Physical maturation life-history classes and age estimates of free-ranging western gorillasЧinsights from Mbeli Bai Republic of Congo.код для вставкиСкачать
American Journal of Primatology 71:106–119 (2009) RESEARCH ARTICLE Physical Maturation, Life-History Classes and Age Estimates of Free-Ranging Western Gorillas—Insights From Mbeli Bai, Republic of Congo THOMAS BREUER1,2, MIREILLE BREUER-NDOUNDOU HOCKEMBA2, CLAUDIA OLEJNICZAK3, RICHARD J. PARNELL4, AND EMMA J. STOKES4 1 Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 2 Mbeli Bai Study, Wildlife Conservation Society—Congo Program, Brazzaville, Republic of Congo 3 Department of Anthropology, Washington University, St. Louis, Missouri 4 Wildlife Conservation Society, Bronx, New York Physical maturation and life-history parameters are seen as evolutionary adaptations to different ecological and social conditions. Comparison of life-history patterns of closely related species living in diverse environments helps to evaluate the validity of these assumptions but empirical data are lacking. The two gorilla species exhibit substantial differences in their environment, which allows investigation into the role of increased frugivory in shaping western gorilla life histories. We present behavioral and morphological data on western gorilla physical maturation and life-history parameters from a 12.5-year study at Mbeli Bai, a forest clearing in the Nouabalé-Ndoki National Park in northern Congo. We assign photographs of known individuals to different life-history classes and propose new age boundaries for lifehistory classes in western gorillas, which can be used and tested at other western gorilla research sites. Our results show that western gorillas are weaned at a later age compared with mountain gorillas and indicate slower physical maturation of immatures. These findings support the risk-aversion hypothesis for more frugivorous species. However, our methods need to be applied and tested with other gorilla populations. The slow life histories of western gorillas could have major consequences for social structure, mortality patterns and population growth rates that will affect recovery from population crashes of this critically endangered species. We emphasize that long-term studies can provide crucial demographic and life-history data that improve our understanding of life-history evolution and adaptation and help to refine conservation strategies. Am. J. Primatol. 71:106–119, 2009. r 2008 Wiley-Liss, Inc. Key words: age estimation; development; western gorilla; life-history classes; long-term studies INTRODUCTION Life-history traits and physical maturation are assumed to be the result of evolutionary adaptations to various socioecological factors and are shaped by differences in substrate use, body or brain size and diet [e.g. Kappeler & Pereira, 2003; Leigh, 1994a, 2004; Ross & Jones, 1999; van Schaik & Deaner, 2003; Walker et al., 2006]. Nutrition is an obvious factor affecting primate life-history pace. For example, rates of maturation and reproduction of wild animals are considerably slower than those of animals under foodprovisioned conditions [e.g. Altmann & Alberts, 2005; Leigh, 1994b; Sigg et al., 1982; Strum, 1991; Zihlman et al., 2007]. Spreading the metabolic needs for juvenile (JUV) maturation over a longer period (growth at a slow rate) in environments with poorer and unstable or unpredictable food availability will help to reduce the risks of starvation, primarily resulting from intraspecific feeding competition [Janson & van Schaik, 1993]. Hence this ‘‘risk-aversion’’ hypothesis assumes that feeding on seasonally available resources, such as ripe fruit, will result in prolonged periods of JUV maturation, and feeding r 2008 Wiley-Liss, Inc. on leaves that are assumed to be an abundant and predictable resource is expected to speed up the life-history pace of primates. Empirical evidence for the risk-aversion hypothesis has been equivocal [Leigh, 1994a; Ross & Jones, 1999; Wich et al., 2004, 2007]. For example, Leigh [1994a] demonstrated that more folivorous anthropoid primates Contract grant sponsors: Brevard Zoo; Chicago Zoological Society; Columbus Zoo and Aquarium; Cincinnati Zoo and Botanical Garden; Sea World and Busch Gardens Conservation Fund; Toronto Zoo; Wildlife Conservation Society; Woodland Park Zoo; Little Rock Zoo; Lincoln Park Zoo; Zoological Society of Milwaukee County Global Environmental Facility CongoPROGEAP; Louis Leakey Foundation; Wenner-Gren Foundation; German Academic Exchange Service (DAAD); Max Planck Society. Correspondence to: Thomas Breuer, Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany. E-mail: firstname.lastname@example.org Received 18 March 2008; revised 15 September 2008; revision accepted 17 September 2008 DOI 10.1002/ajp.20628 Published online 10 November 2008 in Wiley InterScience (www. interscience.wiley.com). Western Gorilla Maturation and Life History Classes / 107 have rapid growth rates in the earlier stages of ontogeny and cease growth earlier than nonfolivorous species and postulated a relationship between life-history pace and digestive system. Similarly, Godfrey et al.  found that folivorous primate species exhibit faster dental development. In contrast the risk-aversion hypothesis does not predict patterns of ontogenetic diversity in small-bodied New World monkeys [Garber & Leigh, 1997] and folivorous indriids mature more slowly than like-sized frugivorous lemurids [Godfrey et al., 2004]. Most of our knowledge about primate life-history evolution has been gained through broad-scale interspecific studies [e.g. Lee, 1999; Ross & Jones, 1999]. However, some life-history traits (e.g. weaning age, age at first reproduction or age at full body size) of a given species also vary according to the ecological conditions (phenotypic plasticity) [Lee & Kappeler, 2003]. Therefore, comparisons of closely related species