Laboratory Primate Newsletter

References

Disler, P. B., Lynch, S. R., Charlton, R. W., Torrance, J. D., Bothwell, T. H., Walker, R. B., & Mayet, F. (1975). The effect of tea on iron absorption. Gut, 16, 193-200.

Gonzales, J., Benirschke, K., Saltman, P., Roberts, J., & Robinson, P. T. (1984). Hemosiderosis in lemurs. Zoo Biology, 3, 255-265.

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Corresponding author: S. G. Fang, College of Life Sciences and Key Laboratory of Conservation Genetics and Reproductive Biology for Endangered Wild Animals of Ministry of Education, Zhejiang University, No.268 Kai Xuan Road, Hangzhou 310029, Zhejiang, People's Republic of China [e-mail: sgfang@mail.hz.zj.cn].

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Ontogeny of Vocal Communication in Nonhuman Primates: A Review

Communication in nonhuman primates can take many forms: olfactory; visual/gestural; and/or vocal. This review will focus on vocal communication and whether its developmental influences are genetic or learned, among other factors. Though current evidence is incomplete, most scientists generally agree that the ontogenies of vocalizations in nonhuman primates are probably a result of several factors: genetic fixity; learned variability by species, social organization, environment, and type of call; and physiological development. However, there is no broad consensus about the relative role of each element.

Early studies on vocal development in nonhuman primates commonly found it to be fixed at birth with little effect of experience (Nottebohm, 1972). These studies have questioned whether infant primates require acoustic feedback in order to produce species-specific repertoires. Squirrel monkeys (Saimiri sciureus) have provided substantial evidence supporting genetically inherited vocalizations, because they are easy to maintain in captivity and most of their vocalization falls within the range of human hearing (Biben & Bernhards, 1995). In a landmark study by Winter et al. (1973), captive female squirrel monkeys were surgically muted during pregnancy so as not to pass on normal auditory cues to their newborn infants. Within the first day after birth, the infants from both the altered and the normal groups displayed similarly structured isolation peeps, cackling, yapping, grumbling, shrieks, and alarm peep calls, and within three days after birth "location" trills began. Compared to the infants in the control group, there were no significant differences in duration or structure in the calls of infants with muted mothers, or between the calls of those infants and the call repertoires of the adults under normal conditions. This suggests that even without normal auditory input, squirrel monkey infants have an innate ability to demonstrate certain functionally and contextually correct species-specific vocal repertoires.

Another study with squirrel monkeys investigated infant isolation peeps (brief, frequency-modulated calls given by offspring when separated from mothers) in Roman Arch and Gothic Arch hybrids (named for their facial hair patterns). Lieblich et al. (1980) found that the basic calls that differentiated the two hybrids were consistent and apparent from birth, and Newman and Symmes (1982) found that the calls of the infants were structurally similar to those of their mothers.

In certain species of nocturnal strepsirhines (Galagidae, Lorisidae, and Cheirogaleidae spp.), infants from birth give purr calls, scream calls, and grunt calls in situations of comfort, discomfort, hunger, injury, or anger (Kuhn, 1989; Stanger, 1988, 1993; cited in Zimmerman, 1995 and 1991). These types of calls are generally seen as involuntary and fixed at birth, reflecting emotional states and regulating the social interaction patterns between mother and infant.

Tracing inheritance patterns in nonhuman primates can present challenges because of their long lives, but some evidence for genetic vocal attributes have been found in cross-breeding and cross-fostering experiments. Two gibbon species - the Borneo gibbon (Hylobates muelleri) and the white-handed gibbon (H. lar) - were cross-bred to produce two hybrid offspring, who sang their appropriate sex-specific "parts" in gibbon songs, each with structural similarities to the same-sex parent (Marler & Tenaza, 1977). In contrast to results found in previous cross-fostering studies on macaques (Masataka & Fujita, 1989), Owren et al. (1992) found that after placing two infant rhesus monkeys (Macaca mulatta) with Japanese macaque (M. fuscata) mothers, and two infant Japanese macaques with rhesus monkey mothers, in their first week of life, no significant differences appeared in the call behavior appropriate to each species.

Different rearing conditions and their effect on chimpanzee (Pan troglodytes) vocalizations have been compared as well, and results have shown that the structure of whimpers and screams in infants is similar between captive and wild populations, suggesting that these sounds may be present at birth (Randolph & Mason, 1969).

Recent research continues to find evidence for genetic inheritance of call structure in certain species. In a study by Castro and Snowdon (2000), captive infant cotton-top tamarins (Saguinus oedipus) under twenty weeks of age were found to comprehend and "produce chirps with adult form", suggesting that there is some fixity of chirp structure at birth.

Though inheritance of fixed call structures is generally acknowledged as a contributing factor, many scientists believe that with their high intelligence, long lives, and long periods of social development, nonhuman primates have great potential capacity for vocal learning. Learned vocalizations would naturally become more evident in studies where increased stereotypy of the known species repertoire would occur with age. Learning requires change, and "if change is predictably responsive to experiential influences, then learning may be said to occur" (Biben & Bernhards, 1995). Some of these changes may be attributed to learning, and some to physical maturation.

Technology has facilitated our ability to investigate vocal communication through quantitative analysis by spectrograph. A recent study of squirrel monkeys improved on Winter et al.'s (1973) methodology with contrasting results. By analyzing more types of calls and using more sophisticated techniques, Hammerschmidt et al. (2001) discovered ontogenetic changes for all of the 12 call types he investigated. Most of the vocal development took place within the first four months of the squirrel monkeys' lives. These structural changes were measured using more fine-grained acoustic parameters than the previous study, allowing analyses of higher frequencies and varying durations.

There is also evidence for learned vocalizations in several species of prosimian. Zimmerman (1989) found that much of the vocal repertoire of infant Senegal galagos (Galago senegalensis) differed significantly from that of adults, and most of the known adult calls developed gradually after five to nine months of age. Zimmerman found similar results in 1991, concluding that for gray mouse lemurs (Microcebus murinus), "stabilization of a part of the vocal communication system...may be triggered by learning".

Much of the evidence for learned vocal development in primates has come from Old World species, particularly vervet monkeys (Chlorocebus aethiops). Dorothy Cheney and Robert Seyfarth have obtained longitudinal data on wild populations of vervets in East Africa, showing how their communication systems develop and mature. By conducting a series of playback experiments, they investigated the ontogeny of alarm calls (1980). Although they found that infant vervets produce some rudimentary alarm calls, they were significantly less sophisticated in structure than those used by adults. Most adult vervets have a repertoire that includes acoustically distinct calls for leopards, martial eagles, pythons, and baboons. Infant vervets both call and respond in a more generalized way, only distinguishing between terrestrial and aerial predators, for example. Infants also gave alarm calls to arbitrary species and objects that posed little or no threat, such as pigeons and falling leaves. This suggests that vocal development in vervets occurs gradually over a number of years.

Other evidence for gradual learning in vervets was found in studies conducted on grunts, a type of contact or cohesion call found in many Old World species (Seyfarth & Cheney, 1986). Many types of grunts are distinguishable by the monkeys themselves and by sonogram analysis, but humans find them difficult to differentiate acoustically. It is generally thought that grunts and other contact calls play an important role in the social cohesion of group-living primates. Seyfarth and Cheney found, through a playback experiment, that although infant vervets did use grunt calls from birth, they were significantly different in usage, structure, and duration from those used by adults. These acoustic features changed at different rates during the first three years of life, suggesting that the association between call type and social context develops over time.

Vervet monkeys use "wrr" calls during intergroup encounters. Hauser (1989) investigated the comprehension and production of these calls, and concluded that they develop gradually over time. Interestingly, Hauser found that the "contact" and "lost" "wrrs" used by infants for the first three months disappear from the repertoire until ten months, when the "intergroup" "wrr" begins to form. One possible explanation Hauser suggested is the influence of the acquisition of other calls, a phenomenon known in human childhood development as "phonemic regression". A child's acquisition of new words may interfere with the production of earlier words, but these articulation rules stabilize as "...these earlier word forms regain their acoustic similarities to those produced by adults...". By focusing on topics such as phonemic regression, future studies may strengthen evidence for learned vocalizations in nonhuman primates.

Other studies on Old World species find similar results. For example, during agonistic encounters, significant contextual errors were found in the scream calls of pigtail macaques (Macaca nemestrina) under three years of age (Gouzoules & Gouzoules, 1989); and studies on talapoin monkeys (Miopithecus talapoin [Gautier, 1974]) and Japanese macaques (Nishimura, 1973) have found that vocal behavior differs both quantitatively and qualitatively between age classes. The development of the loud calls of male Nilgiri langurs (Trachypithecus [or Presbytis] johnii), were found to coincide with social maturation and experience, and were not completely fixed at birth (Hohmann & Vogl, 1991). The responses to conspecific barks in infant chacma baboons (Papio cynocephalus ursinus) were also found to be learned gradually over time and driven by experience (Fischer et al., 2000).

There is also a growing body of evidence for learned vocal development in several species of New World primate. Research into human speech development and birdsong ontogeny has found similarities in their vocal learning patterns. By studying primate species with social structures (i.e. monogamous families) similar to those of most humans and song birds, Snowdon et al., (1986) found parallel evidence for vocal learning in two species of callitrichid. The "long calls" of cotton-top tamarins and saddleback tamarins (Saguinus fuscicollis) serve as intergroup spacing mechanisms, promote intragroup cohesion, and attract potential mates, playing an important role in daily social life. Initial observations have suggested that some of these calls do not appear in the vocal repertoire until maturity, while others illustrate experiential differences. Further, infant cotton-top tamarins and pygmy marmosets (Callithrix [or Cebuella] pygmaea) have been observed "babbling" in the absence of other vocalizations before shifting to more adult-like calls (Snowdon et al., 1986; Elowson et al., 1998; Snowdon, 1999). Babbling is found in human infants and is generally thought to play an important role in human vocal development (Locke, 1993); evidence for the same behavior in nonhuman primates suggests parallels in ontogeny. Durational and structural differences in the "trill" and "J-call" of different age classes in pygmy marmosets have also been observed, leading to similar conclusions (Elowson et al., 1992). In contrast to earlier studies on squirrel monkeys, Biben and Bernhards (1995) found that production and usage of "masted" and "peep" calls undergo age-specific changes varying with affiliative relationships, suggesting learned influences.

Studies on vocal development in apes have focused on teaching apes human languages, but the natural ontogeny of ape vocalizations is less well documented. There is evidence, however, to suggest age-class differences in some species. In gorillas (Gorilla spp.), mature silverback males have a vocal repertoire distinct from younger blackback males in usage and frequency, suggesting an element of social learning (Marler & Tenaza, 1977). Similarly, in chimpanzees, specific vocalizations such as laughter, barks, rough grunts, whimpers, and pant-grunts are used more extensively by individuals of specific age classes (Marler & Tenaza, 1977). Though the chimpanzee "pant hoot" has received more scientific attention than other ape vocalizations, there is little or no information on its ontogeny. Evidence suggests, however, that rates and durations of pant-hooting behavior may differ between age classes (Pusey, 1990; Marler & Hobbet, 1975).

There is much speculation about the role physical growth and maturation may play in the ontogeny of vocal repertoires. Predicted models of physiological vocal development would involve consistent patterns of the changes in repertoire over several groups in variable environments. In most species there is little data to formulate conclusive inferences, although sex classes of some species with distinct vocalizations may provide clues. The "loud calls" of adult males in species such as gibbons (Hylobates spp.) and howler monkeys (Alouatta spp.) are not possible without the supralaryngeal accessory organs or vocal sacs, which only develop at sexual maturity. Moreover, individuals of these species have not been observed "practicing" these sounds, suggesting physical growth as a key component (Newman & Symmes, 1982).

