Ecological Influences on Primate Sociality Why are primates and other animals social? SOLITARY
*Males defend home ranges that encompass home ranges of several females. -solitary species -pottos, galagoes, orangutans
MONOGAMOUS PAIRS *When females are dispersed (eg. solitary), males may associate permanently with one of them. -gibbons, some lemurs POLYANDRY *Several males associate with one reproductive female. -Callitrichids
POLYGYNY: ONE MALE *If females are clumped in groups, one male may be able to monopolize access to a group. -gorillas, Hanuman langurs, patas monkeys (kind of)
POLYGYNY: MULTIMALE *Females clumped in groups, and multiple males associate with them. -baboons, vervet monkeys, macaques, chimpanzees Gorillas: 2 Species; 4 Subspecies Western Gorillas Eastern Gorillas (Gorilla gorilla) (Gorilla beringei)
Cross River Gorillas
Mountain Gorillas
Western Lowland Grauer’s Gorillas Gorillas Mountain Gorillas are the Most Studied
MPI research ongoing in Bwindi since 1998.
Altitude: 1160-2600m
Karisoke- Established by Dian Fossey in 1967.
Altitude: 2200-4500m
Lots of variability between populations. What is the relationship between primate social behavior & ecological parameters?
Characteristics of Primate Groups:
-Size -Composition -Sex ratio -Degree of cohesion -Patterns of dominance (hierarchical or egalitarian) -Patterns of aggression -Patterns of affiliation -Coalition formation -Dispersal patterns Chimpanzee Gorilla Savanna Ring-tailed Baboon Lemur Group Multi-male, One-male, Multi-male, Multi-male, Composition Multi-female multimale, Multi-female Multi-female Multifemale Group Size ~30-150 ~2-60 ~15-100 ~5-30
Grouping Fission- Cohesive Cohesive Cohesive Pattern Fusion Natal Group Female- Both Sexes Male-Biased Male-Biased Dispersal Biased Home Range Territorial Overlapping Territorial Territorial Utilization Ranges Female Weakly Weakly Hierarchical Hierarchical Relationships hierarchical hierarchical Can a systematic relationship between variation in ecological parameters & primate social behavior be explained by one logical framework? Behavioral Ecology
Links scientific approach to studying : -behavior -ecology -evolution
Aim: to understand why different species behave in different ways and why there are individual differences in behavior.
Socioecology
-how natural selection shapes social organisation in response to ecological pressures.
-evolution of sociality -evolution of individual behavioral strategies -resource gathering and distribution strategies -reproductive strategies The Strategy Metaphor
Individuals acting to maximize their reproductive success. (no implication of consciousness)
Ultimate Causation
Adaptive significance of traits on the evolutionary history of a species.
Comparative Approach
Make predictions of how a change in one variable will influence other variables
‘Natural experiments’
Comparisons of closely related species or populations of same species under differing environmental conditions Individual
Group
Population
Species Food is everything!
Food Influences:
Survival
Growth
Reproduction An Animal’s Environment Influences it in many ways:
Ranging Patterns: Diet/Activity Patterns:
-Size of range -What is eaten, -How much, -Territoriality or overlapping ranges -When -Obtaining Food -Patterns of habitat utilization -Time spent in different activities Social Behavior:
Group Attributes -Relationships within a group
-Group size -Relationships between groups
-Group composition -Competition/aggression
-Dispersal Patterns -Affiliation
-Reproductive Skew -Cooperation Influences on Sociality
1. Food Availability
2. Predation Pressure
3. Reproductive Strategies
(Crook & Gartlan, 1966; Eisenberg et al., 1972; Emlen & Oring, 1977; Sterck et al., 1997; Kappeler & van Schaik, 2002; Clutton-Brock & Janson, 2012) Costs of Sociality:
-increased competition for resources (food, mates)
-increased likelihood of disease and parasite transmission
-increased conspicuousness (predation)
Benefits of Sociality:
-increased probability of obtaining resources
-lower risk of predation Reproductive Success (number of offspring produced) limited by:
Females: access to food resources
Males: access to females Socioecological Model
(Koenig et al., 2013) Not all Food is Equal, nor Equally Attainable
Food Quality:
*Macronutrients: Protein, Fat, Carbohydrates *Vitamins & Minerals *Secondary Compounds (tannins & phenols)
Sources of Nutrients: Fruit – carbohydrates (simple sugars) Leaves & Herbs – protein Insects – fat, protein Meat - protein Animals tend to have physiological & physical adaptations for the type of diet they have:
-Body Size
-Teeth
-Digestive Tracts
Primate Species tend to be dietary specialists:
-Frugivores
-Folivores
-Frugivores/Folivores
(but these are very broad classifications) Food Availability Differs in Time and Space
Time: Seasonality of Fruit, Young Leaves
Space: Variability in Distribution & size of patch Resource Distribution
May vary in both time and space. Types of Competition
Contest/Interference Competition:
-resources are not shared equally -individuals benefit by excluding others from resources -agonistic interactions
Scramble/Exploitation Competition:
-individuals cannot effectively exclude others from resource -individuals ‘scramble’ for resources in autonomous ways -individuals lose access to resources because others have already found them and used them.
