1. Nocturnal primate social systems The nocturnal primates Features Diversity Slow loris! 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

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

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

4. 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 Tapetum shows nocturnal adaptation. (= small layer behind the retina to reflect light back to the retina) All strepsirhines have it.

5. 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 Nocturnal primates: social systems not well known

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

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

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

9. Microcebus spp. Cheirogaleidae

10. Cheirogaleus medius

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

12. Galagidae African FAST Matriarchies

13. 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 “Vertical clinging and leaping” 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?

17. Lepilemur “Vertical clinging and leaping” 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 Lepilemur

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 Special features of lemurs Reconstructing primate social evolution

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

20. 1. Dispersed pairs Schülke & Kappeler (2003) Anim Behav Phaner furcifer Cf Euoticus 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

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

22. Females Males “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) Schülke & Kappeler (2003) Anim Behav Females rarely meet each other

23. 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 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?) Frequent interactions of F and M

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-FRegular (all 8 FF)Rare (no fights) M-MNeverCommon (+ fights) F-MNeverIntermittent (F>M)

26. 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? 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

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

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

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

30. 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 Owl monkey, Aotus: Argentina

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

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

33. 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 3. Dispersed Multi-male social systems

34. 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) 3. Dispersed Multi-male social systems

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

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. 1.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: 1. Extinction of the large diurnal raptors 2. 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 1.adaptations to conserve energy (e.g. BMR, hibernation, sperm competition, small group size, seasonal breeding) Or 2.to maximize use of scarce resources (e.g. cathemerality, territoriality, female dominance, fibrous diet, weaning synchrony).

43. Energy frugality hypothesis (EFH) 1. Conserve energy (e.g. BMR, hibernation, sperm competition, small group size, seasonal breeding) 2. Maximize use of scarce resources (e.g. cathemerality, territoriality, female dominance, fibrous diet, weaning synchrony).

44. 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” Theories of primate social origins. But rare! Only Galago alleni? Even this is doubtful. Unknown in basal mammals! Reconstructing primate social evolution

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

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

47. 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) Theories of primate social origins.

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

49. Müller & Thallman (2000) Biol Rev

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