Session 5: The Callitrichids

1.  Key Concepts:

 The Callitrichines are known for their small body sizes, their cooperative breeding, twinning, and flexible mating systems.  Additionally, they are characterized by claw-like nails, found on all digits but the hallux, and dramatic variation in color.

2. Terms & Definitions:

Cooperation

Mutually beneficial interaction among organisms living in a limited area.

Territoriality

The behavior of an animal as it relates to defining and defending resources and habitat.

Social Organization

The structure of social relations within a group, usually the relations between its subgroups.

3.  Taxonomy of Callitrichids:

 The Callitrichids are among the most controversial taxa of primates, largely because the combination of morphological, genetic, and ecologic characters place Callitrichids in an historically ambiguous taxonomic location.  Recent, well-supported revisions (Rylands et al. 2000), place it as one monophyletic group with six genera and 60 species and sub-species.  Callitrichids have a long evolutionary history distinct from other neotropical primates which may explain why they are so derived.

Callitrichid Genera:

• Callithrix or Atlantic marmosets
  
• Mico or Amazonian marmosets
• Cebuella or pygmy marmosets
• Callibella or dwarf marmosets
  
• Saguinus or tamarins
  
• Leontopithecus or lion tamarins
  
• Callimico or Goeldi's monkeys

 Callibella, or the dwarf marmoset, is a very recently proposed genus to this group.

Basic characteristics:

The Callitrichids are extremely small, neotropical primates, weighing between 100 and 700g.  Their body size is characteristic of ancient primates and is extremely derived.  In large part because of their small size, the Callitrichids have the weakest thermoregulatory system and sleep in a near torpor-like state.  Callitrichids are entirely arboreal.  Twin births are the normative pattern, and each twin can have distinct paternity.  Callimicos are the exception, due to their common singleton birth patterns.  Morphologically, Callitrichids have distinct traits, including:

• 2-1-3-2 dentition, except Callimico which has 2-1-3-3 dentition
  

• Claw-like nails
• No lactactional amenorrhea
  

• Marmosets: elongate, narrow incisors
  
• Tamarins: short, broader incisors.

4.  Habitat & Behavior:

The range of the Callitrichids includes much of northern South America.  As might be expected from this wide distribution, these primates inhabit a variety of neotropical habitat types.  The key factor determining differences between the marmosets and the tamarins appears to be the marmosets' morphological specializations for consuming exudates.

General habitat choices:

The Callitrichids generally prefer non-primary forest.  Marmosets thrive in a wide spectrum of forest types, including extreme anthropogenically-altered forests, if allowed to begin growth again.  Cebuella prefers riparian and marginal habitats (both gum specialists).  Terminal and mid-canopy branches are favored.

General Behavioral Patterns:

•   Rapid, leaping movement.

• Multi-female/multi-male groupings generally with some one female/multi-male; most only have one breeding female.
• Practice infant care, including high levels of “cooperative,” or non-maternal, care.
• Mixed species groups common.

Ranging and mixed species groups:

The mean daily range of a Callitrichid is high, relative to its body size and thermoregulatory abilities.  Temperature and climatic variables can have significant impacts on day ranging.  There is often no set "range" or territory for Callitrichid groups, but when these groups overlap, aggression can occur.  The core area of a range will be defended, but never the entire range.  Also, both sexes disperse, so meta-groups can form of hypothetically related individuals.

Diet:

Callitrichids will try to eat anything—the diet is extremely variable.  They have a small, simple stomach which allows for non-specificity.  Individuals will try to eat vertebrates, such as lizards and snakes, but the capture rate is low.  young individuals will take food from adult members of a group. Sub-adults and juveniles will even take food from the mouth of an adult.  The high levels of infant care and alloparenting facilitate this in Callitrichids more so than in most other primates.  Food sharing is extremely common, and adults are extremely tolerant of infants and young. 

Marmosets will gouge out trees to access the exudates, which they preferentially consume.  Tamarins will follow marmosets and opportunistically utilize marmoset holes.

  Broadly, the diet rules are as follows:

• Insects, Vertebrates, Fruit, Nectar, Fungus
• Food sharing with high value foods
• Exudates

Activity patterns:

Generally, most Callitrichids utilize holes in trees for nests.  Groups sleep communally, with infants located near the core.  This benefits thermoregulation but can come at the cost of increased predation risk.  Most Callitrichids utilize about 7 hours of day in order to maximize exertion output.  Activity patterns include:

• Leaving sleeping site well after sunup
• Returning to sleeping site before sundown
• Generally limited energy expenditures

Predation:

Callitrichids have been documented as succumbing to predation more than any other primate.  Predation pressure is very important, as supported by the high number of predator-avoidance adaptations.  Rapid cryptic behavior is important to Callitrichids.  Alarm calls sound like birds, and mobbing behavior has been observed.  Callitrichids have been preyed on by:

• Birds
• Snakes
  
• Cats
• Other mammals
  

5.  Social organization & Reproduction:

The variation in habitat and diet of Callitrichids are not reflected in their social organization.  Generalities of the social organization of Callitrichids include:

• Small groups size (~2-20), with means of 6-12 individuals.
• Both sexes disperse.
• One reproductive pair or one reproductive female per group.
• Twin births, up to twice per year, with one twin commonly dying.
  