Studies on Old World species have offered some suggestions on the role of physical growth in vocal development. Research on captive populations of Japanese macaques with infants reared in isolation found three consistent stages of vocal development within thirty weeks of birth comparable to control groups, suggesting fixed patterns that develop gradually (Kawabe, 1973). In studies of the "coo" calls of infant rhesus macaques, Hammerschmidt et al. (2000) found no sex or environmental differences in the developmental stages of the vocalizations, but they did find positive correlations between increased body weight and more mature vocal production, suggesting physical growth as the main factor.

Similar results have been found in studies on a few species of callitrichids. Vocal development in pygmy marmosets has been attributed at least partially to physical growth, because duration of the "trill" call consistently increased with age for four out of five litters studied (Elowson et al., 1992).

As new data emerge, primate vocalizations are proving to be more complex than had been thought. Researchers are now speculating on the contribution made by other factors such as affiliative processes, individual variation, and social conditions. Because many of the vocalizations associated with these contexts are softer and more cryptic to the human ear, they are more difficult to measure (Snowdon, 1999).

As far back as the 1960s, inferences were already being made about the social influences of vocal ontogeny. Randolph and Mason (1969) conducted a laboratory experiment on two groups of chimpanzees ranging in age from two to four years. They found, when comparing the wild-born chimpanzee group to a captive, socially-deprived group, that wild-born chimpanzees produced more distress vocalizations when isolated from familiar group members than the socially-deprived individuals.

New World monkey "babbling" has provided some evidence of the role socialization plays in vocal development: "Within a month after birth tamarin infants are frequently left on their own ...[and]...begin to call and continue to call until a caregiver retrieves them...later on we began to notice clear elements of adult vocalizations in the chatter. However, the vocalizations were not given in the proper context and many vocalizations were juxtaposed which would never be heard in adults. Many...are not perfectly formed." (Snowdon et al., 1986). Other research on callitrichids has described these babbling bouts as complex (Elowson et al., 1998), although the sounds have no obvious referent (Snowdon, 1999). Elowson et al. (1998) found social reinforcement to be a contributing factor in the rates and durations of babbling in infant pygmy marmosets. A caregiver was more likely to respond by contact and grooming to infants who babbled than to those who did not. Snowdon (1999) speculates that nonhuman primate infant babbling "...can be an important phenomenon for understanding how affiliative interactions shape vocal development...".

Other evidence of social influence has been investigated in cotton-top tamarins, who show abrupt patterns of vocal change that vary as an individual enters breeding status (Roush & Snowdon, 1994). In other studies relating to the status of individuals, Roush and Snowdon (1999) found that sub-adult cotton-top tamarins shifted to more adult-like "chirp" calls only when they were mated and increased their dominance status, while subordinate individuals did not. Callitrichids have also shown a tendency to change their vocal rates and structures when infants are present (McConnell & Snowdon, 1986; de la Torre, 1999). Snowdon (1999) has found inferential evidence that certain social interactions may inhibit the expression of adult calls, and that positive affiliative relationships with new mates change vocal structure.

Much research on the role of social conditions in vocal ontogeny has focused on the separation calls used by infant rhesus macaques. Rates and variants of "coo" call structure differ according to social context and whether infants are within visual range of their mothers (Snowdon, 1999). Other studies have focused on differences between closely related species, such as food calls in rhesus and Japanese macaques (Owren et al., 1992). The results of the cross-fostering experiments found substantial evidence for individual variation, suggesting that individuality may be explained by social influences of peers, especially in cross-fostered pairs. In another study comparing four Old World species - bonnet macaques (Macaca radiata), liontail macaques (M. silenus), Nilgiri langurs, and patas monkeys (Erythrocebus patas) - Hohmann (1991) found that overall differences between Macaca spp. and Presbytis spp. were probably related to maternal behavior and treatment of infants by other group members, that is, to social influences.

In sum, most scientists agree that primate vocalizations are complex and often cannot be defined as simply genetic or learned. A call that begins as a genetic vocalization may develop and evolve differently with maturity and/or learning, depending on the species and type of call, and researchers are only beginning to formulate inferences regarding social influences. Some researchers maintain that conclusive evidence for vocal learning has been difficult to obtain because we may not be asking the right questions of the right species, and we must take into account selection pressures and individual vocalizations in order to fully understand differences between those calls that are necessary to survive, and those that are socially flexible (Roush & Snowdon, 1994). A more complete understanding is required of vocal repertoires and neural mechanisms across taxa, as well as the roles of physiological development, dialect, individualized calls, production, usage, and response. More cross-fostering studies would further our understanding of the roles of genetics, imitative learning, and social learning. We do not know whether full call repertoires, or simply sound production, are fully developed at birth. Longitudinal studies of individuals and investigations of species less well adapted to captivity are necessary.

References

Biben, M., & Bernhards, D. (1995). Vocal ontogeny of the squirrel monkey, Saimiri boliviensis peruviensis. In E. Zimmerman, J. D. Newman, and U. Jurgens (Eds.), Current topics in primate vocal communication (pp. 99-120). New York: Plenum Press.

Castro, N. A., & Snowdon, C. T. (2000). Development of vocal responses in infant cotton-top tamarins. Behaviour, 137, 629-646. de la Torre, S. (1999). Environmental correlates of vocal communication of wild pygmy marmosets, Cebuella pygmaea. Ph.D. Thesis, University of Wisconsin.

Elowson, A. M., Snowdon, C. T., & Lazaro-Perea, C. (1998). Infant 'babbling' in a nonhuman primate: Complex vocal sequences with repeated call types. Behaviour, 135, 643-664.

Elowson, A. M., Snowdon, C. T., & Sweet, C. J. (1992). Ontogeny of trill and J-call vocalizations in the pygmy marmoset, Cebuella pygmaea. Animal Behaviour, 43, 703-715.

Fischer, J., Cheney, D. L., & Seyfarth, R. M. (2000). Development of infant baboons' responses to graded bark variants. Proceedings of the Royal Society of London, 267, 2317-2321.

Gautier, J. (1974). Field and laboratory studies of vocalizations of talapoin monkeys (Macaca talapoin). Behaviour, 51, 209-273.

Gouzoules, H., & Gouzoules, S. (1989). Design features and developmental modification of pigtail macaque, Macaca nemestrina, agonistic screams. Animal Behaviour, 37, 383-401.

Hammerschmidt, K., Freudenstein, T., & Jurgens, U. (2001). Vocal development in squirrel monkeys. Behaviour, 138, 1179-1204.

Hammerschmidt, K., Newman, J. D., Champoux, M., & Suomi, S. J. (2000). Changes in rhesus macaque 'coo' vocalizations during early development. Ethology, 106, 873-886.

Hauser, M. D. (1989). Ontogenetic changes in the comprehension and production of vervet monkey (Cercopithecus aethiops) vocalizations. Journal of Comparative Psychology, 103, 149-158.

Hohmann, G. (1991). Comparative analyses of age- and sex-specific patterns of vocal behaviour in four species of Old World monkeys. Folia Primatologica, 56, 133-156.

Hohmann, G., & Vogl, L. (1991). Loud calls of male Nilgiri langurs (Presbytis johnii): Age-, individual-, and population-specific differences. International Journal of Primatology, 12, 503-524.

Kawabe, S. (1973). Development of vocalization and behavior of Japanese macaques. In C. R. Carpenter (Ed.), Behavioral regulators of behavior in primates (pp. 164-184). Lewisburg: Bucknell University Press.

Lieblich, A. K., Symmes, D., Newman, J. D., & Shapiro, M. (1980). Development of the isolation peep in laboratory-bred squirrel monkeys. Animal Behaviour, 28, 1-9.

Locke, J. L. (1993). Learning to speak. Journal of Phonetics, 21, 141-146.

Marler, P., & Hobbett, L. (1975). Individuality in a long-range vocalization of wild chimpanzees. Zeitschrift für Tierpsychologie, 38, 97-109.

Marler, P., & Tenaza, R. (1977). Signalling behavior of apes with special reference to vocalization. In T. A. Sebeok (Ed.), How animals communicate (pp. 965-1033). Bloomington: Indiana University Press.

Masataka, N., & Fujita, K. (1989). Vocal learning of Japanese and rhesus monkeys. Behaviour, 109, 191-199.

McConnell, P. B., & Snowdon, C. T. (1986). Vocal interactions between unfamiliar groups of captive cotton-top tamarins. Behaviour, 97, 273-296.

Newman, J. D., & Symmes, D. (1982). Inheritance and experience in the acquisition of primate acoustic behavior. In C. T. Snowdon, C. H. Brown, & M. R. Petersen (Eds.), Primate communication (pp. 259-278). Cambridge: Cambridge University Press.

Nishimura, A. (1973). Age changes of the vocalization in free-ranging Japanese monkeys. In E. W. Menzel, Jr. (Ed.), Symposia of the IVth International Congress of Primatology, Volume 1: Precultural primate behavior (pp. 76-97). Basel: S. Karger.

Nottebohm, F. (1972). The origins of vocal learning. American Naturalist, 106, 116-140.

Owren, M. J., Dieter, J. A., Seyfarth, R. M., & Cheney, D. L. (1992). "Food" calls produced by adult female rhesus (Macaca mulatta) and Japanese (M. fuscata) macaques, their normally-raised offspring, and offspring cross-fostered between species. Behaviour, 120, 218-231.

Pusey, A. E. (1990). Behavioural changes at adolescence in chimpanzees. Behaviour, 115, 203-246.

Randolph, M. C., & Mason, W. A. (1969). Effects of rearing conditions on distress vocalizations in chimpanzees. Folia Primatologica, 10, 103-112.

Roush, R. S., & Snowdon, C. T. (1994). Ontogeny of food-associated calls in cotton-top tamarins. Animal Behaviour, 47, 263-273.

Roush, R. S., and Snowdon, C. T. (1999). The effects of social status on food-associated calling behaviour in captive cotton-top tamarins. Animal Behaviour, 58, 1299-1305.

Seyfarth, R. M., and Cheney, D. L. (1980). The ontogeny of vervet monkey alarm calling behavior: A preliminary report. Zeitschrift für Tierpsychologie, 54, 37-56.

Seyfarth, R. M., and Cheney, D. L. (1986). Vocal development in vervet monkeys. Animal Behaviour, 34, 1640-1658.

Snowdon, C. T. (1999). Affiliative processes and vocal development. In C. S. Carter, I. I. Lederhandler, & B. Kirkpatrick (Eds), The integrative neurobiology of affiliation (pp. 141-152). Cambridge: MIT Press.

Snowdon, C. T., French, J. A., & Cleveland, J. (1986). Ontogeny of primate vocalizations: Models from bird song and human speech. In D. M. Taub & F. A. King (Eds.), Current perspectives in primate social dynamics (pp. 389-402). New York: Van Nostrand Reinhold.

Winter, P., Handley, P., Ploog, D., & Schott, D. (1973). Ontogeny of squirrel monkey calls under normal conditions and under acoustic isolation. Behaviour, 47, 230-239.

Zimmerman, E. (1989). Aspects of reproduction and behavioral and vocal development in Senegal bushbabies (Galago senegalensis). International Journal of Primatology, 10, 1-17.

Zimmerman, E. (1991). Ontogeny of acoustic communication in prosimian primates. In T. Kimura, O. Takenada, & M. Iwamoto (Eds.), Primatology today: Proceedings of the XIIIth Congress of the International Primatological Society, Nagoya and Kyoto (pp. 337-340). Amsterdam: Elsevier Science Publishers.

Zimmerman, E. (1995). Loud calls in nocturnal prosimians: Structure, evolution and ontogeny. In E. Zimmerman., J. D. Newman, & U. Jurgens (Eds.), Current topics in primate vocal communication (pp. 47-72). New York: Plenum Press.