or populations living in different environments would help to clarify the role of ecological factors in shaping life-history parameters. However, with a few exceptions [e.g. Altmann & Alberts, 2005; Barrett et al., 2006; Borries et al., 2001], empirical data from closely related species or populations of the same species are missing. In this study we provide life-history data on western gorillas (Gorilla gorilla) in order to investigate whether increased frugivory can lead to differences in life-history pace between closely related species within a single genus. Great apes mature slowly and have long life spans, making it difficult to obtain life-history data from wild populations [Knott, 2001] as most ape studies are too short to cover all stages of the life cycle. Long-term studies are therefore needed to provide detailed ape life-history data for addressing such evolutionary and ecological questions. Furthermore, population parameters and life-history data have important conservation implications in the light of the crisis now facing great apes [Tutin et al., 2005]. Gorillas are the largest living primates and they are primarily herbivores [Doran-Sheehy et al., 2006; Robbins, 2007; Rogers et al., 2004]. According to the risk-aversion model, they are assumed to mature much faster than other, more frugivorous apes and an ontogenetic analysis of captive African apes supports this assumption [Leigh & Shea, 1996]. Moreover, comparison of some life-history parameters with free-ranging chimpanzees (Pan troglodytes) and orangutans (Pongo spp.) supports the hypothesis of faster maturation of species with a more folivorous diet [Hill et al., 2001; Knott, 2001; Wich et al., 2004]. Our current knowledge about gorilla life-history patterns comes predominantly from one high-altitude mountain gorilla population and long-term study site (Karisoke Research Center) located at the extreme range of gorilla distribution in the Virunga Volcanoes [summarized in Robbins, 2007]—with preliminary data available on Grauer’s gorillas [Yamagiwa & Kahekwa, 2001]. However, western gorilla habitat differs from that of mountain gorillas: in lowland forests terrestrial herbaceous vegetation occurs at lower densities and is more patchily distributed [e.g. Rogers et al., 2004]. Western gorillas are more frugivorous than mountain gorillas with fruiting trees being more abundant but showing large seasonal variation in fruit availability [Masi, 2007; Rogers et al., 2004]. Differences in resource availability combined with reduced folivory could have direct effects on western gorilla development leading to slower life histories [Doran & McNeilage, 2001] and particularly to a later weaning age. If such differences in life-history patterns between western and mountain gorillas occur, then age boundaries delimiting life-history classes (infants (INF), juvenile (JUV), subadults (SAD), adults) should consequently differ between the two gorilla species. However, western gorilla researchers have typically adopted age boundaries from mountain gorillas (see Table I). This is simply owing to a lack of longterm field studies spanning a full generation meaning that previous studies of western gorillas could only accurately age immature gorillas that had been seen since birth, e.g. those of 1–2 years (yr) (or gorillas of up to 6 yr of age at Mbeli Bai) [Gatti et al., 2004; Magliocca et al., 1999; Parnell, 2002a; Stokes et al., 2003]. Moreover, in the early years of western gorilla studies, researchers aged wild gorillas by making comparisons with captive individuals, potentially leading to an underestimation of true age. Long-term demographic data on known individuals provide the ages associated with external and behavioral criteria that demark the boundaries of life-history classes [e.g. Altmann et al., 1981]. Here, we investigate whether the physical maturation of western gorillas supports the riskaversion hypothesis and is slower than that of mountain gorillas. Secondly, we aim to assign the age boundaries for western gorilla life-history classes, which have previously been impossible to accurately define owing to the lack of long-term studies, and introduce techniques that will help to compare physical maturation between different gorilla populations. Finally, we discuss the implications of our findings for the social structure, population growth and conservation of western lowland gorillas. METHODS Observations were made at Mbeli Bai, a 12.9 ha large swampy clearing (‘‘bai’’ in the local language) in the Nouabalé-Ndoki National Park, Republic of Congo [see also Parnell, 2002a; Stokes et al., 2003]. This pristine protected area has never been logged and no illegal human activities have been recorded in the study area since the start of the Mbeli Bai study in 1995 (following pilot studies in 1993 and 1994). We Am. J. Primatol. Am. J. Primatol. Subadult Juvenile Infant Age category Gorilla beringei beringei Gorilla beringei graueri Gorilla gorilla Gorilla gorilla Gorilla gorilla An infant is carried by a female for prolonged periods and remains closely attached to the female Schaller , Harcourt et al.  and Watts  Subadults have more A subadult is slender bodies, advanced beyond the starting to show juvenile period secondary sexual characteristics and A juvenile is weaned No morphological and more description provided independent but with in the references a plump morphology, remaining close to the mother and carried dorsally under stressful situations An infant is still suckling and carried by the mother Gatti et al. a Behavioral and morphological and life-history markers This study This study Harcourt Watts  Yamagiwa Magliocca Parnell [2002a], et al.  and et al. Stokes et al. , and Harcourt Kahekwa  Gatti et al. a and Robbins et al. and Stewart    0–4 yr 0–4 yr 0–3 yr 0–3 yr 0–4 yr An infant is an 0–3b yr unweaned gorilla, still suckling and riding ventrally or