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

18 genera

> 60 spp (approx 25% of all primates)

Daubentonia Ayeaye

Aotus

AvahiMicrocebus, Allocebus, Mirza, Cheirogaleus, PhanerLepilemur

Loris, Nycticebus, Arctocebus, Perodicticus

Galago, Galagoides, Otolemur, EuoticusGalagidae

Daubentoniidae Daubentonia

Nocturnal primates

Tarsius

Galago crassicaudatus

E.g. Galago8 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)

Activity patterns

NOCTURNAL

DIURNAL

CREPUSCULAR: activity peaks at dawn and dusk (no primates)

CATHEMERAL: activity peaks occur both night and daye.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.

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

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:

Angwantibo

Galago senegalensis

“Parked” baby

Mothers feed without infants

Some nocturnal primatesDiversity...

Lorisoidea

Aotus

AvahiMicrocebus, Allocebus, Mirza, Cheirogaleus, PhanerLepilemur

Loris, Nycticebus, Arctocebus, Perodicticus

Galago, Galagoides, Otolemur, EuoticusGalagidae

Daubentoniidae Daubentonia

Tarsius

Microcebus spp. Cheirogaleidae

Cheirogaleidae

Cheirogaleus medius

Lorisoidea

Galagidae

African

FAST

Lorisidae

Asian/African

SLOW

Fruits, insects, gums

Galagidae

African

FAST

Matriarchies

Loris

Slow lorisSlender loris

Slender loris

Lorisidae

Asian/African

SLOW

Insectivorous:

Highly tolerant of toxin

(e.g. ants)

Head first !

Geckos and lizardsMost faunivorous primates

Slow loris is more frugivorous than other lorises

DaubentoniaFruit / insect diet

“Woodpecker” of Madagascar

Slow (unafraid?)

Primary rainforest, deciduous, secondary growth, cultivation, dry forest

Solitary, FF HR = 36 ha, MM HR = 170 ha

Tarsius is an anthropoid, not a lemuriformS-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

Tarsier

“Vertical clinging and leaping”

T. bancanus: Nightly Path Length = MM 2,082 m FF 1,448 mSolitary but..

T. spectrum is monogamous (socioecological models)Prefers Ficus trees for sleepingGestation around 6 months

Birth seasonality among wild populationsBut NO seasonality among captives. Why?

Lepilemur

“Vertical clinging and leaping”

Sportive lemurs Lepilemur

Madagascar, originally 1 species, now 7 species(chromosome study)

100% plant dietFast, long day-range, humid to dry forest (adaptable!)3 species = Solitary1 species = Dispersed pair (sleep together)2 species = Mix of solitary and dispersed pair (but sleep together)1 species = Unknown

Lepilemur

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

2. Cohesive pairs

(gregarious)Aotus

1.Dispersed pairs

(stable monogamy)Phaner furcifer

3. Dispersed Multi-male social systems

Microcebus Mouse lemur

1. Dispersed pairs

Schülke & Kappeler (2003) Anim Behav

Phaner furcifer

Cf Euoticus

Stable monogamy

E.g. fork-marked lemur, Phaner furcifer8 pairs, focal follows, studied for 3 years (excellent!)

330 gram (F = M)

Gum diet

>50% one species, 15-39 trees/range

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

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

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

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)

Interactions between pairs: SUMMARY

Frequent: 6 per night!

Affiliation Aggression

F-F Regular (all 8 FF) Rare (no fights)

M-M Never Common (+ fights)

F-M Never Intermittent (F>M)

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

2. Cohesive pairs

(gregarious)Aotus

1.Dispersed pairs

(stable monogamy)Phaner furcifer

2. Cohesive (gregarious) pairs

Owl monkey, Aotus (+ woolly lemur, Avahi)

Fruit diet; cathemeral

Aotus

Avahi

Indriidae, cf. Indri, Propithecus

Owl monkey Aotus spp.

The only nocturnal (cathemeral) monkey

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

2. Cohesive pairs

(gregarious)Aotus

1.Dispersed pairs

(stable monogamy)Phaner furcifer

3. Dispersed Multi-male social systems

Microcebus Mouse lemur

Microcebus Mouse lemur

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

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

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

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

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

Special features of lemurs

Female dominanceTargeted female-female aggressionLack of sexual dimorphismHigh infant mortalityCathemeralityStrict 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)

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?...)

Synchronized weaning, asynchronized birth

Wright, 1999

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

Evolutionary disequilibrium hypothesis (EVDH) (van Schaik & Kappeler 1996)

Loss of diurnal lemurs rapid evolution of cathemerality, pair-living?

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).

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).

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

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

3. “Dispersed Pair” (Jolly 1998).

Pairing = ancestral pattern for diurnal lemurs?

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)

Theories of primate social origins.

P MM/PPro ProProProMM/P

MM/P

MM/P P

Pro

Pro

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

Müller & Thallman (2000) Biol Rev

Zhangeotherium quisquecuspideus

140-120 mya 5 inches long

Early placental mammal

Eosimias

40 mya

Early haplorhine?