Avoiding predation Hunting and sex

PredationRed

colobusStanford (2002)

Procolobus badius

Red colobus

Zanzibari red backed colobus monkey

Gambia red colobus monkey

Shoot-specialist

Large groups

High WSC (Snaith and Chapman 2005)

Multi-male (except Tana River)

Female emigration

Males jointly defend group

F-F alliances in W AfricaMale sexual ‘swellings’Key prey of humans/chimps

Predation rates on primates

Expect:Low rates (long life-span)

Explain by:

Arboreality

Few predators

Quick escape

GroupingLarge groupsMany males

Palatability?

LESS predation in:

Larger groups (r = -.49, P < .01)

Bigger species (r = -.40, P < .02)

Human-contact groups (r = -.95, P < .05)

% killed / yr

Ln (Group size)

15

0

% killed / yr

15

0

Body weight (kg)150

% killed / yr

100

0

Distance to human settlement (km)

20 1

Isbell (1994) Evol Anthropol

INFLUENCES ON PREDATION

ECOLOGICAL

EAGLE PREDATION AND

POLYSPECIFIC ASSOCIATION

EAGLES <-> SAME (monospecific) group size; POLYSPECIFICS

AMERICA AFRICA ASIA

Folivore Alouatta Colobus Presbytis

Predators

Eagle Harpy Crowned -

Mammal - Chimpanzee -

Group size 1-10 1-13 (+26) 1-8 (+14)

MM/F High High Low

PSAs Common Common Absent

# ADULT MALES

# ADULT FEMALES

4

1

1 10

COLOBUS

ALOUATTA

PRESBYTIS (arboreal)

Van Schaik & Horstermann (1994) BES

(1) MORE MALES IN SPECIES PREYED ON BY EAGLES

INFLUENCES ON PREDATION

SOCIAL

(2) LESS predation if More Male Defenders

(against chimpanzees)

Isbell et al 1993

Anim Behav

(3) LESS predation when settled in group

Cost of dispersal:

recent immigrants suffer higher mortality

Maybe because new

immigrants tend to live at the

edge of the group

(like subordinates often do)

VIGILANCE: TWO benefits?

1. Do larger groups detect predators better than smaller groups?

Prediction: Larger groups detect predators better

Detection

Group size

Vigilance rate

Blue monkey. Photo by A. Houle

VIGILANCE: 2 benefits?

Prediction: Larger groups reduce predator’s success

Survival

Group size

% successful kills

1. Do larger groups detect predators better than smaller groups?

RESULTS:

Group size can affect the detection distance

(distance at which monkeys saw or heard humans)

van Schaik et al 1983

Macaca fascicularis

Presbytis thomasi

P< 0.001

P< 0.05

P ns

P ns

M. nemestrina

Hylobates

VIGILANCE

2. Do large groups reduce the cost of vigilance?

Larger group -> less scanning (4 groups C. capucinus)

VIGILANCE: larger groups beneficialRose and Fedigan 1995 (Anim Behav)

% time spentVigilant

Time Alone

MM > FF

Who is most vigilant? (C. capucinus)

Rose and Fedigan 1995 (Anim Behav)

VIGILANCE (vervet monkeys)

Is male vigilance anti-predator?

Males spent a lot of time vigilant…

Males

October June ......... Mating season

Females

% time spentVigilant

Males are MORE vigilant

… but don’t alarm-call much!

Male vigilance directed at other males ?

“Vigilance” increases during mating season

Alpha male seen from top of canopy

Male vigilance may be selfish.

Males

% time Vigilant

Females

#Alarm Calls

Males are LESS efficient

Predation rates on red colobusGombe Kanyawara Ngogo Mahale Tai

% killed per year 5-15 < 1? > 10? 5? 10?

% adults 20-25 30 45

Big Brown (Nov 2004). Photo by A. Houle

LARGE GROUPS can ATTRACT PREDATORS (Gombe)

Population density (per sq km)

Group size

0 100 200 300

50

40

30

20

10

0

J

T

AM

TK

G+ CHIMPSGombeTaiMahaleKanyawara

- CHIMPS Jozani Abuko Tana

NO EVIDENCE THAT CHIMP-HUNTING BIG COLOBUS GROUPS

Budongo: no red colobus, and chimps do not hunt that much on other species

Effects of CHIMPANZEE HUNTING INTENSITY on Colobus demographyGombe (Stanford 1999)

50

40

30

20

10

0

G

G

G

G

G

Center S edgeSNN edge

Group sizeG

Chimpanzee community territory

J

J

J

J

J

% immatures

J

HUNTING and SEXMORE HUNTING PER ENCOUNTER with increasing n males

Chimpanzees

HUNTING and SEXMore success per hunt with increasing number of males (Gombe data)

Chimpanzees

% NFF [ = % feeding time on Non-Fig Fruits]

Kanyawara 1990-2000. Food seasons > 150 obsvn hrs.

r2 = 0.28n = 34

P < 0.005

Nu

mb

er

of

Ad

ult

+ A

do

les

cen

t M

ale

s What effect on hunting rate and success?

