates Diversity... Daubentonia Lepilemur Lorisoidea Microcebus, Allocebus, Mirza, Cheirogaleus, Phaner Avahi Galago, Galagoides, Otolemur, Euoticus Loris, Nycticebus, Arctocebus, Perodicticus Tarsius Aotus

  9. Cheirogaleidae Microcebus spp.

  10. Cheirogaleus medius Cheirogaleidae

  11. Galagidae African FAST Lorisidae Asian/African SLOW Lorisoidea Fruits, insects, gums

  12. Galagidae African FAST Matriarchies

  13. Slender loris Loris Slow loris Slender loris Lorisidae Asian/African SLOW Insectivorous: Highly tolerant of toxin (e.g. ants) Head first ! Geckos and lizards Most faunivorous primates Slow loris is more frugivorous than other lorises

  14. Daubentonia Fruit / insect diet “Woodpecker” of Madagascar Slow (unafraid?) Primary rainforest, deciduous, secondary growth, cultivation, dry forest Solitary, FF HR = 36 ha, MM HR = 170 ha

  15. Tarsius is an anthropoid, not a lemuriform S-E Asia, traditionally 3 species, now 5 No field study on T. pumilus yet BW: very small = 58-141 g 100% animal diet, “Owl-like” Nocturnal, activity at sunset Fast, long day-range

  16. Tarsier T. bancanus: Nightly Path Length = MM 2,082 m FF 1,448 m Solitary but.. T. spectrum is monogamous (socioecological models) Prefers Ficus trees for sleeping Gestation around 6 months Birth seasonality among wild populations But NO seasonality among captives. Why? “Vertical clinging and leaping”

  17. Lepilemur Lepilemur Sportive lemurs Lepilemur Madagascar, originally 1 species, now 7 species (chromosome study) 100% plant diet Fast, long day-range, humid to dry forest (adaptable!) 3 species = Solitary 1 species = Dispersed pair (sleep together) 2 species = Mix of solitary and dispersed pair (but sleep together) 1 species = Unknown “Vertical clinging and leaping”

  18. Nocturnal primate social systems The nocturnal primates Types of social system Dispersed pairs: Phaner Gregarious pairs: Aotus Dispersed multi-male: Mirza Significance of nocturnal primates Specialfeatures of lemurs Reconstructing primate social evolution

  19. Phaner furcifer Microcebus Mouse lemur 1.Dispersed pairs (stable monogamy) 2. Cohesive pairs (gregarious) Aotus 3. Dispersed Multi-male social systems

  20. Phaner furcifer Cf Euoticus 1. Dispersed pairs Stable monogamy E.g. fork-marked lemur, Phaner furcifer 8 pairs, focal follows, studied for 3 years (excellent!) 330 gram (F = M) Gum diet >50% one species, 15-39 trees/range Schülke & Kappeler (2003) Anim Behav

  21. Close match of F and M territory Ranges as Minimum Convex Polygons F/M overlap 82% Neighbors overlap 11-18% Schülke & Kappeler (2003) Anim Behav

  22. Females rarely meet each other “Kernel” Ranges (95% and 50% core areas) F/M overlap: F 92%; M 52% (i.e. M range = larger) Neighbors overlap 3% (F) - 11% (M) Males Females Schülke & Kappeler (2003) Anim Behav

  23. Frequent interactions of F and M Sleep-time 8-38 sleeping sites per individual (tree-holes, or Mirza nests) 36% co-sleeping - i.e. choose to co-sleep Who approaches? 0.2 affiliative interactions / h (5 observation hours to see one interaction!) Groom, sit together (< 2 min) Hinde index: M > F (n= 4) … i.e. M approaches F (monitoring F’s cycle?) But low cohesiveness High F-M encounter rates (13x “chance”) - mainly at food trees BUT: Mean distance: > 100 m (cf. range diameter = ~200 m) < 15 m apart: 9% time

  24. F-M Aggression (within pairs) Frequent: 0.5 conflict / h, 60% over food F always dominant MM often fall, including to ground ! Interactions between pairs Frequent: 6 per night! Affiliation: F-F intermittent (all 8 focal FF) M-M never (mate competition?) Aggression: F-M intermittent (F > M) M-M common (include fights) F-F rare (no fights)

  25. Interactions between pairs: SUMMARY Frequent: 6 per night! AffiliationAggression F-F Regular (all 8 FF) Rare (no fights) M-M Never Common (+ fights) F-M Never Intermittent (F>M)

  26. Dispersed pair: summary. F-M shared their home range F and M have very low ‘cohesiveness’ (low % time together) Most F-M interactions = conflict! Two-third of time for food F & M mostly don’t know each other’s location Dispersed pair found in other species: Cheirogaleus, Lepilemur, Galagoides, Tarsius (?) i.e. dispersed pair not dependent on F-M dominance N.B.F-M dominance as lemur specialty. F = M body size Absent in other mammals (e.g. Lorisoids) Uniform in lemurs (40-50 species) Presumed ancestral condition - but why?