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Author's address: 40 Country Village Landing NE, Calgary, AB T3K 5K1, Canada [e-mail: lcorewyn@shaw.ca].
The author gratefully acknowledges the feedback and support of Dr. James Paterson of the University of Calgary.

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A Descriptive Analysis of a Spontaneous Dominance Overthrow in a Breeding Colony of Rhesus Macaques (Macaca mulatta)

Introduction

The social behavior of rhesus macaques is generally characterized by relatively stable and often linear dominance relationships between individuals within social groups (Maslow, 1936; Southwick, 1967; Walters & Seyfarth, 1987). However, spontaneous changes in dominance hierarchies have been observed in stable social groups in captivity (Ehardt & Bernstein, 1986; Samuels & Henrickson, 1983), yet the events immediately preceding these changes have rarely been seen or recorded, and the causal mechanisms have not been determined. Experimentally induced rank reversals in macaques have suggested precipitating factors, e.g., the absence and/or removal of agonistic allies, particularly those who are kin (Chapais, 1988; Chapais & Larose, 1988; Marsden, 1968). However, the explanations posed fail to account for all cases (Ehardt & Bernstein, 1986).

We observed the overthrow of the alpha female and reversal in rank of the members of the two high-ranking families within a single matriline in a captive social group in which dominance ranks among adults had remained stable for ten years. In accordance with Ehardt and Bernstein (1986), we use the term "overthrow" to describe the unexpected and unusually aggressive events associated with the reversal of rank relationships. The potential for severe and lethal injuries in captive social groups makes clear the need for researchers and colony managers to closely coordinate their research and management procedures, and to exchange information regarding the possible determinants of highly aggressive behaviors associated with reversals in rank (Ehardt & Bernstein, 1986; Samuels & Henrickson, 1983).

Background

Subjects: The members of a social group of rhesus macaques (Macaca mulatta) born in captivity at the Yerkes Regional Primate Research Center (now known as Yerkes National Primate Research Center) Field Station in Lawrenceville, Georgia, served as subjects. In 1992, ten years following formation of this group, it consisted of four adult males (7.5 -14.5 years), 36 adult females (3.5-14.5 years), and 37 juvenile males and females. In the ten years preceding this study, the group had a history of stable dominance relationships among its adult members. In particular, the respective positions of adult females within a single matriline of high-ranking individuals had not changed. The highest-ranking adult females, Herc, Mabel, and Um, are descendants of Nadine, a high-ranking female who died prior to the formation of this social group (See Table 1).

--------------------------------------------------------------------
                             [Nadine] 
                              (1965)
                                 |
         --------------------------------------------
       [Qq]                                       [Sloe] 
      (1972)                                      (1976)
         |                                           |
-----------------------                   ----------------------
[X]       Um       [X]                   Herc     [Wisk]    Katie 
(1976)   (1997)   (1979)                 (1983)   (1988)   (1990)
           |                               |
--------------------------------        ---------------------------------
  [X]   Mabel  Iago male Zwing male   [Ferd] male [Aorta]   Gyro   Zeus male 
(1976) (1983)   (1988)     (1990)        (1993)    (1989)  (1990)   (1992)
          |
 -----------------------------
[Tiny] male   Trev male   Whisper 
   (1988)       (1990)     (1992)  
--------------------------------------------------------------------

Table 1: Nadine's matriline. [ ]: not present at time of overthrow; X: stillbirth; ( ): year of birth; Bold: females involved in overthrow

Housing: The social group was housed at the Yerkes facility in an uncovered outdoor enclosure (38.1 m x 38.1 m), which comprised one quadrant of a four-unit compound. Two walls of each enclosure consisted of sheet metal fencing (2 m height) attached vertically above chain link fencing (3 m height). The interior walls were constructed of sheet metal only, minimizing visual and tactile contact between animals in adjacent enclosures. A climbing structure was located in the center of each enclosure, surrounded by six concrete culverts that provided cover. Adjoining one of the chain link walls in each outdoor enclosure was a temperature-controlled indoor room (3 m x 10 m). On two opposite exterior fences, an observation platform overlooks the two enclosures below. Originally, the enclosures contained native north Georgia flora, but at the time of these observations, the substrate was primarily soil. For a more detailed description of Yerkes outdoor animal enclosures, see Bernstein, Gordon, and Rose (1974a). Hard plastic balls were provided periodically as toys.

Procedures: The social group was observed regularly as part of a research protocol five days per week during the three years surrounding the overthrow of the alpha female, Herc. In addition, as routine management, the group was monitored for health problems and any unusual activity twice daily. The dominance rank of each of the animals in the social group was determined from "does-receives" matrices comprised of the outcomes of dyadic agonistic interactions (Bernstein, 1970; Wilson, 1981).

Dominance Reversal

Ten years of stability in the respective positions of the highest ranking females were followed by a reversal that occurred after the temporary removal of the alpha female, Herc, for veterinary care.

Herc was removed from the social group for medical treatment of mild dehydration on Friday, April 3, 1992, and was found to have a bacterial infection. Following five days of antibiotic treatment, Herc was returned to the social group.

Approximately 1.5 hours into Herc's absence, Gyro, Herc's daughter, almost two years old and second in the dominance hierarchy after her mother, was observed carrying Mabel's newborn infant Whisper. Mabel, the second ranking adult female, persistently followed Gyro and attempted to retrieve the infant. Gyro continued to elude her. After about 5 minutes, Mabel grabbed and bit Gyro on one side of her face, and then on the other, as Gyro squealed submissively. Mabel then retrieved Whisper from the ventrum of Gyro and pinned Gyro to the ground. Gyro continued to squeal. Mabel released Gyro after about 30 sec. Gyro fled squealing and head-flagging for agonistic aid. When she received none, Gyro ran toward and presented to Nubbs, a low ranking adult male. Nubbs looked about, mounted Gyro and then presented to her for grooming. Gyro continued head-flagging for aid for a few seconds, and then began to groom Nubbs. Over the next five days, Gyro was observed to avoid and submit to Mabel, Um, and their offspring. These events clearly indicate change in rank order among Nadine's descendents, the highest ranking females in the group.

Herc was returned to the group at approximately 11:00 a.m. on April 8, 1992. The alpha male, Yi, immediately approached and mounted her. The other group members exhibited general excitement and vocalized, but did not approach Herc and Yi at that time. Gyro was first to approach within 2 m, but she did not contact Herc. Next Mabel and Um approached, grimaced, and then avoided Herc as she approached. Yi mounted Herc again.

About 2 minutes after the return of Herc, Gyro began to scream at Um and Mabel, and to enlist Herc against them. Um charged Gyro, then Herc defended Gyro by charging and biting Um. Herc restrained Um who was squealing, and continued to bite her. Mabel attempted to aid Um by biting Herc. Yi, the alpha male, responded in defense of Herc, biting and mounting Mabel. At this point Um ceased screaming, and both Herc and Um repeatedly bit one another. Gyro was unable to enlist others, approached and clung to Herc's ventrum momentarily during the struggle, and then fled. Mabel then joined Um in attacking Herc. Yi provided no additional aid and moved away from the three females. After about one minute, Herc broke free and fled, but Um and Mabel pursued and continued to attack her. Soon after, Herc was crouched in the tunnel door leading to the indoor quarters. At this point a number of other animals, including low ranking adult females and juveniles, joined Um and Mabel, biting and mobbing Herc. The four adult males kept clear from and did not participate in the mobbing.

To prevent further injury, Hambright entered the compound to remove Herc. All of the attackers dispersed, except a juvenile male, Frank, who persisted in attacking Herc until Hambright approached within 1 m, and then Frank fled. Herc appeared to be in shock, because she allowed Hambright to pick her up and place her in a transfer box. She was immediately taken to the Field Station veterinary hospital for treatment; an examination revealed no lethal wounds. The entire incident took place within a ten-minute period.

Following the removal of Herc, observation of the group continued. Mabel and Um had received scratches and bruises, but were not seriously injured. They sat together at the back of the compound with kin (Iago, Trev, Zwing and Whisper), and Yi, the alpha male. Gyro attended to the minor scratches she had received and kept within 5 m of Mabel and Um, occasionally lip-smacking and grimacing in submission to them. Mabel and Um appeared to ignore Gyro. Gyro was removed from the group an hour later and housed with her mother in order to prevent further aggression directed toward her.

Twenty-one days later, Gyro was returned to the social group. She assumed rank beneath the members of the Um family without any aggressive interactions at the time of reintroduction. Upon her release into the group, Gyro grimaced, approached, and maintained proximity to Mabel. Herc remained in the veterinary hospital and gave birth to Zeus on April 12, 1992.

Six months later, during the breeding season, Herc and Zeus were placed in the capture unit portion of the indoor enclosure of her former social group. When group members were first allowed to see Herc, the 3rd, 4th, and 5th ranking adult females threatened her through the fence. Um defended Herc by chasing the females. During the remaining time Herc was housed in the capture unit, she received few threats from group members. When Herc and Zeus were released into the outdoor enclosure two weeks later, her daughter Gyro approached, contacted, and then bit Herc. Herc fled in response. When a lower ranking female, Jody, from an unrelated matriline threatened Herc, Gyro and Um defended Herc by chasing and biting Jody. During this reintroduction, Herc squealed frequently, but she also chased the 4th, 5th and several other lower ranking adult females. When Mabel approached, Herc grimaced and presented to her. The two then sat together and groomed each other. Gyro asserted her rank and displaced Herc in grooming Mabel. At that point it was clear that Herc ranked below Mabel, Um, and Gyro. Yet two weeks later, Herc ranked over Gyro, as Gyro was observed submitting to Herc. This latter dominance rank order among members of the Nadine matriline, and that of the group overall, remained stable during the following year.

Discussion

The events described above bear structural similarity to overthrows described previously, in that they are rare and appeared to be opportunistic outcomes of intra-family agonistic behavior among females (Ehardt & Bernstein, 1986). The reintroduction of individuals into an established rhesus social group can be a potent stimulus for eliciting aggression (Bernstein et al., 1974b, Southwick, 1967). Bernstein and colleagues (1974b) proposed that when introduced into an established social group, competitors for high rank meet with greater resistance than individuals that initially assume a subordinate rank and gradually work their way up through the hierarchy. Further, whether an individual can easily reclaim his/her former position depends on a number of factors such as duration of separation, individual variation, past social history of the individual, social support, whether any significant restructuring of the social dominance hierarchy occurred during his/her absence, ability to form a rapid alliance with resident high-ranking animals, and size and physical condition of the individual returned (Bernstein et al., 1974b). Chapais and Larose (1988) predicted that dominant Japanese macaques (Macaca fuscata) may need kin support to maintain their rank when subordinates are able to form coalitions.

Herc was briefly separated from the social group for five days. During this time, the opportunistic outcome of the "kidnapping" incident appears to have resulted in a significant restructuring of the dominance hierarchy as the entire Um family rose above Gyro, who had previously been second only to Herc, her mother. Herc's initial return to the group began much as we had expected given the group's history of stability. She was greeted and mounted by the alpha male Yi, and Mabel and Um appeared to have resumed their subordinate positions relative to that of Herc. Behavioral interactions such as these are rather typical of the return of high-ranking individuals following a brief absence (T. P. Gordon, personal communication). Unfortunately, the routine return changed radically when Gyro enlisted Herc against Mabel and Um and the alpha male failed to aid Herc and Gyro in their aggression toward Mabel and Um. As in previous reports (see Bernstein, et al., 1983; Bernstein & Ehardt, 1985; Ehardt & Bernstein, 1986), there was an unexpected reversal from submissive to aggressive behavior by a previously subordinate individual (Um) that escalated into severe and prolonged contact aggression, which is ordinarily controlled in rhesus social groups. Submissive behavior patterns, e.g., crouching passively, failed to inhibit the attacks and the aggression peaked with the mobbing of the deposed individual by lower ranking females and their offspring.