Kanyawara 1996-2000.

61 hunts, 9278 hours

r2 = 0.90n = 11

P < 0.0001

NUMBER OF HUNTS

PER 1000 HOURS

Number of Adult + Adolescent Males

‘## of Males’ > 150 obsvn hrs.

Gombe

Kanyawara

Number of males in party (adult + adolescent)0 2 4 6 8 10 12

80

60

40

20

0

100

% of hunts with at least one kill

For each site:r2 = 0.70, n = 13, p < 0.001

Number of Adult + Adolescent Males

> 40% NFF (non fig fruit)

< 40% NFF

Effect of fruit availabilityon hunting rates

NUMBER OF HUNTS

PER 1000 HOURS

r2 = .80, P < .001

r2 = .70, P < .01

WilcoxonP < 0.05

HUNTS

/ 1000 h

Number of Adult + Adolescent Males

Kanyawara 1996-2000. ‘## of Males’ > 150 obsvn hrs.

No swollen female

≥ 1 swollen female

WilcoxonP n.s.

Luxuryactivities

Swollen females

High-quality plant diet

More hunting

Largeparties

Nu

mb

er

of

Ad

ult

+ A

do

les

cen

t M

ale

s

% NFF [ = % feeding time on Non-Fig Fruits]

Kanyawara 1990-2000.

Increasing # males with NFF

r2 = 0.28n = 34

P < 0.005

Uvariopsis

Pseudospondias

Mimusops

Non-Fruit (THV)

Other Fruits

% NFF [ = % feeding time on Non-Fig Fruits]

Kanyawara 1990-2000.

Uvariopsis

Pseudospondias

Mimusops

Non-Fruit (THV)

Other Fruits

High residual

ANOVA (Bonferroni)

P < 0.005

Nu

mb

er

of

Ad

ult

+ A

do

les

cen

t M

ale

s

Swollen females

Largeparties

High-quality plant diet

More hunting

Food type

Swollen females

Largeparties

High-quality plant diet

More hunting

Food type

Swollen females

Largeparties

High-quality plant diet

More hunting

Food type

Swollen females

Largeparties

High-quality plant diet

More hunting

Food type

Swollen females

Largeparties

High-quality plant diet

More hunting

Food type

Swollen females

Largeparties

High-quality plant diet

More hunting

Food type

Swollen females

Largeparties

High-quality plant diet

More hunting

Food type

Largeparties

High-quality plant diet

More hunting

SUMMARYFood type

Largeparties

High-quality plant diet

More hunting

WHY?

More hunting

Assesshunting success

Show-off to males

More Friends present

Large parties

HYPOTHESES TO BE TESTED

More hunting

High daily travel

Risk- prone

strategy

Low- protein

fruit

High-quality plant diet

HYPOTHESES TO BE TESTED

Kanyawara 1989-2001, n = 122 months, 110 kills

Ngogo 1995-2000, n = 37 months, 361 kills (Watts & Mitani 2002)

8

10

12

14

0 4 8 12 16 20 24

6

4

2

0

Number of males in party

# prey / hunt

NO INTER-SITE DIFFERENCE IN KILLS / HUNT (controlling for number of males)

0 4 8 12 16 >20

80

60

40

20

0

100

Number of males in party

% hunts successful

Gombe, Kanyawarar2 = 0.70, n = 13, p < 0.001

Gombe Kanyawara Ngogo

NO INTER-SITE DIFFERENCE IN % HUNT SUCCESS (controlling for number of males)

Gombe: Stanford 1998. Ngogo: Watts & Mitani 2002

Gombe: Stanford 1998:198

INTER-SITE DIFFERENCE IN HUNTING RATE?controlling for number of males

Gombe, n =

Kanyawara, n = 178% Red Colobus encounters Hunt

NGOGO 37%

Number of males in party

n = 92 encounters 178 12-h days,

1999-2001

Chimps hunt colobus r2 = .65, P < .01

Colobus supplant chimps r2 = .52, P < .01

N = 241 encounters, all data sources%

en

cou

nte

rs

Number of males in party

INTER-SITE DIFFERENCE IN AVOID RATE? controlling for number of males

Social cognitionChimpanzee cultures

Cognition,Culture

&Capuchins

Cebus apella

Brown capuchin

Capuchins:

• 3-4 kg

• males 25-30% larger than females

• multi-male, multi-female social groups

• high EQ (and are tool users)

• “eclectic omnivores” 40-60% fruit, 5-10% leaves, 20-55%

insects, plus a wide range of vertebrates that are hunted

opportunistically.