What is Dominance?
Dominance:
* an attribute of the pattern of repeated, agonistic interactions between two individuals,
*characterized by a consistent outcome in favor of the same dyad member,
*and a default yielding response of the opponent rather than escalation (Schjelderup-Ebbe, 1922)
-Ability to exclude others from resources & elicit submissive behavior.
Ranking of individuals according to dominance status
Dominant vs. subordinate individual = dominance relationship
If you have more than 2 individuals you may get a Dominance Hierarchy
Alpha = Rank 1 Beta = Rank 2 ….. Rank 3 Rank 4 Rank 5 etc…
What behaviors are indicative of dominance?
Supplantation
Avoidance
Submissive Behavior
Aggression (?)
Winner of fights? Group of 4: A, B, C, D A supplant B = 2
B supplant A = 0 Actor Action Recipient A Supplant B A supplant C = 1 A Supplant C C supplant A = 0 B Supplant C C Supplant D A supplant D = 1 A Supplant D D supplant A = 0 A Supplant B B Supplant D B supplant C = 1 C Supplant D C supplant B = 0 B Supplant D B supplant D = 2
Dyad = 2 individuals D supplant B = 0 A – B, A – C, A – D, B – C, B - D, C - D C supplant D = 2
D supplant C = 0
Create a matrix of the individuals
Recipient
A B C D
A
B Actor C
D
Recipient
A B C D A B C D A 20 18 31 A 5 2 1 B 0 17 20 B 0 3 1 Actor C 0 0 12 C 0 0 2 D 0 0 0 D 0 0 0
A B C D A 5 2 1 B 0 3 1 C 1 0 2 D 0 2 0
Elo Rating for Dominance Ranking
1400 BY JN 1300 KR MG 1200 ST TN TW 1100
1000 1:10 EloRating
900
800
700
2010 2011 2012
Date Types of Competition
Contest/Interference Competition:
-resources are not shared equally -individuals benefit by excluding others from resources -agonistic interactions
Scramble/Exploitation Competition:
-individuals cannot effectively exclude others from resource -individuals ‘scramble’ for resources in autonomous ways -individuals lose access to resources because others have already found them and used them.
Within Group Contest Competition
(Koenig et al., 2013) Pure Within-Group Contest Competition
p p p p p WGC g g g g
n n n
u u
r Reproductive Success Reproductive
1 2 3 4 5
Number of adult females in a group
Average reproductive success declines with increasing group size (solid line) Within-Group Contest Competition AND Within-Group Scramble Competition
p
p
g WGS
p
g
n p
g
n p Reproductive Success Reproductive WGC u g
n
u
r
1 2 3 4 5
Number of adult females in a group Individual & Average reproductive success declines with increasing group size. According to Socioecological Model:
*When resource distribution leads to high contest competition: -leads to decided agonistic & dominance relationships -benefits of coalitions, particularly with kin -beneficial to remain with kin – female philopatry
*Competition between groups may cause tolerance within-groups.
*If resources are distributed in a way that primarily results in little contest competition: -few agonistic interactions occur -no or weak dominance relationships -little benefit of kin – may result in female dispersal
* but scramble competition should always occur in social groups.
Dimensions of Female Social Relationships to Achieve Reproductive Goals (Sterck et al., 1997)
Egalitarian: females have no detectable or poorly defined dyadic dominance relations
Despotic: females have clearly established and often formalized dominance relations
Nepotistic: female relatives rank close together as a result of coalitionary support from relatives
Individualistic: ranks of female relatives are independent of each other
Tolerance: severity of aggression and likelihood of reconciliation
Dispersal or Philopatry Resident-Nepotistic: Resident-Egalitarian:
Vervet monkeys Patas monkeys Macaques (most) Black & white colobus monkeys Baboons (most) Other Cercopithecine spp?