dorsally. Infants are nutritionally dependent on their mother and do not survive maternal death. White buttock tufts of infants are very obvious. Infants have large heads in relation to the torso and possess very dark hair 3–6 yr 4 yr to age at 4–7 yr 3–6 yr 3–6 yr 4–7.5 yr Juveniles are weaned first gorillas that can copulation survive the death of the mother but they are occasionally seen suckling but predominantly feeding on their own. Juveniles are occasionally riding dorsally on the mother’s back and are often staying in close proximity to the mother 6–8 yr 7–10 yr 6–8 yr 6–8 yr 7.5–10 yr Subadult gorillas still for have slender females bodies and are much 7.5–11 yr smaller than adult for males size but are mainly Gorilla beringei beringei TABLE I. Comparison of Age Boundaries of Life-History Classes and the Markers (Morphological Markers in Bold) Used for Those Classes in Wild Western and Mountain Gorillas 108 / Breuer et al. 48 yr Young 12–15c yr silverback Blackback 8–12 yr Adult female 10–13 yr Over 13 yr – Age at first 10–13 yr copulation to approximately 11–13 yr Age at first Over 10 yr Over 8 yr labial swelling (6–7 yr) 12–15 yr 8–12 yr Over 8 yr 14–18 yr 11–14 yr Over 10 yr behavioral traits, such as independence from their group and aggression (in the case of males) Nulliparous females An adult female has An adult female is are slightly smaller obvious nipples and persistently than parous females developed breasts transporting infant, and can show small has a round body and sexual swellings. A smooth curves, parous female has sagging breasts with obvious elongated long nipples nipples and developed breast A blackback male is A blackback is similar A blackback is a reaching or larger in size or larger than female-sized gorilla than the size of an adult female, but with angular and parous females. with more developed muscular body with Blackback males musculature and red- conspicuous (start to) show signs brownish backs pectoralis major of secondary sexual muscle over which the characters, such as skin is usually taut longer arm hair and red-brownish saddle and strong neck muscles, but these signs are not yet fully developed Young silverbacks are A silverback’s saddle A young silverback is clearly larger than turns silver silvering but not yet parous females and fully grown reach adult male body length. However, their secondary sexual characters are incompletely developed. The brownish saddle is gray but not fully silver and the saddle hair is much shorter than that of adult females. Their sagittal crest is not yet fully developed and they are lacking a silverline. Young independent of the mother. Females can be seen with small labial swellings Western Gorilla Maturation and Life History Classes / 109 Am. J. Primatol. Am. J. Primatol. 414 yr Gorilla beringei beringei Gorilla beringei graueri Over 13 yr Gorilla gorilla Over 15 yr Gorilla gorilla A silverback is very large sized with prominent sagittal crest, muscular and angular build, with the pelage of the saddle and sometimes legs, neck and sides gray to silver in color; in fully mature males; hair of the lumbar region turns silver Behavioral and morphological and life-history markers silverbacks often range on their own Over 18 yr An adult silverback is a fully grown male with fully developed secondary sexual characters. He often has a peaked sagittal crest and his saddle coloration is gray to silver (sometimes also the legs). They can also develop a very bright silverline that is running along the belly. Adult silverbacks can have one or more females Gorilla gorilla The definitions used to assign the photographs are listed in the column ‘‘This study.’’ a No young silverback class, silverbacks are considered as males older than 12 yr. b The boundary of the infant class is occasionally set at an age of 3.5 yr, particularly in census studies, indicating that infants do not build sleeping nests [Weber & Vedder, 1983]. c Males over 12 yr are occasionally classified as silverbacks [e.g. Robbins, 2007; Williamson & Gerald-Steklis, 2001]. d Watts and Pusey  consider male gorillas at the age of 15–16 yr to be fully grown, but can mate exclusively with fertile females at 14 yr when they should be called silverbacks; juveniles are defined as males between 4 yr and age at first copulation and adolescents are between age at first copulation and approximately 11–13 yr. Silverback Over 15d yr Gorilla beringei beringei TABLE I. Continued 110 / Breuer et al. Western Gorilla Maturation and Life History Classes / 111 collected data during nearly continuous monitoring by four principal investigators and assistants from February 1995 until July 2007 on 303 different gorillas living in 61 social units (groups or solitary males). We made observations with 15–45 telescopes from a platform overlooking the clearing. Gorillas were habituated to the presence of observers on the platform and were individually identified from features such as size, pelage, shape of ears and brow ridge and nose prints [Parnell, 2002b]. One advantage of studying gorillas at forest clearings lies in the accumulation of demographic and life-history data of many different gorilla groups compared with only one or two groups followed in the forest. Limitations of bai studies include the gaps between visits of certain gorilla groups, which may in some cases span several months. These observational gaps can limit the accurate assessment of developmental processes, exact birth dates, and hinder our ability to distinguish ‘‘death’’ vs. ‘‘dispersal’’ away from the population in individuals that disappear from a group. However, it was often possible to limit the error in birth date estimates to just a few weeks (see below). Of the 303 gorillas monitored, 59 were parous females and 32 were adult males (silverbacks) when first observed (parous females and adult silverbacks (ASB) not considered in this study), whereas 110 