The number of close kin in the Sloe family of the Nadine matriline from whom Herc could enlist agonistic aid had gradually, over two years, dwindled to two yearlings following the permanent transfer of her mother Sloe, the death of her daughter Aorta, and the permanent transfers of Herc's 4-year-old brother and 3-year-old son. In contrast, the Um family of the Nadine matriline included two adult females, Mabel and Um, and three juvenile males, Iago, Trev, and Zwing. Despite a number of separations for routine veterinary treatment, some of which exceeded five days, the former alpha female, Sloe, had been unchallenged. However, unlike Herc, Sloe had both adult and juvenile close kin allies for agonistic support in the event of any threat to her position by members of the Um family. These events underscore the importance of agonistic alliances in the maintenance of female dominance hierarchies.

As for physical condition, Herc was fully recovered and near term in pregnancy when returned from veterinary treatment. It is possible that her pregnancy could have contributed to physical and/or motivational limitations in terms of self-defense. Physical condition was more likely to have been a significant factor in the defeat of yearling Gyro by Mabel, an adult more than twice her weight and stature. Like her mother, Gyro had no immediate kin available for agonistic aid except another yearling, Katie.

The limited degree in which adult males participated is another important similarity with past reports. Both here and in the report of Ehardt and Bernstein (1986), the alpha male mounted female aggressors, and briefly attempted but failed to maintain the pre-existing female rank order. Subsequently, the alpha male moved away from the agonistic interactions between females. The other adult males not only refrained from participating, but also avoided them. This predominance of female-female aggression is consistent with the conclusion that female dominance hierarchies operate independently of adult males (Ehardt & Bernstein, 1986).

While the dominance relationships of individuals outside the two families in conflict were unchanged as in previous reports, in contrast, the surviving members of Herc's family did not fall to the bottom of the group hierarchy, but instead assumed the rank just beneath the Um family. One factor that may account for this is that Herc and Gyro were removed prior to serious injury, and upon their subsequent reintroductions, they were allowed in proximity to and received agonistic aid from their kin in the Um family.

In conclusion, we had a unique opportunity to observe and provide a detailed description of the preceding and perhaps causal events of a rare and substantial change in female dominance ranks within a social group of rhesus macaques. We agree with Samuels and Henrickson (1983) that regular behavioral monitoring and documentation of rank relationships are essential in the management of social groups of macaques, and that it is imperative to exercise extreme caution when considering and undertaking the removal of high-ranking animals and their kin support. Further, communication between management and investigators regarding management practices and other factors that may influence the stability of dominance hierarchies is critically important. We hope that this report will aid in the anticipation and prevention of dominance overthrows and their potentially grave consequences in captive groups of macaques.

References

Bernstein, I. S. (1970). Primate status hierarchies. In L. A. Rosenblum (Ed.), Primate behavior: Developments in field and laboratory research, Vol. 1 (pp. 71-109). New York: Academic Press.

Bernstein, I. S., & Ehardt, C. L. (1985). Intragroup agonistic behavior in rhesus monkeys (Macaca mulatta). International Journal of Primatology, 6, 209-226.

Bernstein, I. S., Williams, L., & Ramsay, M. (1983). The expression of aggression in Old World monkeys. International Journal of Primatology, 4, 113-125.

Bernstein, I. S., Gordon, T. P., & Rose, R. M. (1974a). Aggression and social controls in rhesus monkey (Macaca mulatta) groups revealed in group formation studies. Folia Primatologica, 21, 81-107.

Bernstein, I. S., Gordon, T. P., & Rose, R. M. (1974b). Factors influencing the expression of aggression during introductions to rhesus monkey groups. In R. L. Holloway (ed.), Primate aggression, territoriality, and xenophobia (pp. 211-240). New York: Academic Press.

Chapais, B. (1988). Rank maintenance in female Japanese macaques: Experimental evidence for social dependency. Behaviour, 104, 41-59.

Chapais, B., & Larose, F. (1988). Experimental rank reversals among peers in Macaca fuscata: Rank is maintained after the removal of kin support. American Journal of Primatology, 16, 31-42.

Ehardt, C. L., & Bernstein, I. S. (1986). Matrilineal overthrows in rhesus monkey groups. International Journal of Primatology, 7, 157-181.

Maslow, A. H. (1936). The role of dominance in the social behavior of infrahuman primates. Journal of Genetic Psychology, 49, 161-198.

Marsden, H. M. (1968). Agonistic behavior of young rhesus monkeys after changes induced in social rank of their mothers. Animal Behaviour, 16, 38-44.

Samuels, A., & Henrickson, R. V. (1983). Outbreak of severe aggression in captive Macaca mulatta. American Journal of Primatology, 5, 277-281. Southwick, C. H. (1967). An experimental study of intragroup agonistic behaviour in rhesus monkeys (Macaca mulatta). Behaviour, 28, 182-209.

Walters, J. R., & Seyfarth, R. M. (1987). Conflict and cooperation. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. T. Struhsaker (Eds.), Primate societies (pp. 306-317). Chicago: Aldine.

Wilson, M. (1981). Social dominance and female reproductive behaviour in rhesus monkeys (Macaca mulatta). Animal Behaviour, 29, 472-482.

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Corresponding author: M. Karen Hambright, Dept of Social Sciences and Physical Education, Coastal Georgia Community College, Brunswick, GA 31250 [e-mail: khambrig@cgcc.edu].
This investigation was supported by NIMH Grant MH46676 and NIH Grant RR-00165 from the National Center for Research Resources. The Yerkes Primate Research Center is fully accredited by the American Association for Accreditation of Laboratory Animal Care. We wish to thank Professor T. P. Gordon for his helpful comments on earlier versions of this manuscript.

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Travelers' Alert: Yellow Fever in Monkeys in Southern Brazil

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Urine-Washing Behaviors as Condition-Dependent Signals of Quality by Adult Mantled Howler Monkeys (Alouatta palliata)

Introduction

Communication may be defined as the transmission of information from one animal ("the sender") to another ("the receiver") that presumably benefits both (Bradbury & Vehrencamp, 1998). Information is contained in signals whose design may vary in response to constraints imposed by the physical and biotic (including social) environments as well as the physiological mechanisms of the organisms (Bradbury & Vehrencamp, 1998). Chemical signals are the most primitive mode of animal communication, and their transmission must broadcast molecules the complete distance between sender and receiver (Bradbury & Vehrencamp, 1998).

Milton (1975) studied "urine-rubbing" (i.e., "urine-washing": Milton, 1985) in mantled howlers (Alouatta palliata) at Barro Colorado Island, Panama, a semideciduous lowland tropical forest, concluding that these behavior patterns were most likely to function in "intra-troop cohesion" and that adult males were likely to employ urine-washing behaviors during periods of stress. Milton also considered other possible functions of urine-washing in mantled howlers such as thermoregulation, communication of cycling state by females, and repelling of insects.

Data on urine-washing behaviors from two groups of mantled howlers in two habitats of Costa Rican tropical dry forest are presented here. It is concluded that these behavior patterns function as condition-dependent signals (see Brockmann, 2001) in sexual and agonistic contexts for adult males and females who advertise their quality by way of volatile urinary compounds.

Subjects, Study Site, and Definitions

The study was conducted in 1976 and 1977 at Hacienda La Pacífica, Cañas, Guanacaste, Costa Rica (10° 28' N, 85° 07' W). Details on study groups (Group 5: three adult males, 15 adult females, 402 hours of observation; Group 12: two adult males, eight adult females, 114 hours of observation), habitats (seasonal: Group 5, riparian; Group 12, deciduous), data collection (focal and ad lib.), social organization and mating system (multimale-multifemale, polygynandrous), and life history may be found elsewhere (Jones, 1980, 1985, 2000, and references).

"Copulation" was defined as mounting with intromission, with or without ejaculation. "Displacement" is used to mean that one animal approaches (moves at least 1 meter toward) another and the second moves away. The "receiver" of the display's signal was defined as the "sender's" nearest neighbor, although other animals within the range of the chemical signal may also detect the information presumably contained in the urine's volatile compounds ("eavesdropping": Bradbury & Vehrencamp, 1998).

The nonparametric Chi-squared test ("goodness of fit") was used to assess statistical significance with alpha set at 5%.

Results

Milton (1975) described the behavior patterns characteristic of urine-washing in mantled howlers. She observed howlers "rubbing urine on the soles of the feet and/or palms of the hands as well as the ventral surface of the tail and, occasionally, the throat" (p. 105). In addition to the motor patterns she described, I observed a behavior pattern in which both adult males and females passed the palm-like ventral surface of the tail and surrounding pelage through a stream of urine and washed urine over the body with the tail in a swooping movement. This gave the urine-wash behavior pattern the appearance of a stereotyped display.

The results of my observations for Groups 5 and 12 are presented in Table 1. In the riparian forest, urine-washing was observed 42 times (0.11 observations/hour), in the deciduous forest, seven times (0.06 observations/hour). The difference in rates is not statistically significant (Chi-squared = 1.47, df = 1, P > .05). Because of the small sample size for Group 12, further analyses will be based solely upon the results for Group 5.

Urine-washing was more likely to be observed in sexual than in agonistic contexts (Chi-squared = 13.71, df = 1, P = 0.001). Adult males of Group 5 displayed urine-washing behaviors 20 times, 14 times in sexual contexts to cycling females (see Jones, 1985) and six times in agonistic contexts to other adult males (Chi-squared = 3.2, df = 1, P > 0.05). Adult males, then, were as likely to display to other males as to females, although contexts differed. Agonistic contexts involving males were generally associated with mating competition since one of the males (i.e., sender or receiver) was always associated with a cycling female. Y and G, the dominant and middle-ranking males, respectively, each directed urine-washing behaviors to other males one time. R male, the lowest ranked, exhibited urine-washing behaviors to other males four times (?2 = 3.00, df = 2, P > 0.05). Males, then, display to other males with equal likelihood. When displays to females are considered, Y exhibited urine-washing behaviors to cycling females seven times, G, five times, and R, twice (?2 = 2.71, df = 2, P > 0.05). Thus, males were equally likely to display to cycling females.

----------------------------------------------------
Group  Direction of   Sexual  Agonistic   ?   Total
       Interaction   Context   Context 
----------------------------------------------------
  5      M to F         14                      14
         M to M                   6       6
         F to M         16                      16
         F to J                   1              1
         F to ?                           5      5
----------------------------------------------------
  12     M to F          1                       1
         M to ?                           1      1
         F to M          2                       2
         F to F                    2             2
         F to ?                           1      1
----------------------------------------------------
Total                   33         9      7     49  
----------------------------------------------------

Table 1: Urine-washing behaviors observed in two A. palliata groups (5 and 12), including direction of display (sender(r) receiver) and context. Sexual contexts were identified by the exchange of sexual behaviors (e.g., the "lingual display" [Carpenter, 1934; Jones, 1985] and copulation). Agonistic contexts were identified by the presence of behaviors such as the "branch-break" display (Carpenter, 1934; Jones, 2000), paedomorphic (immature sounding) whines (Jones, 1985), fighting (Carpenter, 1934; Jones, 1985, 2000), and displacements. J= juvenile. See text for further explanation.

Adult females of Group 5 exhibited urine-washing behaviors 22 times, 16 times directed at an adult male, once directed at a juvenile (Chi-squared = 13.24, df = 1, P = 0.001), and five times for which the recipient was undetermined. Related to this, displaying females were usually noted to be cycling. Females directed urine-washing behaviors to Y male, seven times, to G male, four times, and to R male, five times (Chi-squared = 0.87, df = 2, P > 0.05). Thus, females displayed to all males equally. Certain of these displays by females appeared to function to incite male-male competition since they were sometimes given in contexts in which more than one male was present (n = 7), sometimes engaging in agonistic interactions (e.g., exhibiting the "branch-break" display during ritualized confrontations [Carpenter, 1934; Jones, 2000]). Urine-washing behaviors also sometimes occurred in association with vocalizations by either sex (N = 8); thus, chemical, visual, and auditory signals may be components of a "compound display" (Bradbury & Vehrencamp, pp. 394-397). It is also likely that urine-washing by adult females pertains to female-female competition since the two ?? ? events observed in Group 12 (Table 1) occurred in association with pairwise displacements.