Resident-Nepotistic-Tolerant: Dispersal-Egalitarian:
Sulawesi macaques Ring-tailed Lemurs Howler monkeys Hamadryas baboons Chimpanzees Gorillas
Tests of Socioecological Model:
Many of the assumptions and predictions of the model are difficult or impossible to test. (so is the model useful?)
Does the type of competitive interactions exhibited result in the expected variation in food intake and/or reproductive success?
Does a change in ecological conditions (eg. distribution of resources) result in expected variation in social relationships and/or reproductive success?
Tests of model:
What evidence is there of the effects of scramble & contest competition?
Scramble: -Group size, sociality, and reproductive success
Contest: -Dominance asymmetries -Predicted types of social interactions -Impact on Energy Balance and Female Reproductive Success
Scramble Competition:
Predict that as group size increases, reproductive success should decline.
Different measures/proxies for costs of additional group members.
Sociality & Group Size:
1. Sociality does appear to reduce risk of predation.
2. Intensity of scramble & contest competition for resources increases with group size.
(Strier, 2007) Food Availability Influences: Ranging Patterns
Daily Travel Distance & Home Range size influenced by diet:
-both variables should also increase as group size increases.
-typically larger for frugivores than folivores
-groups should spend more time in areas of higher food availability (optimal foraging)
(Janson & Goldsmith, 1995) (Koenig et al., 2013) Food Availability Influences: Ranging Patterns
Bwindi Mountain Gorillas
Monthly Home Range Size Influenced By:
-Food availability (energy of herbaceous foods) YES -Frugivory NO -Density of Neighboring Groups YES -Group Size YES
Daily Travel Distance Influenced By:
-Food availability (energy of herbaceous foods) NO -Frugivory YES -Density of Neighboring Groups NO -Group Size NO
(Seiler et al., in review)
Analysis of 40 years of data for Virunga mountain gorillas: (evenly distributed food resources)
Despite the groups becoming 2-5 times larger than the population average, there was no impact of group size on female reproductive success.
Have ecological conditions changed over time?
(Robbins et al., 2007) Interbirth Interval in Baboons increases as Group Size increases (Resident-Nepotistic)
(Packer et al., 2000) Factors other than feeding competition that may limit group size & stability:
-predation pressure -exploitation by parasites/disease -reproductive competition between females -rate/risk of infanticide by males
No single explanation is likely to account for interspecific variation in group size.
(Schuekle & Ostner, 2012)
CONTEST COMPETITION
Dominance Asymmetries
Prediction: if food is distributed in patches of high value, direct competition between group members should be common & females should develop linear dominance relationships.
-Intraspecific variation in food distribution often does affect the frequency of competitive interactions.
-studies of same group feeding on different resources
-comparisons of different populations of same species
Dominance Asymmetries
Prediction: Female hierarchies should be more predictable & female rank should have a stronger effect on female fitness in species exhibiting female philopatry than in those where females disperse. (benefits of grouping with kin)
-Some evidence, but obvious exceptions.
Eg. Species where females are philopatric, but don’t form linear hierarchies. (eg. lions)
Species where females are not philopatric, so don’t reside with kin, but linear hierarchies are observed. (mountain gorillas, chimpanzees, Phayre’s leaf monkeys)
Matrilineal ‘inherited’ rank – female spotted hyenas
Holekamp et al., 2011 Holekamp et al., 2011 Holekamp et al., 2011 Rank and Reproductive success of Female Baboons (Resident-Nepotistic)
Altmann & Alberts, 2003 Comparison of two baboon populations
(Barton et al., 1996) MPI gorilla research Mountain ongoing in Bwindi since 1998. Gorillas -Feed on highly abundant herbaceous vegetation, but also on seasonally available fruit. -Weak dominance Relationships. Karisoke- Established by Dian Fossey in 1967. Highest altitude-living gorillas.