offspring were born during the study. The remaining 102 gorillas were not fully adult when observed for the first time, and their birth date was estimated according to the procedure outlined below. Age Estimation Given the long period of immaturity in gorillas, a study duration of 12.5 yr is too short to track individuals longitudinally from birth to adulthood, and to provide exact ages for mature gorillas. We therefore used a combination of (1) the assignment of a reliable birth date based on observations of the first appearance of a newborn to a known female (n 5 110), or the first sighting of a newborn in a previously unknown group (carried ventrally, pink coloration; n 5 9), and (2) retrospective assignment of age to immatures of unknown birth date by comparing their physical maturation with individuals of known age. For INF born during the study, age was estimated based on morphology and size of the INF, their behavior and that of their mother at first observation of the newborn [Nowell, 2005; Nowell & Fletcher, 2007; Parnell, 2002b]. We compiled a good record of the physical maturation and behavior of INF of known age and could therefore improve the precision of estimated birth dates, even for groups that were absent from the clearing for several months. In the second case, we did not have accurate records of age, because the immature gorillas were either born before the study began or transferred into the population. We therefore assigned a birth date retrospectively using both external morphology (e.g. body size, hair color, body proportions) and behavior (e.g. suckling behavior, proximity to and dependence on the mother) compared with gorillas of known age. This was not possible in the first 5 yr of the study, because we did not have any gorillas of known birth date for comparison. We therefore retrospectively aged all nonadult gorillas (n 5 93), identified both at the start of the study and those that immigrated into the population, using supplementary data (e.g. field notes on physical maturation, photographs, 4200 hr of video footage). Retrospective classification will produce a degree of error in age estimates owing to individual variation, and certain biological questions such as age at first parturition can only be answered with data from gorillas of known birth date. However, we argue that, given the objective of dividing a continuum of development into biologically meaningful classes, our methodology for assigning age boundaries to lifehistory classes is justified. Life-History Classes and Their Age Boundaries To define the boundaries of life-history classes we first used morphological and behavioral criteria and also assigned photographs of known individuals to the different classes (see below). Some class boundaries are easier to recognize in some animals than in others and there is much variation between individuals [e.g. Strum, 1991]. Our definition of lifehistory classes follows Setchell and Lee  and has been adopted by various primatologists for a number of different species. We did not distinguish between males and females before females were considered adult (the blackback/female separation) (BB/AF) (Table II) because determining the sex of gorillas at Mbeli Bai is almost impossible once gorillas are no longer riding dorsal on the mother. The developmental stages of wild western gorillas have been assumed to mirror that of mountain gorillas [Nowell, 2005] and our criteria represent a summary of previous definitions of life-history classes and the morphological and behavioral markers used in different gorilla studies (Table I). Infancy ends when an animal can survive maternal death. Although there are large individual differences (see ‘‘Results’’), the INF/JUV transition is best described by life-history parameters, such as lactational weaning, which can be identified by field observations. Between November 2002 and July 2007 we noted every suckling event and assigned weaning age as the mid-point of visits before and after suckling termination [see also Nowell & Fletcher, 2007]. We furthermore provide information on the minimum age of survival after the disappearance of a mother and the minimum age of dispersal. The JUV period ends when puberty (SAD class) starts; however, that is difficult to determine without hormonal data unless external signs, such as sexual swelling in Am. J. Primatol. 112 / Breuer et al. TABLE II. Mean Estimated Ages of Western Gorillas That Were Assigned, Using 201 Photographs, to Different Life-History Stages by Two Judges LifeNumber Sample Known history of size year of class different (] of Judge birth assigned gorillas photos) 1 2 1 2 1 2 1 2 1 Yes Yes Yes Yes Yes Yes Yes Yes Yes 2 Yes 1 Yes 2 Yes 1 Yes 2 Yes 1 2 1 2 1 2 1 No No No No No No No 2 No 1 No 2 No Infant Infant Juvenile Juvenile Subadult Subadult Blackback Blackback Young silverback Young silverback Adult female Adult female Adult female/ blackback Adult female/ blackback Juvenile Juvenile Subadult Subadult Blackback Blackback Young silverback Young silverback Adult silverback Adult silverback Mean age (yr) of gorillas Minimum age Maximum age P-values of assigned to Standard (yr) of gorillas (yr) of gorillas Mann–Whitney Ulife-history error assigned to life- assigned to life- test of differences class (yr) history class history class between judgesa 6 7 15 14 5 9 2 2 1 11 14 34 32 20 25 16 11 3 2.2 2.6 5.2 5.4 9.0 9.6 12.8 13.4 15.3 0.4 0.4 0.2 0.2 0.2 0.3 0.2 0.2 0 0.5 0.5 4.0 4.1 7.9 7.9 11.4 11.4 15.3 3.6 4.2 9.4 9.0 10.9 11.9 13.8 13.8 15.3 1 3 15.3 0 15.3 15.3 1 1 12.2 – 12.2 12.2 1 1 12.225 0 12.225 12.225 1 6 12.086 0.457 9.802 12.611 1 5 12.543 0.017 12.517 12.611 1 2 4 4 10 11 6 1 3 10 13 34 28 23 6.5 7.5 9.7 10.4 11.8 12.1 16.2 – 0.3 0.5 0.3 0.2 0.2 0.2 6.5 7.1 7.1 6.5 10.7 10.7 14.8 6.5 8.0 10.9 11.5 14.6 14.8 18.2 7 33 16.4 0.3 12.2 18.3 6 42 20.0 0.3 17.4 23.6 5 33 20.7 0.3 17.6 23.6 0.358 0.441 