Discussion

Condition-dependent behaviors are a function of environment or phenotype. The present results suggest that urine-washing behaviors by adult male and female mantled howlers are condition-dependent signals of quality (see Gosling & Roberts, 2001), since males displayed with equal likelihood to cycling females and to other males in contexts that appeared to reflect intrasexual competition for mates. Because the frequency of displays by males did not differ significantly as a function of dominance rank, they may represent "cheap" (low-cost) signals (Silk et al., 2002) that facilitate the assessment of quality and decrease the likelihood of damaging aggression. Females displayed urine-washing behaviors equally to all males, suggesting that, from their point of view, all males were equally good mating partners or that urine-washing behaviors functioned to incite male-male competition. These results are consistent with previous findings for this group that females exhibited sexual solicitations equally to all three males (Jones, 1985). The present study, combined with other work considering the significance of urinary signals in Alouatta (Milton, 1975; Jones, 2002), highlights the need for additional research, including laboratory and field experiments, on urine-washing behaviors and related topics in this taxon.

References

Bradbury, J. W., & Vehrencamp, S. L. (1998). Principles of animal communication. Sunderland, MA: Sinauer Associates, Inc.

Brockmann, H. J. (2001). The evolution of alternative strategies and tactics. Advances in the Study of Behavior, 30, 1-51.

Carpenter, C. R. (1934). A field study of the behavior and social relations of howling monkeys. Comparative Psychology Monographs, 10, 1-167.

Gosling, L. M., & Roberts, S. C. (2001). Scent-marking by male mammals: Cheat-proof signals to competitors and mates. Advances in the Study of Behavior, 30, 169-218.

Jones, C. B. (1980). The functions of status in the mantled howler monkey, Alouatta palliata Gray: Intraspecific competition for group membership in a folivorous Neotropical primate. Primates, 21, 389-405.

Jones, C. B. (1985). Reproductive patterns in mantled howler monkeys: Estrus, mate choice and copulation. Primates, 26, 130-142.

Jones, C. B. (2000). Alouatta palliata politics: Empirical and theoretical aspects of power. Primate Report, 56, 3-21.

Jones, C. B. (2002). How important are urinary signals in Alouatta? Laboratory Primate Newsletter, 41 [3], 15-17.

Milton, K. (1975). Urine-rubbing behavior in the mantled howler monkey Alouatta palliata. Folia Primatologica, 23, 105-112.

Milton, K. (1985). Urine washing behavior in the woolly spider monkey (Brachyteles arachnoides). Zeitschrift für Tierpsychologie, 67, 154-160.

Silk, J. B., Kaldor, E., & Boyd, R. (2000). Cheap talk when interests conflict. Animal Behaviour, 59, 423-432.

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Author's address: Dept of Psychology, School of Liberal Arts, Livingstone College, 701 W. Monroe St, Salisbury, NC 28144 [e-mail: cjones@livingstone.edu and howler425@cs.com].

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Personnel / Animal Relationships: Affectionate or Neutral? A Discussion

Most correspondents agreed that development of an affectionate relationship with the animals in their charge is almost unavoidable (Clark, Hartley, Hunnicutt, Lablans, Moreau, Van Loo, Vitale). Empathy can even arise in researchers who go to great lengths to try to ensure that their data are objective (Sherwin). "Having a close relationship with your animals is necessary to regard them as living beings, rather than biological test tubes. As such, you are more careful and patient, and will think more about what the procedures mean to the animals. You will become more creative in finding animal-friendly alternatives for the procedures you need to do on the animals. You will thus increase the well-being of your animals and, by doing so, make them better research subjects and increase the validity of test results" (Van Loo).

There was a consensus that emotional attachment provides an assurance that the animals receive optimal care, both physically and behaviorally (Clark, Hartley, Van Loo, Vitale). "If I didn't think about the animals in my care, I wouldn't notice that someone seems a little off today, he's not participating in social activities like he normally does. I wouldn't notice that one animal suddenly flinches when I feed her something with a spoon, indicating a possible tooth problem. I've seen 'caregivers' that treat the animals with complete indifference miss a million details that they should have noticed. They don't clean well, are callous to the animals, and forget important things. I have watched animals cringe or cower when these individuals enter the room. I have seen these individuals breaking for lunch rather than take a few extra minutes for enrichment. Their emotions may not be absent from the situation, but they're focused somewhere else and so they don't do a good job since they aren't emotionally vested in the outcome" (Hunnicutt). A relationship based on trust rather than fear is particularly important when potentially dangerous animals such as macaques are being trained to actively cooperate during handling procedures (Lablans, Moreau). "Whether such a relationship enhances training success is another question, but it certainly is an effective safeguard against injuries resulting from defensive aggression" (Reinhardt).

There was disagreement about whether it is more difficult to establish a relationship with some animal species than with others. "I wonder if there is a size limit. Is it still possible to establish a relationship of trust with mice, where they will come to you and enjoy being with you, where you can exchange signs of affection?" (Olsson). "There is definitely a taxonomic hierarchy of emotional attachment anywhere you go; the higher you go the more likely bonding will occur" (Hartley). It was pointed out that to work closely with individual animals or a small group of animals and to observe them for an extended period of time is probably a more important factor for the development of a bond with them than their evolutionary relatedness with our own species or their size (Patterson-Kane, Reinhardt). If you take the time to discover the uniqueness of individual animals and to get to know their species-typical needs well enough to develop empathy for them, you will readily form close ties also with the perhaps less charismatic species such as pigs, rats, mice or chickens (Morton, Patterson-Kane, Van Loo).

Concern was expressed that establishing an affectionate relationship with experimental subjects and knowing them as individuals would hamper one's impartiality and capacity to be objective when observing and registering their behavior (Olsson). A caregiver strongly objected: "It seems to me that we get hung up on trying to divorce our emotions from what we hope to be our objectivity. I do not think that any normally functioning human being in the world does anything for any reason other than emotional. Sure, research is done to answer questions, but isn't the premise of all research to make human (or animal) lives better? If you want to make lives better, it's because of emotion, not because you are logically attached to life" (Hunnicutt).

"Having a name for the animals is one way of being personal" (Olsson). Several participants of this discussion give names to the animals in their charge or to the animals they study as a tool to quickly remember and recognize individuals (Hartley, Patterson-Kane) and/or as a reflection of their empathy (Moreau, Troc, Vitale). Identification numbers are kept in the records for cross-reference (Hartley, Troc). "As a clinical veterinarian I had the experience that nonhuman primate caregivers became markedly more concerned for and interested in individual animals in their charge when the identification number tags on the cages were replaced with name tags. I guess we can all relate much better to names than to numbers, and we tend to treat named animals versus numbered animals differently. The labels (numbers or names) we put on animals are irrelevant as long as we take the time to get an understanding of the subjects' needs and treat them according to those needs" (Reinhardt).

Naming can have its pitfalls. "We should remember that sometimes there are very good reasons for NOT giving laboratory animals names. When we give an animal a name, this is often because of our anecdotal impression of its appearance or behavior. But this can subsequently influence the way that we think about how an animal responds, or the motivations behind its behavior" (Sherwin). Two correspondents responded that name-giving is the result of our subjective, direct (e.g., reconnaissance observations prior to onset of data collection) or indirect (e.g., information gathered about a research subject from caretakers) experiences with a particular animal and that it is this experience rather than the name per se that pre-conditions our perception of the subject. It's almost impossible not to be preconditioned (Hartley, Reinhardt).

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Publication Announcements

The American Journal of Primatology Editorial Board announces that manuscript submissions as e-mail attachments in pdf format are now welcomed and encouraged. Complete instructions for contributors are available at <www.interscience.wiley.com/jpages/0275-2565/info.html>, and are published in each issue of the journal.

Nursery Rearing

Gerry Ruppenthal and Jim Sackett are co-editing a book, Nursery Rearing of Nonhuman Primates in the 21st Century, to be published in the Kluwer/Plenum series titled Developments in Primatology: Progress and Prospects, edited by Russell Tuttle. They are seeking normative data on any aspects of growth (body weights, brain, skeletal, or dental parameters, etc.) or physiology (hematology, immunology, hormone values, etc.), to be included in either an appendix or an online Web supplement. They are especially interested in data for rare species and species found mainly in zoo nurseries, although generally unavailable data on common laboratory species are also of interest. One primary requirement for inclusion will be a sufficient description of the nursery or hand-rearing housing, husbandry, and testing conditions under which the data were collected. They expect to publish the book by summer, 2003, so interested participants need to contact them as soon as possible.

They also wish to provide information on husbandry techniques and outcomes for nursery- or hand-rearing of any prosimian, marmoset, or tamarin species, and for other New World monkeys (with the exception of squirrel monkeys). To date, they have found only a few individuals with such information. If you are interested in participating or want more information please contact Jim [e-mail: jsackett@bart.rprc.washington.edu] or Gerry [e-mail: gruppenthal@mail.magee.edu], University of Washington Primate Center, P.O. Box 357330, Seattle, WA 98195. - posted to Primate-Science, November 14, 2002

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Applications for 2003 AVTA Exam

For further information, and the application packet, contact AVTA Executive Secretary, P.O. Box 426, Rossville, IN 46065 [e-mail: vetamac@geetel.net]. Request either an electronic or paper copy version of the application. Include your name, address, phone number and e-mail address. The completed packet must be received by the Executive Secretary no later than January 31, 2003.

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Research and Educational Opportunities

The Glenn/AFAR Scholarships for Research in the Biology of Aging are designed to attract potential scientists and clinicians to aging research. They provide PhD and MD students the opportunity to conduct a three-month research project. Students will work in an area of biomedical research in aging under the auspices of a mentor. Each scholarship carries an award of $5,000. Deadline for receipt of application is February 26, 2003. For an application, see <www.afar.org/grants.html> or contact the American Federation for Aging Research office [212-703-9977].

NIH Graduate Partnerships Program

While scientists at the National Institutes of Health (NIH) traditionally have participated in the training of graduate students on an ad hoc basis, graduate programs at universities have never been able to take full advantage of the resources available on the NIH campus to help achieve their predoctoral training objectives. To improve this situation, in July, 2000, the NIH implemented the Graduate Partnerships Program (GPP). The GPP has the responsibility to formally link NIH intramural research with universities in the training of predoctoral students in the biomedical sciences and to facilitate the development, operation, and oversight of university-NIH predoctoral training partnerships. The GPP's Website, <gpp.nih.gov/overview/index.html>, comprehensively provides extramural institutions and scientists descriptions of and access to the research groups at the NIH, facilitating the development of ad hoc and formal arrangements between extramural and intramural research groups, with the GPP serving as broker and facilitator.

In addition, the GPP has expanded a prior model for university-NIH partnerships in broad areas of research training. Currently, there are nine of these partnerships: Johns Hopkins University (Biological Sciences); George Washington University (Genetics); University of Maryland (Biophysics); University of Pennsylvania (Immunology); Boston University (Bioinformatics); University of Maryland (Hearing and Communication Disorders); Oxford University, England (Biomedical and Biological Sciences); Cambridge University, England (Health Sciences Scholars Program); and the Karolinska Institute, Sweden (Neurosciences). There are currently 24 predoctoral students in the National Cancer Institute Intramural Program participating in the GPP: 20 in the Center for Cancer Research (CRC), and four in the Division of Cancer Epidemiology and Genetics. While these broad arrangements more aggressively broker connections between graduate programs and intramural research groups, they do not involve any NIH funding or formally integrate extramural and intramural scientists in a specific training program.