-Feed on highly abundant herbaceous vegetation -Weak Dominance Relationships. Feeding Competition in Bwindi Mountain Gorillas
1.6
1.4
1.2
1.0
0.8
0.6 aggression/gorilla/hour
0.4
0.2
275 299 43 73 69 9 203 230 34 0.0 all adults silverbacks adult females
nonfeeding herbaceous fruit
-higher rates of aggression when feeding on fruit than herbs
Robbins (2008) Dominance – Karisoke Mountain Gorillas (Dispersal-Egalitarian)
Predict little or no relationship between dominance rank & FRS, because of evenly distributed, abundant food resources.
Results:
Female dominance relationships are stronger and more stable over time than previously reported.
Higher ranking females have:
- shorter interbirth intervals - longer adult lifespans - higher lifetime reproductive success
Robbins et al (2005, 2007, 2011) Feeding Competition: Does dominance rank correlate with access to food resources & energy balance?
Karisoke Bwindi Cyril Grueter Edward Wright
Methods: -Behavioral observations for dominance, aggression, and food intake
-Nutritional Analysis
-Estimates of energy intake & expenditure
In Bwindi:
Dominance rank correlates: -Positively with Energy Balance -Positively with Energy Intake
-Negatively with Energy Expenditure balance Energy (Wright et al., 2014) Low High -Aggression was predominantly ‘down’ Dominance rank the hierarchy, but rank was not correlated with aggression rates.
-Lower ranking females had fewer neighbors– probably avoiding higher ranking individuals. (Wright et al., 2014; Wright & Robbins,2014)
At Karisoke:
Dominance rank did NOT correlate with energy intake or expenditure.
-Higher ranking females were more aggressive, but didn’t appear to influence energy intake or expenditure. (Grueter et al., 2016) *Variables other than socioecological factors may influence female reproductive success.
*Morphological characteristics
*Does Body Size influence Reproductive Success?
Dominance Asymmetries & Female-Female Competition
-not yet sufficient data/studies on correlations between: a) Social structure & feeding competition b) Female dominance hierarchies & feeding competition to demonstrate strong associations among these variables.
In other words, need more studies that support model.
Challenges of testing and modifying the Socioecological Model:
-defining and measuring ‘clumpiness’ of resources
-variability in measures of behavior (eg. dominance)
-focus on relatively few species
-few studies have good measures of relative food intake and/or reproductive success
-too focused on females and forgetting about males???
-too primate-centric? Food Availability Differs in Time and Space
Time: Seasonality of Fruit, Young Leaves
Space: Variability in Distribution & size of patch Variability in Food quality, availability & contestability in Bwindi:
(Wright & Robbins, 2014) Difficulties for Testing Predictions of Socioecological Model
Eg. Estimating fruit availability: density of each tree species Size of trees Amount of ripe fruit
3000 2500 2000 Buhoma 1500 Ruhija 1000 500
Fruit Fruit Availability Index 0
Jan Apr Sept Oct Nov Dec Feb Mar May June July Aug Month Ganas et al., 2009
-2 areas only 15 km apart in Bwindi Impenetrable National Park, Uganda -measured for only 1 year (inter-annual variation) Estimating fruit availability:
-may vary inter-annually. -may depend on what a particular primate species eats.
Fruit availability for chimpanzees & gorillas in Loango, Gabon
(don’t eat all the same fruits)
(x1000)
Head et al., 2011 Challenges of testing and modifying the Socioecological Model:
-defining and measuring ‘clumpiness’ of resources
-variability in measures of behavior (eg. dominance)
-focus on relatively few species
-few studies have good measures of relative food intake and/or reproductive success
-too focused on females and forgetting about males???
-too primate-centric? Challenges of Studying Primates:
-Time/investment to habituate wild animals
-Difficulty of Field Work & Observation Conditions
-Small sample sizes
-Long Life Span
-Endangered Status Social Relationships Carbohydrates
Reproductive Success
Scramble Competition Baboons Herbs Patchy Resources
Dominance Home Range Activity Patterns
Group Structure Diet Food Availability Environment -Variable in Time and Space -Can be assessed on different scales
Diet/ Habitat Utilization Group Attributes Social Behavior Activity Patterns
Fitness
Tinbergen’s 4 levels of explanation:
-Phylogenetic: evolutionary history (how a trait or behavior is distributed across related species)
-Ontogenetic: developmental trajectory for a particular trait (when)
-Proximate: underlying neural, chemical, physiological, or immediate causes for a particular behavior or trait (how)
-Ultimate: evolutionary function of a behavior or trait (why)