• High rates of scent marking and intragroup vocalization.
• Close physical contact frequent.
• Low rates of aggression.

Reproductive suppression of non-dominant females:

Oldest females tend to reproduce, while younger females, though sexually mature, do not reproduce.  The rarity of sexual activity in non-breeding adults is due to leutenizing hormone suppression.  The mechanisms of this suppression is unclear.  The generalities of suppression include:

• Behavioral-physiological suppression of non-dominant females.
• Not general “stressing” response.
• Lack of sexual activity on non-breeding adults.
• Suppression may vary based on relatedness and/or familiarity.

Mating and Caretaking:

Cooperative breeding can often be explained by kin selection; however, genetic relatedness within individuals participating in cooperative breeding here is extremely low.  Often, due to the high levels of female and male dispersal, alloparenting individuals are not related to breeding adults.  So why do individuals participate in caretaking?  There are several hypothesized reasons, including:

1. Individuals are waiting "in line" for resource availability.
2. Males gain experience in parental care.
3. Females prefer mating with experienced males.

It is highly likely that all three work together.  Infant carrying males have extremely high prolactin levels which is hypothesized to be important in primates for bonding.  The hyper-physical contact style of Callitrichids primes non-reproducing males and females to be involved in parental care of young.  Extra-pair copulations (EPC's) are common, especially between neighboring groups.  Cooperative breeding is actually evolutionary competition for mates because the best cooperators are preferentially allowed to breed.  Humans are the only other primate group to practice extensive cooperative breeding.  Generally, the normative behavioral patterns of mating and caretaking include:

• Multiple individual caretaking of infants.
  
• "Family" groups = Cooperation via kin selection.
• Non -”Family” groups and alloparenting individuals = Cooperation and reciprocal altruism via gain in experience as it relates to mate choice.
• High prolactin levels in “helping” males.
• Practice and selfish learning-competition in cooperative breeders.

Infanticide:

Often, specifically with Callithrix and Leontopithecus, the dominant female kills subordinate female's offspring.  Ultimately, the subordinate females are "punished" for reproducing via infanticide.  The group cannot afford to raise an extra two infants due to competition for resources and cooperative breeders.  If not killed, infants of subordinate females usually die via neglect.  Behavioral patterns are more complex than simple kin selection models would predict.

6.  The Tamarins of the Potawatomi Zoo in South Bend, IN

Meet the Tamarins of the Potawatomi Zoo:
Orlando: Orlando is the dad of the group. He was born in October, 1992. You can recognize him by his shorter tail and mohawk. He spends lots of time resting alone on top of the nesting box and large branch to the left of it.	Mary Anne: Mary Anne is the mom of this tamarin family. She was born in May, 1994. Her skinny tail and spiky white hair distinguish her from the others. Sometimes she likes to be acrobatic and hang upside down in the back left corner by the nesting box. She likes to rest with Orlando and spend time with Bonnie and the youngest twins.
Frank: Frank is the older brother of this tamarin family. He was born in August, 2000. Frank can often be picked out by his less than fluffy fur. He likes to sit by himself or groom his sister, Bonnie. One of his favorite spots to sit is near the glass by their water dish.	Bonnie: Bonnie is the older sister in this troop. Her birthday is in July of 1999. Bonnie has very fluffy white fur on her chest. She likes to play follow-the-leader with the other monkeys, especially her mom, Mary Anne. She also likes to cuddle and groom with the rest of her family.
The Younger Siblings: The two sets of twins were born in 2003 and 2004. The white fluff on their heads is a little smaller than their older brother and sister, and their mom and dad. They like to play and run around, getting into all kinds of trouble

The Details of the Speceis, Saguinus Oedipus:

• Native to northern Colombia and southern Panama.
• Live in multi-female/multi-male groups.
  
• Group size ranges from ~ 6 - 8 individuals.
• Weigh approximately 400-450g.
• Prefer secondary and mixed forest habitats; 0-1500m. in altitude.
• Sexual maturity is reached at ~18 months.
• Female carries infants for first 1-2 weeks then male and other group members carry nearly 100%.
• Adults participate in high levels of food sharing.
• High mortality in naïve mothers.
• More than 30,000 exported in 1960-70s for biomedical research.

7.  Additional Information:

 Required Reading:

Primates in Perspective.  2007.  eds.  C. J. Campbell, A. Fuentes, K.C. MacKinnon, M. Panger, and S. K. Bearder.  Oxford University Press.

Chapter 6:  The Callitrichines: The Role of Competition in Cooperatively Breeding Species - Digby, Ferrari, & Saltzman.