0.199 0.226 – – 0.751 – 0.659 0.218 0.382 0.159 Photos were assigned according to external appearance of examples given in Figure 1 and morphological markers described in Table I and correspondingly number of gorillas assigned to life-history classes varied between two judges. P-values indicate if there were any significant differences between judges in their ratings of gorillas (using the estimated age as a measure of this). The data set is split by whether or not the year of birth is a known variable to the study. a Mann–Whitney U (MWU) exact test only applied when sample size was larger than three. females (albeit small in gorillas) or ejaculation of semen in males, can be observed [Setchell & Lee, 2004]. Puberty is considered to have ended once an individual attains reproductive competence. In mountain gorillas, nulliparous females go through a 2-yr period of adolescent sterility [Harcourt et al., 1980]. Thus the AF class used for mountain gorillas includes nulliparous females because first parturition occurs at a median age of 10 yr (range 8.7–12.8) [Harcourt et al., 1981; Watts, 1991]. For female gorillas born during our study, we noted when we first saw the small labial swellings and age at first Am. J. Primatol. birth, to determine the boundary between SAD/AF accordingly. Delayed male maturation is the result of sexual dimorphism in gorillas [Leigh & Shea, 1995]. Therefore, gorilla researchers define additional classes for males that are fertile but are not yet fully grown. We defined the SAD/BB boundary as the same cut-off point as for SAD/AF. To support this assignment, we also determined when males reached approximately the body length of an AF, which is one criterion for BB classification [Schaller, 1963]; however, this criteria from the early years at Karisoke has never Western Gorilla Maturation and Life History Classes / 113 been properly tested and others have grouped JUV and SAD into an old JUV class [Watts & Pusey, 1993]. We used digital photogrammetry to measure the body length of nonadult males and fully grown female gorillas [Breuer et al., 2007]. Between January 2004 and July 2007 we took digital photographs of gorillas standing perpendicular to the gorilla–camera axis and simultaneously measured the distance between gorilla and camera with a laser range finder, and then calculated body length as the product of distance and pixel length [Breuer et al., 2007]. Young silverbacks (YSB) are larger and more muscular than AF and start to develop a silver saddle and strong gluteal and nuchal muscles; however, their secondary sexual characteristics (e.g. silvering of saddle, development of sagittal crest) are not fully developed and this process of maturation takes several years. YSB in western gorillas become increasingly peripheral to a group and eventually leave to become solitary males [Parnell, 2002a; Robbins et al., 2004]. We therefore provide the earliest age at male emigration. Similar to other sexually dimorphic primate species [e.g. Altmann et al., 1981; Sigg et al., 1982; Watts, 1985], male gorillas are considered adult (ASB) with cessation of their growth in both body size and full development of secondary sexual characteristics (see details in Table I). Achievement of full body size in western gorillas reflects competitive ability to acquire females and we therefore also provide the earliest age when harems are formed. However, it should be noted that in the absence of morphological data on body size (which are difficult to obtain noninvasively) any comparison between gorilla species should be treated as preliminary and we propose ways that will help to make such comparisons. Photographic Assignment of Age Boundaries We used photographs (taken between 16th April 2004 and 16th August 2007) to improve the definition of boundaries between classes that did not show morphological discontinuity (INF/JUV, JUV/SAD, SAD/BB, BB/YSB, YSB/ASB). We assigned 201 photographs of 53 different gorillas (covering approximately all ages from 6 months (mo) to approximately 24 yr) to life-history classes described above (see Fig. 1 and Table I). We only used photographs of gorillas standing quadrupedal and perpendicular to the gorilla–camera axis to avoid effect of body posture on appearance of coloration [Breuer et al., 2007]. This assignment was done on the basis of external appearance using different morphological cues such as body proportions, muscle developments (gluteal and neck muscles) or the development of secondary sexual characters (arm hair, saddle coloration, sagittal crest). This assignment procedure was carried out independently by two of the authors Fig. 1. Photos showing side profiles of gorillas of different lifehistory classes. The two photos in each row present a typical example of the life-history classes used in this study (from top: infant (INF), juvenile (JUV), subadult (SAD), blackback (BB), young silverback (YSB) and adult female (AF)/adult silverback (ASB)). (T. B. and M. B.-N. H.). We compared our results with those of two independent experienced gorilla observers who were not familiar with the age of the study animals to verify that our assignment was not biased by knowledge of the identity and age of the gorillas. All judges were familiar with the criteria describing gorilla life-history classes and we found that definitions of life-history stages were equal among all four judges (Table I and Fig. 1). We calculated the boundaries between life-history classes using binary logistical regression, with life-history Am. J. Primatol. 