Field Studies in Animal Behavior

The Georgia Institute of Technology and Zoo Atlanta present a four-week field course in animal behavior, tentatively scheduled from June 9 to July 6, 2003, for six semester credits in psychology. The course takes place in Atlanta (four days at the zoo), South Africa (three days), and Kenya (20 days). The goal of the course is to provide intensive instruction in animal behavior and observational methodologies. In Atlanta, students are taught data collection methods and their application and general behavioral profiles for various taxonomic groups (i.e. primates, carnivores, ungulates, birds). This information is then applied in the field through daily observations designed to permit comparisons of the same species in different habitats as well as comparisons across closely-related species. In addition, students are assigned several small-scale research projects to further their understanding of scientific methods. Observational assignments are supplemented by readings, discussions, and lectures by field scientists. The course also places strong emphasis on conservation, and students read about and discuss many of the issues related to conservation in eastern Africa. Students visit a variety of locations, including national parks and reserves, private research centers, sanctuaries, and private game reserves, as well as local cultural centers.

Estimated cost will be $6500, which includes: roundtrip airfare Atlanta-Johannesburg-Nairobi, room and board, ground transportation, tuition, lecture fees, and park fees. The application deadline is February 15, 2003. For information, contact Tara Stoinski, Zoo Atlanta, 800 Cherokee Ave, Atlanta, GA 30315 [404-624-5826; fax: 404-627-7514; e-mail: tstoinski@zooatlanta.org]; for an application, e-mail <study.abroad@gatech.edu>.

Workshop and Symposium

The Midwest Division of the Charles Louis Davis, D.V.M. Foundation will present a Workshop and Symposium on Laboratory Animal Diseases, April 23-26, 2003, in Chicago, co-sponsored by the Biologic Resources Laboratory (BRL) of the University of Illinois at Chicago.

The BRL's 2" x 2" slide collection will be available for review at the BRL, 1840 West Taylor St, beginning at 8:30 AM, Wednesday, April 23rd, and continuing through Friday the 25th. The 2" x 2" slide collection includes 14,000 Kodachromes on laboratory animal diseases and management. In addition 3,000 glass micropathology slides with histories and sixty-six T60 video tutorials of the Foundation's Independent Study Center at the BRL will be available for individual and/or group study. Microscopes, projectors, and VCRs will be available. Members of the senior staff of the BRL will give Simulated Practical Examinations on Friday the 25th.

Dr. Dean Percy will be the speaker at the Symposium on Saturday, April 26. He will review the diseases of rabbits and rats. For the complete text of the announcement and for registration information, contact Jim Artwohl [e-mail: jeart@uic.edu] or the C. L. Davis Foundation [e-mail: cldavisdvm@earthlink.net].

Research and Conservation on Endangered Species

The Research and Conservation Department in Wildlife Reserves Singapore (WRS), which manages the Singapore Zoological Gardens, Night Safari, and Jurong Bird Park, aims to promote research and conservation on endangered species by directing, coordinating and facilitating relevant activities in those institutions. The Research and Conservation Department has resumed stewardship of the Wildlife Conservation Fund, renamed the Wildlife Research and Conservation Fund. A committee composed of senior managers from the Wildlife Reserves Singapore will judiciously manage the fund, which will support research and conservation of endangered species, especially in the biological hotspots of Southeast Asia.

Native biologists from government and non-government organizations and students from Southeast Asian countries are encouraged to apply to the Wildlife Research and Conservation Fund to carry out conservation research projects to protect endangered species and their habitats. Local and foreign nationals also may conduct research at WRS institutions. For details and a copy of the application procedures, contact Dr. G. Agoramoorthy, Director (Research and Conservation), Singapore Zoological Gardens, Wildlife Reserves Singapore, 80 Mandai Lake Rd, Singapore [e-mail: agoram@mail.nsysu.edu.tw]. "We look forward to working with you."

Fyssen Foundation Postdoctoral Study Grants

The aim of the Fyssen Foundation is to "encourage all forms of scientific enquiry into cognitive mechanisms, including thought and reasoning, that underlie animal and human behavior, their biological and cultural bases, and phylogenetic and ontogenetic development." The Foundation supports research in ethology, psychology, neurobiology, anthropology, ethnology, human paleontology, and archeology. The Foundation will award grants of up to 20,124 Euros per year for the training and support of postdoctoral researchers, under 35 years of age, working in these fields. They are intended to assist French research scientists who wish to work abroad, and foreign research scientists who wish to work in France. These grants are awarded for a maximum of one year.

Application forms may be obtained from the Secrétariat de la Fondation Fyssen, 194, rue de Rivoli, 7500l Paris, France [e-mail: secretariat@fondation-fyssen.org]; or see <www.fondation-fyssen.org/>. The closing date for proposals is March 31, 2003.

Courses in Laboratory Animal Science

Courses in laboratory animal science will be given at the Royal Veterinary and Agricultural University in Copenhagen, Denmark, as part of the postgraduate program Master of Laboratory Animal Science, but individual courses can be taken. The language of instruction is English. Homework is required in connection with each course, if one wishes to take the exam and get credit.

Courses available are: * Anesthesia, Analgesia, Euthanasia of Laboratory Animals: March 11-13, 2003; Course number 150132. Cost: 4850 DKK.
* Laboratory Animal Health and Pathology: March 10, March 17-20, March 24-28, 2003; Course number 150131. Cost: 9300 DKK. See <www.ifp.kvl.dk/education/animal/Master_3_2003.htm>.

For more information and to enroll contact Mette Sonne Brendstrup, Royal Veterinary and Agricultural University, Office of Continuing Education, Bülowsvej 17, DK-1870 Fredriksberg C, Denmark [+45 3528 2093 / +45 3528 3768; e-mail: efteruddannelse@kvl.dk].

2003 IPS - Martha J. Galante Award

Grant proposals for the 2003 Galante Award are solicited from professionals who are citizens of primate habitat countries. Money awarded is intended to be used for conservation training, such as courses or professional meetings, and may include: * transportation to a course or event location; * course or event fees; and * expenses during the event period. People interested in receiving this award should be officially connected to an academic institution or a similar organization (taking or giving courses, or doing research or conservation work). To apply, send * information about the program of interest (courses, congresses, symposia, field work, etc.); * a letter (in English) explaining your interests in participating in the course or event; * a CV in English; * a letter of acceptance for the course; and * two recommendation letters (including information about the referees). Send all this material to: Claudio V. Padua, PhD, IPE - Instituto de Pesquisas Ecológicas, UnB Colina Bloco G, Apto 503, cep 70910-900 Brasília DF Brasil [e-mail: cpadua@unb.br]. Review of applications will be made by the International Primatological Society's Conservation Committee, and the results announced by the end of August, 2003. The deadline for applications is May 1, 2003.

* * *

Correction

* * *

Meeting Announcements

The National Association for Biomedical Research (NABR) will be hosting its annual conference on legislative and regulatory issues in Washington, D.C., February 23-25, 2003, at the Metro Center Marriott. This conference is offered exclusively to official representatives of NABR member institutions. Researchers, government officials, and industry representatives will discuss developments affecting animal research: * legislative and regulatory policies; * political environment; and * animal rights campaign trends. See <www.nabr.org>.

The 8th "Luis Montané" Physical Anthropology Symposium, the 4th Congress on Primates as National Patrimony, the 1st Colloquium on Primates Across the Caribbean, and the 1st Cuban-Canary Islands Anthropology Encounter will be held together in Havana, Cuba, February 24-28, 2003, in commemoration of the 100th anniversary of the founding of the Montané Anthropology Museum. The program includes lectures by invited speakers, roundtables, workshops, colloquies, oral communications, and posters, as well as recognition to prominent scientists. Courses in primate management, anthropology, and health will be offered before the Congress. These will be four hours long and each will have a registration fee of US$15. Registration fees for the Congress are US$100 (US$50 for students). For more information, contact Lic. Armando Rangel Rivero, Secretario Ejecutivo, Museo Antropológico Montané, Fac. de Biología, Univ. de La Habana, Calle 25 # 455, entre J e I. El Vedado, Ciudad de La Habana 10400, Cuba [537- 832-9000/879-3488; fax: 537-832-1321; e-mail: montane@fbio.uh.cu]; or Antrop. Fís. Braulio Alberto Hernández-Godínez, Centro de Investigación de Proyecto CAMINA A.C., Calzada de Tlalpan 4430, México D.F., México [55732468; fax: 55735545; e-mail: eopithecus@hotmail.com].

An official visa is required to travel to Cuba. The Organizing Committee suggests that you contact travel agencies representing MERCADU S.A. in your country.

Trends & Expectations, the AAALAC Conference on Quality Laboratory Animal Care, will be held May 19-20, 2003, in Reston, Virginia. For details, see <www.aaalac.org/conference.htm>.

The Canadian Association for Laboratory Animal Science invites laboratory science organizations worldwide to the 42nd annual CALAS Symposium, June 21-24, 2003, in Québec City, to meet the Canadian scientific community and exchange viewpoints on "From Theory to Practice: Revisiting the 3 R's". See <www.calas-acsal.org/English/Symposium.html>.

The XVth Congress of the International Union of Anthropological and Ethnological Sciences on "Humankind/Nature Interaction: Past, Present and Future" will be held in Florence on July 5-12, 2003. For information, contact OLIVER Srl, Via Panciatichi, 40/11, I - 50127 Florence, Italy [+39 055 4368455; fax: +39 055 4368781; e-mail: oliver@dada.it]; or see <www.icaes-florence2003.com>.

The 28th International Ethological Conference will be held August 20-27, 2003, at Costão do Santinho Resort, Florianopolis, Brazil, on behalf of the International Council of Ethologists and hosted by the Brazilian Society of Ethology. The deadline for submission of abstracts, financial aid applications, and reduced registration rate is February 20. For information on the conference, contact Prof. Kleber del Claro [e-mail: delclaro@ufu.br]; for information on the scientific program, contact Prof. Regina Macedo [e-mail: rhmacedo@unb.br]; or see <www.iec2003.org/home.htm>.

The 8th World Congress of Veterinary Anesthesia will be held in Knoxville, Tennessee, September 16-20, 2003, hosted by the University of Tennessee College of Veterinary Medicine and the UT-Knoxville Center for the Management of Animal Pain, at the Knoxville Marriott Hotel. The deadline for abstract submissions is March 17. Information and on-line submission of abstracts will be available at <www.vet.utk.edu/wcva>. To receive e-mail notices and registration materials, send a request to <Conferences@utk.edu>, with "WCVA" as the "Subject".

The American Association of Zoo Veterinarians will hold its annual conference in Minneapolis, Minnesota, October 5-9, 2003. Program sessions include Nutrition, Pharmacology, Vaccinations, AZA Programs (SSP/TAG Veterinary Advisory Updates), Advances in Technology and Diagnostic Testing, Case Reports and Practice Tips, Hospital Administration and Leadership, Primates, Pathology, Conservation Medicine, and Emerging Diseases. There will also be a poster session, veterinary and graduate student paper competitions, and workshops/wet labs. For information, see <www.aazv.org> or contact Wilbur Amand, VMD, Executive Director/AAZV, 6 North Pennell Rd, Media, PA 19063 [610-892-4812; fax: 610- 892-4813; e-mail: AAZV@aol.com].

* * *

Positions Available

An assistant animal facility supervisor is sought for the Poolesville, Maryland, area. Candidates must be certified at the LAT level and have at least four years' experience in an animal facility, including experience with nonhuman primates. Send cover letters and resumes to: Priority One Services, Inc., Attn: Recruiter, 6600 Fleet Dr., Alexandria, VA 22310 [fax: 703-971-0117]. EOE; Drug Free Workplace.