• known to use tools both in captivity and in the wild

• start to breed late and reproduce slowly for their body size (age

at first birth= 7, IBI=2 years) maybe related to their large brain

size

• vulnerable to predation by snakes, eagles and cats

Cebus capucinusCebus olivaceus

Cebus apella

Cebus albifronsClosely related to squirrel monkeys (Saimiri)

Cebus apella

Cebus albifrons

New species in BrazilBearded capuchin monkeys, Cebus libidinosus www.ip.usp.br/ebottoni/EthoCebus/ecspec.htm

New species in BrazilYellow-breasted capuchin, Cebus xanthosternos

www.waza.org/virtualzoo/factsheet.php?id=106-006-007-002&view=Monkeys&main=virtualzoo

F-F relationships

• Females are philopatric

• Stable, nepotistic dominance hierarchy

• F groom other F > F groom M = Female-bonded social system

• F form coalitions with each other that can be very stable over time, and appear to be effective in competing with M

• all F allonurse, but high ranking F < low ranking F

M-M relationships

• clear alpha-M but no obvious dominance relationships among subordinates

• alpha-M is spatially central to the group

(anti-predator strategy?) • alpha-M monopolizes matings in Cebus apella, but not in the gracile capuchins

• alpha-M forms coalitions with the subordinate males in the group, and prevents subordinates from forming coalition with each other• males cooperate in defense against predators and non-group males in gracile capuchins (but not Cebus apella)

• in C. capucinus, males never refused solicitations for coalitional support in the context of intergroup interactions

• male C. capucinus actively search for lost group-mates

M-F relationships

• alpha-F ranks immediately below the alpha-M in all species except C. capucinus, where all females are subordinate to all males.• alpha-M requires the coalitional support of F in their group to maintain their rank (C. capucinus)

• F are hypothesized to receive protection from infanticide from the males in their group

Intergroup interactions

• almost always aggressive

• M are primary participants, F rarely

participate (and only if don’t have an infant)

• M form coalitions during intergroup

interactions (except in C. apella)

• lethal, coalitionary intergroup aggression has been seen

• extra-group males may be infanticidal

• In C. olivaceous, large groups displace small groups at feeding

sites, and the females in large groups have higher reproductive

rates.

Cebus olivaceus

Wedge-capped capuchin

Female-bonded

Female-philopatric

All males emigrate

Female rank clear

Daughters inherit rank

Lifespan to 36 years

First birth at 6 years

Cebus olivaceus

Wedge-capped capuchin

Allomaternal nursing

a. Infants

Group-wide

Rank-independent

Clearly affiliative

b. Juveniles or adult females!

High-rankers take

Low-rankers give

Clearly agonistic

Cebus olivaceus

Size fluctuations and persistence

length of eight matrilines in Main

Group over the period 1977-99,

sorted by decreasing matrilineal

dominance rank.

Valderrama et al. (2003)

alpha beta

lowest

What are the social-cognitive consequences of variation in brain size?

Rilling & Insel, 1999

Chimpanzee Capuchin

Hunt / meat-eat Yes Yes

Tool use Yes Yes

Lethal aggression Yes Some

Visual perspective-taking1 Yes No

Tradition Yes Yes

1 Visual perspective taking is one of the cognitive capacities associated with Theory of Mind, which is the ability to understand that other individuals have their own goals and intentions.

Cognition (Strier)1) Learning / imitation (development)

2) Ecological intelligence

Spatial memory

Tool use

Traditions

3) Social intelligence

Alliances

Tactical deception

Perspective-taking (TOM)

4) Implications for ethics

The “Social Brain” hypothesis: are big-brained species socially adept?

Dunbar, 1992; 1993

Conspecifics are competitors

Group living aggravates competition

Selective advantage to individuals successful in inter and intra group competitions

Social problem solving abilities (social cognition) predicted as target of selection

Mean social cognitive ability increases

Social Intelligence Hypothesis: Runaway directional selection for social cognition in primates

Guts are small

(1) Big-brained species: good at signing

(2) Big-brained species successful: mirror test

(3) Big-brained species: many traditions

Ant-fishing Camponotus

Gombe

Tai

Bossou

Mahale-K

BudongoMahale-M

Kibale

Gombe

ALL TRADITIONS

0

5

10

15

20

25

30

35

40

0 5 10 15 20 25 30 35 40

Kibale

Tai

Bossou

Mahale-M

Mahale-K

Budongo

YEARS OF STUDY

All wild chimpanzee populations have traditions

still rising !

Social transmission?