114 / Breuer et al. class of one of two neighboring classes as the dependent variable and age as the covariate. Age boundaries were then calculated by solving the eaxþb following equation: y ¼ ð1þe axþb Þ where x is the age boundary and a and b are estimated by maximum likelihood using SPSS 13 for Windows (SPSS Inc., Chicago, IL). We set y 5 0.5 as the cut-off point when a gorilla should be assigned to the older class and round results to the nearest half year. We found no statistical difference between the assignments of the independent and the authors’ judgement, and thus took the average value of the age boundary sets of both results (Table II). Gorillas that were photographed multiple times generally showed high consistency in class assignment when photos were made within a short time interval. For those cases with a large interval between two photographs, we often assigned nonadult gorillas to a different category. Assignment of life-history classes by all four judges was very similar showing that it was generally easy to assign gorillas to different classes based solely on their external appearance (average k: K 5 0.658; range: 0.593–0.779, all Po0.001, n 5 201 photos; Spearman rank correlations: average: rS 5 0.939, range: 0.913–0.968, all Po0.001, n 5 192 photos not assigned as AF or AF/BB (sex of gorillas unknown)). Hereafter we use only assignments by T. B. and M. B.N. H. We present results of the INF/JUV, JUV/SAD, SAD/BB boundaries for gorillas for which we knew the year of birth (n 5 91 photos). Despite monitoring many immature females, we had only one female whose age we knew at first parturition, because most SAD and nulliparous females emigrated out of the study population (Mbeli Bai study, long-term data). Given the lack of data on accurate ages of AF, and the correspondingly small sample size, we could not apply logistic regression to define the age of the SAD/AF boundary, and the results on this particular age-class boundary should be treated with caution. Unless otherwise stated we present results as yr and mo to the nearest month. All research, protocols reported in this study were reviewed and approved by the Congolese Ministry of Forest Economy and Environment and the Nouabalé-Ndoki Project of the Wildlife Conservation Society. We also confirm that all research reported in this article adhered to the American Society of Primatologists Principles for the Ethical Treatment of Non-Human Primates and no animal handling was involved in the study. RESULTS The youngest immature that survived the dispersal or death of the mother was 4 yr old. There were three events in which a female transferred with her offspring following the death of the group’s silverback and the mothers (n 5 2; one mother transferred two times) remained with their offspring until these were 4 yr 11 mo and 5 yr 6 mo. Similarly, Am. J. Primatol. the youngest gorilla seen to transfer alone was 4 yr; he was also the youngest when last seen suckling. Immature gorillas were last seen to suckle at an average age of 4 yr 9 mo (n 5 25) (median: 4 yr 9 mo, range 3 yr 1 mo–6 yr 1 mo), which is significantly later than that for mountain gorillas (average: 3 yr 5 mo (n 5 11), median: 3 yr 7 mo, range 2 yr 8 mo–5 yr 2 mo) [Fletcher, 1994; Stewart, 1981] (U 5 37, z 5 3.452, P 5 0.001) [see also Nowell & Fletcher, 2007]. We assigned photos of gorillas up to a maximum age of 4 yr 3 mo to INF and the youngest gorilla we assigned as JUV was 4 yr old (Table II). The INF/JUV boundary was best set at 4 yr (summarized in Table III). Therefore, we propose an age boundary for INF/JUV in western gorillas of 4 yr. Boundaries to SAD were solely described by photo assignment. We found substantial overlap between the JUV and SAD classes for both judges (Table II). We determined a boundary of 7 yr 7 mo and proposed 7.5 yr as the JUV/SAD boundary in western gorillas (Table III). The female of known age was seen three times with labial swellings between 9 yr 6 mo and 10 yr 3 mo, which is 2 yr later than in mountain gorillas (7–7.5 yr) [Harcourt et al., 1980]. She had her first baby at 11 yr 5 mo. This age of first parturition falls within the upper range for mountain gorillas (average: 10 yr 3 mo, range 8 yr 8 mo–12 yr 10 mo) [Gerald, 1995]. Two females of known age did not have offspring when they transferred out of the population at the ages of 9 yr 3 mo and 9 yr 11 mo. On the basis of these field observations, we tentatively suggest the designation of the SAD/AF boundary as 10 yr. The youngest male to attain the approximate body length of an AF was 10 yr 8 mo old (Fig. 2). Photo assignment showed that there was almost no overlap between SAD and BB; thus, the boundary between the two classes was estimated to be 11 yr 7 mo (Table III). We therefore designate the SAD/BB boundary at an age of 11 yr. The minimum age (estimated retrospectively) of a BB was 10 yr 8 mo and the maximum was 14 yr 10 mo. Photographs of males ranging from 12 yr 2 mo to 18 yr 4 mo of age were assigned to the YSB class. We calculated a boundary of 14 yr 6 mo (Table III) between BB/YSB. The youngest male that was first seen making visits to Mbeli Bai without his former group had an estimated age of 13 yr 7 mo and we propose that YSB class starts at age 14 yr but also realize that there are large interindividual differences when males become silver. The youngest male classified as fully grown was estimated to be 17 yr 5 mo old. We estimated the YSB/ASB boundary as 18 yr 2 mo (Table III). Therefore, we propose that the ASB class begins at age 18 yr (compared with 15 yr in mountain gorillas) as this corresponds to the estimated age a male can acquire a female [Breuer, unpublished data]. Western Gorilla Maturation and Life History Classes / 115 TABLE III. Results From Logistic Regression of Photo Assignment to Reveal Age Boundaries Between Different Life-History Classes Judge Life-history boundary Estimated age of boundary Number of photos Variable B SE Wald df Sig. 87.764 336.107 13.421 54.946 2.327 17.458 2.014 15.430 58.578 652.110 3.116 37.838 166.724 6191.397 23921.980 7.454 30.835 0.754 5.909 0.623 4.993 5530.692 61604.160 1.466 17.421 4644.687 0.000 0.000 3.242 3.175 9.516 8.731 10.454 9.550 0.000 0.000 4.517 4.718 0.001 1 1 1 1 1 1 1 1 1 1 1 1 1 0.989 0.989 