Clinical / Research Veterinarian - Puerto Rico

The Caribbean Primate Research Center is seeking a clinical/research veterinarian, to be based at the Sabana Seca Field Station, and who will also oversee the well-being of the nonhuman primates on Cayo Santiago. This person must be familiar with USDA, NIH, and other regulations governing animal welfare and care and will have primary responsibility for retaining full AAALAC accreditation for the Center. In addition to clinical and colony management responsibilities, veterinarians assist researchers utilizing the resources of the Center and must develop their own research programs, either individually or in conjunction with other researchers.

Qualifications include a DVM degree from an AVMA-accredited college of veterinary medicine and a veterinary license from a state or territory of the U.S.A. A Puerto Rican veterinary license must be obtained before the end of the first year of employment. Experience in research and nonhuman primate clinical care, husbandry and research is highly desirable.

For more information, contact Janis Gonzalez, Caribbean Primate Research Center, P.O. Box 1053, Sabana Seca, PR 00952-1052 [787-784-0322; fax: 787-797-6500; e-mail: jagonzalez@rcm.upr.edu].

Clinical Veterinarian - Rochester, New York

The University of Rochester is seeking an additional Clinical Veterinarian to help support our diverse population of research animals. Our vivarium contains approximately 23,000 animals, including rodents, primates, rabbits, ferrets, dogs, cats, amphibians and birds. The clinical veterinarian will join a staff of three veterinarians and five licensed veterinary technicians. This position includes overseeing veterinary care, teaching methodology, and maintaining a sentinel health program, as well as evaluating the health of animals entering this facility and consulting with investigators on research matters involving animal use.

Previous experience is appreciated, but not necessary. New York State licensure is required. The University is an equal opportunity employer. Candidates are asked to send a resume to: April Tirabassi, Asst. Director of Finance and Administration, DLAM, Univ. of Rochester, 601 Elmwood Ave, Box 674, Rochester, NY 14642 [fax: 585 273-1085; e-mail: april_rajca@urmc.rochester.edu].

Sanctuary Director - Texas

The Texas Snow Monkey Sanctuary (TSMS), located on a 186-acre ranch about 75 miles south of San Antonio, provides a free-range environment for 325 snow monkeys, vervets, and baboons. The TSMS is seeking a Director, who will work with the Operations Site Manager in directing sanctuary operations including facilities, veterinary care, rescues, feeding/nutrition, etc. The Director will also ( provide some direct animal care to all animals at the facility; ( supervise animal care staff, volunteers, and interns; ( update and manage database and Internet communications; and ( establish cooperative efforts with other sanctuaries and animal care facilities.

A bachelor's degree, with a biology, zoology, or other appropriate science major, and some primatology courses are required, as well as animal care experience, including primates. Excellent communication skills and the ability to work in a team environment are also important. Two or more years of supervisory experience are desirable.

Housing is provided, along with a salary to be negotiated and excellent benefits. The TSMS is an affiliate of the Animal Protection Institute (API), a national animal advocacy nonprofit organization. Contact Alan Berger, Executive Director, API, 1122 S Street, Sacramento, CA 95814 [916-485-1707 ext. 211; fax: 916-447-3070; e-mail: aberger@api4animals.org].

Primate Colony Manager - Michigan

The University of Michigan is seeking a full time colony manager for over 100 rhesus macaques. The successful candidate will * assume full accountability for developing, implementing and realizing the department's strategic, operational, personnel and research objectives; * supervise the husbandry staff and oversee the operation of all research, colony facilities, research protocols, animals and staff; * ensure that the Department's goals and objectives support and enhance compliance with AAALAC, USDA and IACUC guidelines (an in-depth knowledge of the laws and regulations pertaining to laboratory animal care is required); * review, implement, and adjust Standard Operating Procedures (SOPs) to reduce the risks associated with working with macaques; * oversee the entire staff working with nonhuman primates (NHPs) to ensure compliance with the SOPs and safe handling procedures; * maintain liaison between the Department and the IACUC and veterinary staff; * host the IACUC, AAALAC, USDA and veterinary inspections; ( coordinate the disposition and acquisition of NHPs; and * oversee and assist in providing routine and emergency medical treatment to the NHPs. Minimum qualifications include a BA or BS in a science-related field or psychology, excellent verbal and written communication skills, and computer experience. Previous supervisory and NHP experience is preferred.

Please direct inquiries to Tiffany Bass, Univ. of Michigan, Dept of Pharmacology, 1301 MSRB III, Ann Arbor, MI 48109 [734-764-4560; fax: 734-764-7118; e-mail: tifbass@umich.edu].

Research Assistants - Philadelphia

Two research positions are currently available at Thomas Jefferson University: * A research assistant is needed to work on a behavioral toxicology project examining the effects of chronic low level manganese exposure on cognitive and motor functions in nonhuman primates (NHPs). The applicant will be responsible for training monkeys to perform attention, memory and motor tasks; recording behavioral observations; administration of manganese; and continued behavioral assessment of animals. The research assistant will also be responsible for data entry and analysis, maintaining animal records, providing environmental enrichment, and ordering supplies.

* A second research assistant is needed to work on a project examining the contributions of the nicotinic acetylcholine system to attention, memory and motor deficits associated with different stages of Parkinsonism in NHPs. The applicant will be responsible for training monkeys to perform attention, memory and motor tasks, will assist in the induction of Parkinsonism, and then will evaluate the nature of the cognitive and motor deficits and responses to administration of various nicotinic drugs through various stages of symptom progression.

Ideal candidates will have previous primate research experience. Applicants with prior research experience in other areas will also be considered. Minimum educational requirement is a bachelor's degree in psychology, physiology, neuroscience, or a related discipline. Good organizational and communication skills are essential, as is a desire to work closely with NHPs.

Contact Jay S. Schneider, Thomas Jefferson University, 1020 Locust St, Philadelphia, PA 19107 [Fax: 215-923-3808; e-mail: jay.schneider@mail.tju.edu].

Behavioral Neurobiology Postdoc - Switzerland

The Swiss Federal Institute of Technology invites applications for a postdoctoral research position to work on long-term consequences of early life experience in primates. Applicants should have a PhD in a life science, and preferably have experience in the study of primate EEG/sleep, neuroanatomy, or behavior. This appointment will be for two to three years. The application deadline is February 1, 2003. For additional information contact Dr. Christopher Pryce, Swiss Federal Institute of Technology, Schorenstrasse 16, CH-8603 Schwerzenbach, Switzerland [+41 1 655 7386; Fax: +41 1 755 7203; e-mail: pryce@behav.biol.ethz.ch].

* * *

Information Requested or Available

Although alternatives to methods based on the use of animals may not satisfy all requirements and needs of the biomedical research and toxicological testing communities, alternatives to the use of vertebrates are being developed and evaluated. Research on such methodologies is aimed at refining procedures to reduce pain and discomfort; to reduce the number of animals required to provide scientifically valuable results; and to replace live vertebrates when an alternative methodology can be verified and validated by the scientific community. The Toxicology and Environmental Health Information Program's Specialized Information Services, National Library of Medicine, NIH, has prepared Alternatives to the Use of Live Vertebrates in Biomedical Research and Testing: A Bibliography with Abstracts, to assist in: * refining existing test methods; * reducing animal usage; and * replacing animals as test systems. It can be accessed at <toxnet.nlm.nih.gov/altbib.html>. For more information, see that Website, or contact Vera W. Hudson, Project Coordinator and Scientific Editor, National Library of Medicine, NIH, 8600 Rockville Pike, Bethesda, MD 20894 [e-mail: VERA_HUDSON@NLM.NIH.GOV].

E-Mail Lists

Annie and Viktor Reinhardt, of the Animal Welfare Institute, have initiated a closed electronic forum on Laboratory Animal Refinement & Enrichment (LAREF) . The purpose of this discussion group is the factual exchange of experiences about ways to improve the conditions under which laboratory animals (all species) are housed and handled. The forum is intended to serve the international animal care community in its attempt to promote animal welfare and improve scientific methodology by avoiding or eliminating husbandry-related stress situations. The forum is open to animal care personnel, animal technicians, students, attending veterinarians, and researchers who have had first-hand experience in the care of animals kept in laboratories. Currently there are 70 subscribers from 15 countries. To join the group, please send a message to <viktorawi@siskiyou.net>, indicating your * name, * professional affiliation, * professional experience(s) and * professional interest(s).

The Academy for Animal Pain Management has developed an e-mail list for discussion of pain-related issues, and committees have been formed to address organizational needs. To join this group, contact Dr. Peter W. Hellyer [e-mail: phellyer@colostate.edu].

Topics in Primate Care

There is a new Primate Info Net (PIN) series, Topics in Primate Care (TPC). Issues will be posted periodically on both Primate Science and the Primate Enrichment Forum (PEF), and will include current topics (both original submissions and published material), references, news, and information on the topics of environmental enrichment, veterinary care, and colony management of nonhuman primates. This series is coordinated by David Seelig (University of Pennsylvania), Lyna Watson (Wyeth Genetics Institute), and Janette Wallis (University of Oklahoma Health Sciences Center). They encourage original submissions, including enrichment strategies and brief to moderately-sized articles or essays on enrichment or veterinary topics, as well as questions of general interest, which will be discussed in future issues in a Question & Answer section.

For information about subscribing to Primate Science or PEF, you may visit PIN Information Resources at <www.primate.wisc.edu/pin/outreach.html> and click on the link to discussion forums. Please submit original material or questions to David at <dseelig@vet.upenn.edu>, Lyna at <watsonl@gis.net>, or Janette at <janette-wallis@ouhsc.edu>. In addition, please write to us with any comments or suggestions on what you would like to see in this new series. TPC is supported by grants RR13511 and RR00167, National Primate Centers Program, NCRR, NIH.

More Interesting Websites

• Alphabetical listing of CITES Appendix I (threatened with extinction) primate species: <www.aesop- project.org/Primate_Trade/CITES_Appendices.htm>
• Definitions and explanation of regulation of trade in CITES Appendix I and Appendix II Species: <www.aesop-project.org/ Primate_Trade/CITES_Convention_Text.htm>
• Americans for Medical Progress: <www.amprogress.org>
• Animal Research News & Analysis (The Humane Society of the United States): <www.hsus.org/research>
• Annotated bibliography Refinment and Environmental Enrichment for All Laboratory Animals: <www.awionline.org/lab_animals/biblio/laball.htm>
• APHIS Fiscal Year 2001 Annual Report: <www.aphis.usda.gov/ac/awrep2001.pdf>
• Center for Orangutan and Chimpanzee Conservation: <www.prime-apes.org>
• Center for the Rehabilitation and Rescue of Primates, Peñaflor, Chile: <www.macacos.cl/>
• Clinical Neurology in Small Animals: Localization, Diagnosis and Treatment, by K. G. Braund. Publisher: International Veterinary Information Service: <www.ivis.org/special_books/braund/toc.asp>
• Coalition for Animals and Animal Research: <www.swaebr.org/cfaar/index.htm>
• Forests for Life program: <www.panda.org/forests4life/>
• Frontier forests of the world: Interactive forest maps: <www.wri.org/ffi/maps/>
• How does deforestation affect primates? <www-personal.umich.edu/~spencea/>
• NIH's Proactive Compliance Site Visits 2000 - 2002: A Compendium of Findings and Observations: <grants.nih.gov/grants/compliance/ compendium_2002.htm>
• NORINA, database of audiovisual aids and other alternatives/supplements to the use of animals in teaching and training: <oslovet.veths.no/NORINA>
• Report on current practice for assessing and monitoring the well-being of research animals in the U.K.: <www.lal.org.uk/pain/>
• TextBase, database of textbooks in Laboratory Animal Science: <oslovet.veths.no/textbase>
• Utrecht University Department of Laboratory Animal Science: <las.vet.uu.nl>

* * *

Grants Available

The National Institute on Aging (NIA) <www.nia.nih.gov/> solicits multi-component applications on biological mechanisms of aging in tissues and organs. Projects are encouraged that significantly advance basic biology research to understand how and why changes take place in tissues with age and how those changes relate to altered tissue and organ function. Projects that focus on molecular aspects, as well as cellular aspects, of tissue aging are encouraged. Projects are applicable under this announcement that a) emphasize molecular and cellular changes that are common among tissues with aging; b) compare mechanisms of aging change in different tissues; and c) investigate the effects of age-related changes in one cell type, tissue or organ that affect the function of another tissue or organ.