  27. Phaner furcifer 1.Dispersed pairs (stable monogamy) 2. Cohesive pairs (gregarious) Aotus

  28. Avahi Aotus Indriidae, cf. Indri, Propithecus 2. Cohesive (gregarious) pairs Owl monkey, Aotus (+ woolly lemur, Avahi) Fruit diet; cathemeral

  29. Owl monkey Aotus spp. The only nocturnal (cathemeral) monkey

  30. Owl monkey, Aotus: Argentina F-M generally close < 5 m apart ALL the time! M carries infant 80-90% time (certainty of paternity…) Intense F-F aggression ( wounds, deaths, replacements) Why? M-F relationship? Food? Mate competition? Fernandez-Duque

  31. Phaner furcifer Microcebus Mouse lemur 1.Dispersed pairs (stable monogamy) 2. Cohesive pairs (gregarious) Aotus 3. Dispersed Multi-male social systems

  32. Microcebus Mouse lemur Smallest = Pygmy mouse lemur = 30.6 g = 1.1 oz. !

  33. 3. Dispersed Multi-male social systems Solitary feeding MM generally aggressive to other MM MM bigger ranges > FF (hence  overlap several FF’s range) FF share range with kin in ‘matriarchies’ or ‘associations’ FF in one ‘association’ aggressive to neighbors May be floaters or immigrant MM Large testes (sperm competition) Microcebus Mouse lemur

  34. 3. Dispersed Multi-male social systems Galagoides demidoff Matriarchies (= sleeping groups) MM: Central ‘A’: big; overlap ≥ 1 F = ‘association’ Central ‘B’: tolerated by ‘A’; little contact with FF Peripheral [cf. followers?] Nomadic (emigrants) cf. Mirza, Microcebus, Daubentonia, Loris (+ several Galagidae)

  35. F ranges overlap up to 99% (differs from 1.) Spatially clumped matrilines Dispersing FF fail Adult MM disperse, breed Breeding season: MM travel ( 4x area), mate  Multiple paternity within matrilines Coquerel’s dwarf lemur, Microcebus coquereli (genus name changed in 1985, was Mirza) Kinship and paternity assessed genetically 3-year study Solitary; social interactions rare No territorial defense seen Kappeler et al (2003) Nature

  36. Nocturnal primate social systems The nocturnal primates Types of social system Dispersed pairs: Phaner Gregarious pairs: Aotus Dispersed multi-male: Mirza Significance of nocturnal primates Special features of lemurs Reconstructing primate social evolution

  37. Special features of lemurs Female dominance Targeted female-female aggression Lack of sexual dimorphism High infant mortality Cathemerality Strict seasonal breeding (Wright 1999) 1. Energy conservation hypothesis (ECH) (Jolly 1966) 2. Evolutionary disequilibrium hypothesis (EVDH) (van Schaik & Kappeler 1996) 3. Energy frugality hypothesis (EFH) (Wright 1999)

  38. Energy conservation hypothesis (ECH) (Jolly 1966) • To explain the evolution of female dominance in lemurs • Suggests that Madagascar ecology and environment is challenging (strong seasonality) • Energetic stress, especially on reproductively active lemur females (evidence of birth seasonality?...)

  39. Synchronized weaning, asynchronized birth Wright, 1999

  40. 2. Evolutionary disequilibrium hypothesis (EVDH) • (van Schaik & Kappeler 1996) • Explain evolution of traits that show lack of convergence between gregarious lemurs and anthropoids • States that large-scale ecological changes (deforestation, arid habitats, erosion) during last 1500 years resulted in: • Extinction of the large diurnal raptors • Loss of 16 species of large-bodied lemurs

  41. Evolutionary disequilibrium hypothesis (EVDH) (van Schaik & Kappeler 1996) Loss of diurnal lemurs  rapid evolution of cathemerality, pair-living?

  42. 3. Energy frugality hypothesis (EFH) Energy conservation Maximize energy gain • Postulates the majority of lemur traits are either • adaptations to conserve energy • (e.g. BMR, hibernation, sperm competition, small group size, seasonal breeding) • Or • to maximize use of scarce resources • (e.g. cathemerality, territoriality, female dominance, fibrous diet, weaning synchrony).

  43. Energy frugality hypothesis (EFH) • Conserve energy • (e.g. BMR, hibernation, sperm competition, small group size, seasonal breeding) • Maximize use of scarce resources • (e.g. cathemerality, territoriality, female dominance, fibrous diet, weaning synchrony).

  44. Reconstructing primate social evolution Theories of primate social origins. 1. “Dispersed Harem” (Martin, 1995). “It seems likely that the ancestral social system was of the dispersed harem type, with some males possessing home ranges overlapping those of several females and with surplus males peripheralized in some way” But rare! Only Galago alleni? Even this is doubtful. Unknown in basal mammals!

  45. Theories of primate social origins. 2. “Gregarious Pair”. Avahi (wooly lemur) secondarily nocturnal? Other Indriidae diurnal Small olfactory bulb But only occurs in primates that are secondarily nocturnal! So - arose from diurnal pairing?

  46. Theories of primate social origins. 3. “Dispersed Pair” (Jolly 1998). Pairing = ancestral pattern for diurnal lemurs?

  47. Theories of primate social origins. 4. “Dispersed Multi-male system” (Müller & Thallman 2000). Commonest pattern in basal mammals Females separate (matriarchies in Mirza, Galago) Males overlap (may be alpha-beta relations)

  48. KEY Social networks MM Multi-male Pro MM/P MM/P Pro Pro P MM/P Pro P P Pair Pro Promiscuous MM/P P/Pro Pro Pro Pro Non-primate mammals Reconstructing early primate social organization Müller & Thallman (2000) Biol Rev

  49. Müller & Thallman (2000) Biol Rev

  50. Zhangeotherium quisquecuspideus 140-120 mya 5 inches long Early placental mammal Eosimias 40 mya Early haplorhine?

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