0.072 0.075 0.002 0.003 0.001 0.002 0.992 0.992 0.034 0.030 0.971 1 Infant/juvenile 3.8 46 2 Infant/juvenile 4.1 49 1 Juvenile/subadult 7.5 54 2 Juvenile/subadult 7.7 57 1 Subadult/blackback 11.1 36 2 Subadult/blackback 12.1 36 1 Blackback/young silverback 14.7 82 Age Constant Age Constant Age Constant Age Constant Age Constant Age Constant Age 2 Blackback/young silverback 14.4 75 Constant Age 2451.006 1.592 68335.566 0.360 0.001 19.581 1 1 0.971 0.000 1 Young/adult silverback 18.0 68 2 Young/adult silverback 18.3 69 Constant Age Constant Age Constant 22.871 3.364 60.703 2.596 47.586 5.179 1.251 22.562 0.853 15.565 19.503 7.237 7.239 9.264 9.347 1 1 1 1 1 0.000 0.007 0.007 0.002 0.002 Fig. 2. Body length growth of male western gorillas. The horizontal graded bar indicates the range of adult female body length (range: 72.3–74.8 cm) also measured by photogrammetry [Breuer et al., 2007]. Data points are from males with known birth dates and in the cases of gorillas older than 12 yr of known year of birth. The same individual can contribute multiple data points. DISCUSSION Reassigning Age Boundaries of Western Gorilla Life-History Classes Estimating age in free-ranging primates improves with observer experience and duration of the study, and age boundaries of life-history classes have often been re-assessed and refined when knowledge of the physical maturation of wild primates improved [Altmann et al., 1977, 1981; Sigg et al., 1982]. Here, we have revised the age boundaries of lifehistory classes in western gorillas using long-term demographic data from Mbeli Bai (Table I and Fig. 3). Therefore, we propose that these new age boundaries can be tested at other field studies using similar behavioral and morphological criteria. However, these boundaries should not always be considered as clear cut-off points between age classes but rather an estimated age around which a transition occurs (e.g. JUV/SAD, BB/YSB, etc.). It is possible that the development may be faster at sites that are more similar to the habitat of mountain gorillas (e.g. secondary forests with higher herb density). However, our site constitutes a large swampy clearing with superabundant aquatic herbs, and so perhaps already presents a representative assessment of life-history boundaries for western gorillas. Assigning Photographs to Different LifeHistory Classes Currently we have empirical data on individuals of known age ranging from 1 to 12.5 yr. Our procedure allowed us to assign age to gorillas older than 12.5 yr and we have used retrospective aging to assign an age boundary to silverbacks. In spite of practical difficulties in accurately assessing and comparing gorilla sizes owing to different distances of the gorillas from the observer, photo assignment showed interobserver reliability between judges familiar or unfamiliar with the identity and age of the study animals. This method can reliably be used Am. J. Primatol. 116 / Breuer et al. Fig. 3. Developmental stages (life-history classes) in the life cycle of mountain gorillas (MG) and western gorillas (WG). to assign gorillas of unknown ages to different lifehistory classes. However, when morphology changes gradually, the application of photogrammetry to measure body length can provide more precise estimates of age than other physical characteristics—body length is difficult to take into account when assigning photos to life-history classes. Such continuous monitoring of known-aged gorillas will also help identifying growth spurts and modes of development [e.g. Leigh & Bernstein, 2006]. Owing to the fact that some criteria (e.g. age when males reach AF size) for the different boundaries for mountain gorillas have never been tested, it would be important to apply photogrammetry and photo assignment to the Virunga gorillas (albeit this might be difficult owing to the dense vegetation), who have been monitored for several decades, to see how well such assignment fits with the currently used age boundaries in mountain gorillas. Also the application of video images might help make the classification of gorillas and other primates into different life stages easier. Such comparative studies of different gorilla populations would test our conclusions on the slower development of western gorillas. In addition, there is little consensus in the use of life-history classes in the well-studied mountain gorillas and some classes have been poorly defined. For example, although some consider all males over 12 yr of age to be adult or silverbacks [e.g. Robbins, 2007; Williamson & Gerald-Steklis, 2001], others make the distinction between YSB and mature silverbacks that are not fully grown until 15 yr of age [Watts, 1990; Watts & Pusey, 1993]. These caveats should be recognized in the light of our comparison with western gorillas and we urge future studies on both species to follow standardized age-class definitions such as that we have presented here to facilitate comparative analyses. Comparison Between Western and Mountain Gorillas The later weaning age in western gorillas compared with mountain gorillas is supported by an average increase of 16 mo in the duration of suckling. The results presented here and during an Am. J. Primatol. earlier investigation show that western gorilla INF are not weaned before the age of 4 yr, when termination of suckling bouts by the mother peaks [Nowell & Fletcher, 2007]. The INF/JUV boundary determined by our photo assignment was similar to the weaning age and the minimum age we observed a gorilla to survive the death of its mother. Although the cessation of suckling is a more obvious milestone that delimits a life-history class, we confirm that other boundaries, particularly during adolescence (e.g. JUV/SAD boundary), are more fluid [Setchell & Lee, 2004]. Correspondingly, JUV and SAD mountain gorillas have been pooled as adolescents for some data analyses [Watts & Pusey, 1993]. We