This program encourages basic research into processes that lead to altered function of tissues and organs as a result of aging. Research that takes maximal advantage of emerging genetic, genomic and proteomic information on humans and other animals to understand changes that occur with aging is particularly encouraged.

For information, contact Frank L. Bellino, Endocrinology, Physiology, NIA, 7201 Wisconsin Avenue, Suite 2C231 MSC 9205, Bethesda, MD 20892-9205 [301-496-6402; fax: 301-402-0010; e-mail: bellinof@nia.nih.gov]; Jill L. Carrington, Chief, Systems Branch, Biology of Aging Program, Musculoskeletal Biology, same address [e-mail: carringtonj@nia.nih.gov]; David B. Finkelstein, Cardiovascular Biology, same address [e-mail: finkelsd@nia.nih.gov]; Rebecca A. Fuldner, Immunology, same address [e-mail: fuldnerr@nia.nih.gov]; Stanley Slater, Geriatrics and Clinical Gerontology Program, same address, Suite 3E327 [301-496-6761; fax: 301-402-1784; e-mail: slaters@nia.nih.gov]; Bradley C. Wise, Neuroscience and Neuropsychology of Aging Program, same address, Suite 3C307 MSC 9205 [301-496-9350; fax: 301-496-1494; e-mail: wiseb@nia.nih.gov].

Applications submitted in response to this program announcement will be accepted at the standard application deadlines for program project grants, at <grants.nih.gov/grants/dates.htm>.

Comparative Biology: Mechanisms of Aging

The National Institute on Aging (NIA) is soliciting applications that use comparative biology approaches to understand the biological mechanisms that lead to changes in human and other animal cells and tissues with age. The major questions to be addressed are: How does increasing age lead to biological changes, especially decrements in cell, tissue and organ function; and what sets the rate of aging such that different organisms have different life expectancies? Studies that take advantage of the differences in aging and life expectancy between species and within species are encouraged.

Direct your questions about general scientific/research issues and regarding projects focused on non-neural tissues to: Jill L. Carrington, Biology of Aging Program, NIA, Gateway Bldg, Suite 2C231, 7201 Wisconsin Ave, Bethesda, MD 20892-9205 [301-496-6402; e-mail: carringtonj@nia.nih.gov]. For questions on studies focused on the nervous system, contact: Bradley C. Wise, Neuroscience and Neuropsychology of Aging Program, NIA, Gateway Bldg, Suite 3C307, 7201 Wisconsin Ave, Bethesda, MD 20892-9205 [301-496-9350; fax: 301-496-1494; e-mail: wiseb@nia.nih.gov]. The application receipt date is January 23, 2003.

Early Career Development, HIV/AIDS

The National Institute of Mental Health (NIMH) announces a program for competitive supplements to support interdisciplinary research and education on active interdisciplinary HIV/AIDS research grants funded through the Center for Mental Health Research on AIDS. This competitive supplement program encourages and supports HIV/AIDS interdisciplinary research and career development for qualified candidates through an expedited application process. The goals are: * to expand and foster the independent research capabilities of the candidate; and * to strengthen the ongoing research program of the parent grant. Applications may be submitted on behalf of postdoctoral and junior faculty candidates.

The complexity and interconnections of the rapidly growing area of the neuroscience and psychobiology of HIV-related disease underscore the need to provide research opportunities to young investigators so that they may break new ground in this area. It is anticipated that some of the most significant insights and advances in HIV disease are likely to emerge as a result of recognizing and appreciating the intricate interplay among the brain, environment, and behavior. Interdisciplinary and translational research approaches among basic, clinical, and services research are potentially powerful approaches to integrating the rapidly advancing findings in HIV/AIDS research. Yet there seems to be disciplinary fragmentation, with researchers from basic, clinical and services areas working in different venues.

Three major areas of HIV/AIDS research (HIV prevention science, NeuroAIDS, HIV therapeutics) would be facilitated and enriched through an organized research program with researchers employing different approaches. Research in these domains draws upon a number of disciplines such as epidemiology, neuropsychology, brain imaging, neuropathology, genetics, molecular biology, immunology, and behavioral and social sciences. In all cases, the proposed research must be an integral part of the ongoing interdisciplinary HIV/AIDS research program supported by the parent grant and must have the potential to significantly contribute to the research career development of the interdisciplinary candidate.

For information, contact David M. Stoff, Center for Mental Health Research on AIDS, Div. of Mental Disorders, Behavioral Research and AIDS, NIMH, 6001 Executive Blvd, Rm 6210, MSC 9619, Bethesda, MD 20892-9619 [301-443-4625; fax: 301-443-9719; e-mail: dstoff@nih.gov]. Application deadlines will be January 2 and September 1 of each year for the next three years.

Models for Emerging Diseases and Biodefense

The National Institute of Allergy and Infectious Diseases (NIAID) is offering a contract to provide * targeted screening to identify potential therapeutic and preventive modalities, as well as * resources to characterize additional antimicrobial activities of already licensed antimicrobial agents, and * small animal and nonhuman primate models to test the safety and efficacy of therapeutic and preventive modalities that target emerging infectious agents. The objective of this contract is to provide a range of developmental resources to bring new therapies and preventive measures from the laboratory to initial clinical testing in humans. For details see <www.niaid.nih.gov/contract/archive/RFP0339.pdf>. Responses will be due approximately January 30, 2003. For further information, contact Paul McFarlane, Contracting Officer, NIH, NIAID, Contract Management Branch, 6700-B Rockledge Dr., Rm 2230, MSC 7612, Bethesda, MD, 20892-7612 [301-496-0349; fax 301-402-0972; e-mail: pm24@nih.gov].

Noninvasive Measurement of Iron by MRI

The National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), and the National Institute of Biomedical Imaging and Bioengineering (NIBIB) invite Research Grant Applications for projects that have the potential to improve the utility of magnetic resonance imaging (MRI) as a method for quantitative determinations of tissue iron, especially in the liver, heart and brain. A quantitative means of measuring body storage iron that would be non-invasive, safe, accurate, and readily available, would improve the diagnosis and management of patients with iron overload. MRI potentially provides a useful and widely available technique for examining the three-dimensional distribution of excess iron in the body, but further research is needed to develop a way to make measurements quantitative.

Among the experts potentially useful in this research may be investigators active in the development of non-invasive measures of iron, scientists and engineers interested in improving MRI technology, clinicians who care for patients with iron disorders, and experts in the physics and chemistry of iron and in iron metabolism. Projects proposing collaborations among such individuals are particularly encouraged.

Direct questions about scientific/research issues to: David G. Badman, Hematology Program Director, NIDDK, 6707 Democracy Blvd., Rm 621, MSC 5458, Bethesda, MD 20892-5458 [301-594-7717; fax: 301-480-3510; e-mail: db70f@nih.gov]; or John W. Haller, Health Scientist Administrator, NIBIB, NIH, 6707 Democracy Blvd., Suite 920, Bethesda, MD 20892-2077 [301-451-4780; fax: 301-480-4973; e-mail: hallerj@mail.nih.gov]. Letter of intent due date is January 20, 2003, and application due date is February 19, 2003.

Housing, Husbandry, and Welfare in the British Isles

The Pharmaceutical Housing and Husbandry Steering Committee of the Universities Federation for Animal Welfare (UFAW) invites applications for research based in the British Isles into any aspect of laboratory animal housing, husbandry, and welfare, including effects on the quality of science. The cost of the project should be no more than £23,000 per year for up to three years. Application will be by a two-stage process with project supervisors initially submitting a brief Concept Note by January 24, 2003. For further information and for the Concept Note forms, write to UFAW, The Old School, Brewhouse Hill, Wheathampstead, Herts AL4 8AN, U.K. [01582 831818; fax: 01582 831414].

NHP Models of HIV-Associated Disorders

The National Heart, Lung, and Blood Institute (NHLBI) invites applications on the use of nonhuman primate models for the study of Human Immunodeficiency Virus (HIV)-associated pulmonary, cardiovascular, and hematologic disorders. These primate models (e.g., Simian Immunodeficiency Virus [SIV]- and Simian-Human Immunodeficiency Virus [SHIV]-infected monkeys) should be designed to facilitate the study of the biological and clinical characteristics of disorders of lung, heart, blood, and bone marrow, associated with HIV infections and co-infections as well as to evaluate novel methods for prevention and treatment of these conditions.

The intent is to stimulate collaborations among scientists devoted to studies of SIV/SHIV disease in primates as a model for human AIDS, and investigators with expertise and experience in the following fields of relevant research: studies of tuberculosis, Pneumocysis carinii pneumonia, pneumococcal pneumonia, and other pulmonary and cardiovascular infections/disorders and studies of the roles of blood cellular components in the genesis and progression of AIDS. Such collaborations should take advantage of the large wealth of knowledge and resources (e.g., biological and immunologic reagents) that have been generated during the past 15 years.

Please direct questions about scientific/research issues to: Sandra Colombini Hatch, Division of Lung Diseases, MSC 7956 [301-435-0222; fax: 301-480 3557; e-mail: hatchs@nhlbi.nih.gov]; Luiz Barbosa, Division of Blood Disease Research, MSC 7950 [301-435-0075; fax: 301-480-0868; e-mail: barbosal@nhlbi.nih.gov]; or Diane Reid, Division of Heart and Vascular Diseases, MSC 7940 [301-435-0515; fax: 301-480-1336; e-mail: reidd@nhlbi.nih.gov]. The address for all is NHLBI, 6701 Rockledge Dr., Bethesda, MD 20892. The letter of intent receipt date is February 20, 2003; and the application receipt date is March 20, 2003.

ACLAM Foundation Request for Proposals

The American College of Laboratory Animal Medicine (ACLAM) Foundation Committee announces their solicitation of research proposals in laboratory animal science and medicine. The deadline for letters of intent is February 12, 2003; full proposals must be received by May 6. Complete information is available at <www.aclam.org>; or contact: Dr. Martin Morin, Chairman, ACLAM Foundation, 208 Byford Dr., Chestertown, MD 21620 [410-810-1870; fax: 410-810-1869; e-mail: morinasc@hpiug.org].

The Foundation will focus funding on research in the following fields of laboratory animal science and medicine: * analgesia/anesthesia * animal behavior/well-being * diagnostics/diseases of laboratory animals * laboratory animal husbandry * refinement of animal models, including toxicology [note: emphasis is on the 3 R's, not on biomedical research model development] * zoonotic diseases. Successful grantees are encouraged to publish their results in peer-reviewed journals and must agree to provide summary research reports in lay language suitable for inclusion in ACLAM Foundation communications, fund raising solicitations, and the ACLAM Newsletter.

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Resources Available

The Wisconsin Primate Research Center Library and Information Service has established a special archive room to include the extensive records of rhesus monkey families maintained privately for many years by the late June Northrop Barker, a research physiologist at New York University. Dr. Barker's husband, Richard Barker, of Frenchtown, New Jersey, visited the Primate Center on July 12 to dedicate the archive and tour the center. Dick Barker established a $100,000 endowment through the University of Wisconsin Foundation to su