Ant-fish: Mahale, not Gombe

Communication

Hunting

Tai

Bossou

Gombe

Mahale

BudongoKibale

Gombe

0

5

10

15

20

25

30

0 5 10 15 20 25 30 35 40

Kibale

Tai Bossou

Mahale-M

Mahale-KBudongo

Years of Study

Numberof

toolsobserved

ALL TOOLs

All populations use tools...Leaf-grooming

Budongo

TaiBossou

Gombe

Mahale-K

KibaleMahale-M

Gombe

0

2

4

6

8

10

12

0 5 10 15 20 25 30 35 40

Kibale

Tai

Bossou

Mahale-M

Mahale-K

Budongo

Years of Study

AllCustomaryor Habitual

Food-Tools

… but not all use tools for food

KIBALE

BUDONGO

GOMBE

MAHALE

MT ASSIRIK

LOPÉ

BOSSOU

TAI

Patterns of diffusion

NUT-SMASH

Present

Absent (but nuts present)

CULTURAL DIFFUSION

Cultures

Mer

cade

r et

al (

2002

) S

cien

ce

BRUSH-STICK

Present

Absent (but eat termites)

CULTURAL DIFFUSION

LEAF-CLIP: LIMITED DIFFUSION?

Present

Absent

To leaf clip, a chimpanzee gathers one to five stiff leaves and bites little bits off with its front teeth without eating the leaves. The biting produces a distinctive ripping sound, which appears to be the goal. At Mahale Mountains National Park, young male chimpanzees and adult female chimpanzees that are ready to mate make the clipping sounds to attract each other's attention. The sound might be translated as meaning, "I would like to mate."

Present

Absent

PENIS-WIPE: LIMITED DIFFUSION?

In penis cleaning, leaves are

employed as ‘napkins’ to

wipe clean the penis after sex.

Twig, Kanyawara, Feb. 2005

Present

Absent

LEAF-GROOM: LIMITED DIFFUSION?

Kanyawara, Feb. 2005

HAND-CLASP GROOM

Present

Absent

HAND-CLASP GROOMING:DIFFUSION OR RE-INVENTION?

Never. GombeBossou

Budongo

Daily. Kibale, Mahale

Tai: died out!

Population variation:

Due to opportunities for

transmission?

Van Schaik et al (2003) Science

Primate traditions

Chimpanzees >> bonobos (mysterious)

Orangutans few >> gorillas

Capuchins few

Gorilla at Mbeli Bai Nouabalé-Ndoki National Park

1. Do primates know that others can perceive things differently?

Does she see something that I do not?

Yes:

(A) monkeys/apes follow the gaze of conspecifics

Tomasello, Call, Hare 1998

Adults inhibit gaze response to a human who repeatedly looks at nothing

Tomasello, Hare, Fogleman, 2001

(B) Gaze-response adapts to context

(C) Chimpanzees move around visual barriers blocking their view of another individuals gaze

Tomasello, Hare, Agnetta, 1999

•Two subjects compete for food

• Each subject held in an outside cage in a row of three adjacent cages •center cage baited with one or two pieces of food

• food baited different ways

• competitors released into middle cage to retrieve food

(2) Can primates use knowledge of what others perceive when competing over food?

Do subordinates prefer to approach and retrieve food that dominants cannot see?

Hare et al (2000, 2003) Anim Behav

NOYES

Subordinates approached

less when dominant was

informed

Subordinates retrieved more

food when dominants

uninformed or misinformed

Food retrieval

No approaches

Chimpanzee Cultures: New findings from Kibale

Sonya Kahlenbergwith chimpanzeeTease-toy

The Meaning of Weapon Invention

Imoso - alpha male since 1997

“Ah! We must now redefine man, redefine tool, or accept chimpanzees as humans.”

Louis Leakey, 1960.

Termite-fishing

Modifying tool

CULTURAL EVOLUTION DOES NOT DEPEND

ONLY ON INVENTION

FREQUENT INVENTION, FREQUENT EXTINCTION

CLUB USE BY CHIMPANZEES

‘To the Rescue’

O.C. Vane

A mid-Victorian tale

BARBARA (10 yrs) Throw at mangabey

Beat chimpDisplay/throw

AGGRESSIVE STICK USE BY KANYAWARA CHIMPANZEES 1997-2002

1997 1999 20011998 2000 2002

+ otherstick use?

JOHNNY7/14

TWIG YOGI LBSTOUT KAKAMA (x2)7/15

IMOSO7/09

XylocopaApis

HONEY STICK USE BY KANYAWARA CHIMPANZEES

1997 1999 20011998 2000 2002

+ otherstick use?

MAKOKUROSA

STOUT

“To understand the socioecological factors

that promote social learning in an evolutionary

perspective, it is necessary to look beyond the

great apes.” Perry et al. 2003, p. 242

But do socioecological factors promote social learning?

Ha: SL is adapted to specific social ecology

Hb: SL is an incidental consequence of cognitive ability