therefore need more behavioral data to confirm our estimate of the JUV/SAD boundary that is currently based solely on the photo assignment. We assigned the age of the SAD/BB boundary to 11 yr and found that males attain AF size at around 11 yr of age. Similarly, males do not attain the size of AF until they are at least 10 yr old in Bwindi [Robbins, personal communication] where mountain gorillas consume more fruits than in the Virungas [Robbins, 2007]. Although the body length criterion remains to be tested for mountain gorillas, the development of secondary sexual characters (e.g. longer arm hairs of males) is not obvious before the age of 11 yr in western gorillas. This event is assumed to happen much earlier in life in mountain gorillas (Table I). The slower maturation in known-aged males up to the BB age suggests that this likely leads to a later age of growth cessation in western gorilla silverbacks compared with mountain gorillas. Males become solitary when they are considered YSB and appear not to be fully grown until the age of approximately 18 yr when they are able to acquire females, compared with mountain gorillas that are considered fully grown at 15–16 yr [Watts, 1990]. Also gorillas in Bwindi Impenetrable National Park, Uganda, appear to develop more slowly than mountain gorillas monitored in the Virunga Volcanoes [Robbins, personal communication]. Continuous monitoring is needed to assess the accuracy of this age boundary for ASB. Our limited data on age at parturition of AF and age of visible sexual swellings suggest a later age at parturition (although it is possible that we may Western Gorilla Maturation and Life History Classes / 117 have missed the first appearance of these small sexual swellings and a miscarriage owing to the observation gaps of groups). However, more data are needed from SAD and AF of known age in order to confirm the age boundary of 10 yr proposed here. Implications for Life-History Theory, Social Organization and Conservation Our findings provide support for the ‘‘risk-aversion’’ hypothesis and the prediction of slower development of western gorillas owing to greater frugivory, stronger seasonality in the habitat, lower herb density or the rarity of weaning foods [Doran & McNeilage, 2001; Nowell & Fletcher, 2008]. Although slower immature growth and later weaning age do not necessarily lead to later age at parturition or age at maturity (owing to different modes of life histories) [Leigh & Bernstein, 2006], our data indicate that this may be the case in our population. Other aspects of western gorilla biology such as arboreality, large daily ranges [Doran-Sheehy et al., 2004; Remis, 1995] and increased foraging complexity (including cognitive skills for locating ripe fruits) can potentially reduce the allocation of energy to physical maturation [van Schaik & Deaner, 2003; Walker et al., 2006; Zihlman et al., 2007]. Detailed studies on energy gains and overall energy balance are currently under way that will help to explicitly test these predictions [Masi, unpublished manuscript]. In addition, primates that face increased predation risk are assumed to grow faster because smaller individuals are considered at higher risk [Janson & van Schaik, 1993]. In contrast to mountain gorillas, western gorillas face leopard predation risks but the exact degree is unknown [Robbins et al., 2004]. Current life history of mountain gorillas could also reflect adaptation to predation pressures in the past so that we were not able to test whether western gorilla life history has evolved under increasing predation risk. A slower life history and longer period of dependency of immature western gorillas could have important consequences for other aspects of western gorilla biology. A minimum tenure of 18 yr is required for the son of the group’s silverback (who will then be around 36 yr) to reach maturity. Given high levels of male–male competition and the subsequent impacts on male longevity and tenure length, slower life history will impact on the probability of father–son multimale group forming. If male tenure length is shorter than a male’s age to mature, age-graded groups are unlikely to develop. This scenario could provide an alternative explanation for the lack of multimale (kin) groups in western gorillas compared with mountain gorillas [see alternative explanation in Harcourt & Stewart, 2007]. The later weaning age (higher ratio of lactation to gestation) and the predominance of one-male groups in western gorillas could signal increased infanticide risk because INF in multimale mountain gorilla groups face lower risks of being killed by a silverback than do one-male groups [Robbins et al., 2007]. Infanticide and predation risk (and other factors such as fallen from trees) can cause the observed high INF mortality rates [more than 50% to weaning age: Breuer, unpublished results; Robbins et al., 2004] of western gorillas at Mbeli Bai. Recently, western gorillas have been re-classified from endangered to critically endangered on the IUCN Red List, in response to the escalating rates of decline owing to Ebola and commercial hunting across much of their range in the last two decades [Tutin et al., 2005]. Slower development and the potential for higher mortality compared with mountain gorillas will negatively affect their intrinsic rate of increase and their potential for recovery from population crashes. These are therefore important variables to incorporate into models of population dynamics and species-level conservation strategies. This study has provided insights into the potential implications of slower life history for western gorillas, emphasizing the importance of long-term studies in providing accurate baseline demographic and life-history data of undisturbed primate populations in assessing the vulnerability of populations to these threats. 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