American Journal of Primatology 70:1–14 (2008) RESEARCH ARTICLE Physical Maturation, Life-History Classes and Age Estimates of Free-Ranging Western Gorillas—Insights From Mbeli Bai, Republic of Congo THOMAS BREUER 1,2 , MIREILLE BREUER-NDOUNDOU HOCKEMBA 2 , CLAUDIA OLEJNICZAK 3 , RICHARD J. PARNELL 4 , AND EMMA J. STOKES 4 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 Nouabale ´-Ndoki National Park in northern Congo. We assign photographs of known individuals to different life-history classes and propose new age boundaries for life- history 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. 70:1–15, 2008. 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 food- provisioned 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 [Jan- son & van Schaik, 1993]. Hence this ‘‘risk-aversion’’ hypothesis assumes that feeding on seasonally avail- able resources, such as ripe fruit, will result in prolonged periods of JUV maturation, and feeding 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 Published online in Wiley InterScience (www.interscience. wiley.com). DOI 10.1002/ajp.20628 Received 18 March 2008; revised 15 September 2008; revision accepted 17 September 2008 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 Congo- PROGEAP; Louis Leakey Foundation; Wenner-Gren Founda- tion; German Academic Exchange Service (DAAD); Max Planck Society. Correspondence to: Thomas Breuer, Department of Primatol- ogy, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany. E-mail: [email protected]r r 2008 Wiley-Liss, Inc.
Transcript
American Journal of Primatology 70:1–14 (2008)
RESEARCH ARTICLE
Physical Maturation, Life-History Classes and Age Estimates of Free-RangingWestern Gorillas—Insights From Mbeli Bai, Republic of Congo
THOMAS BREUER1,2�, MIREILLE BREUER-NDOUNDOU HOCKEMBA2, CLAUDIA OLEJNICZAK3,RICHARD J. PARNELL4, AND EMMA J. STOKES4
1Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany2Mbeli Bai Study, Wildlife Conservation Society—Congo Program, Brazzaville, Republic of Congo3Department of Anthropology, Washington University, St. Louis, Missouri4Wildlife Conservation Society, Bronx, New York
Physical maturation and life-history parameters are seen as evolutionary adaptations to differentecological and social conditions. Comparison of life-history patterns of closely related species living indiverse 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 investigationinto the role of increased frugivory in shaping western gorilla life histories. We present behavioral andmorphological data on western gorilla physical maturation and life-history parameters from a 12.5-yearstudy at Mbeli Bai, a forest clearing in the Nouabale-Ndoki National Park in northern Congo. We assignphotographs of known individuals to different life-history classes and propose new age boundaries for life-history 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 andindicate slower physical maturation of immatures. These findings support the risk-aversion hypothesisfor more frugivorous species. However, our methods need to be applied and tested with other gorillapopulations. 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 thiscritically endangered species. We emphasize that long-term studies can provide crucial demographic andlife-history data that improve our understanding of life-history evolution and adaptation and help torefine conservation strategies. Am. J. Primatol. 70:1–15, 2008. 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 areassumed to be the result of evolutionary adaptationsto various socioecological factors and are shaped bydifferences in substrate use, body or brain size anddiet [e.g. Kappeler & Pereira, 2003; Leigh, 1994a,2004; Ross & Jones, 1999; van Schaik & Deaner, 2003;Walker et al., 2006]. Nutrition is an obvious factoraffecting primate life-history pace. For example, ratesof maturation and reproduction of wild animals areconsiderably slower than those of animals under food-provisioned conditions [e.g. Altmann & Alberts, 2005;Leigh, 1994b; Sigg et al., 1982; Strum, 1991; Zihlmanet al., 2007]. Spreading the metabolic needs forjuvenile (JUV) maturation over a longer period(growth at a slow rate) in environments with poorerand unstable or unpredictable food availability willhelp to reduce the risks of starvation, primarilyresulting from intraspecific feeding competition [Jan-son & van Schaik, 1993]. Hence this ‘‘risk-aversion’’hypothesis assumes that feeding on seasonally avail-able resources, such as ripe fruit, will result inprolonged periods of JUV maturation, and feeding
on leaves that are assumed to be an abundant andpredictable resource is expected to speed up thelife-history pace of primates.
Empirical evidence for the risk-aversion hypothesishas been equivocal [Leigh, 1994a; Ross & Jones, 1999;Wich et al., 2004, 2007]. For example, Leigh [1994a]demonstrated that more folivorous anthropoid primates
Published online in Wiley InterScience (www.interscience.wiley.com).
DOI 10.1002/ajp.20628
Received 18 March 2008; revised 15 September 2008; revisionaccepted 17 September 2008
Contract grant sponsors: Brevard Zoo; Chicago ZoologicalSociety; Columbus Zoo and Aquarium; Cincinnati Zoo andBotanical Garden; Sea World and Busch Gardens ConservationFund; Toronto Zoo; Wildlife Conservation Society; WoodlandPark Zoo; Little Rock Zoo; Lincoln Park Zoo; Zoological Societyof Milwaukee County Global Environmental Facility Congo-PROGEAP; Louis Leakey Foundation; Wenner-Gren Founda-tion; German Academic Exchange Service (DAAD); Max PlanckSociety.
�Correspondence to: Thomas Breuer, Department of Primatol-ogy, Max Planck Institute for Evolutionary Anthropology,Deutscher Platz 6, D-04103 Leipzig, Germany.E-mail: [email protected]
rr 2008 Wiley-Liss, Inc.
have rapid growth rates in the earlier stages of ontogenyand cease growth earlier than nonfolivorous species andpostulated a relationship between life-history pace anddigestive system. Similarly, Godfrey et al. [2003] foundthat folivorous primate species exhibit faster dentaldevelopment. In contrast the risk-aversion hypothesisdoes not predict patterns of ontogenetic diversity insmall-bodied New World monkeys [Garber & Leigh,1997] and folivorous indriids mature more slowly thanlike-sized frugivorous lemurids [Godfrey et al., 2004].Most of our knowledge about primate life-historyevolution has been gained through broad-scale inter-specific 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 agiven species also vary according to the ecologicalconditions (phenotypic plasticity) [Lee & Kappeler,2003]. Therefore, comparisons of closely related speciesor populations living in different environments wouldhelp to clarify the role of ecological factors in shapinglife-history parameters. However, with a few exceptions[e.g. Altmann & Alberts, 2005; Barrett et al., 2006;Borries et al., 2001], empirical data from closelyrelated species or populations of the same species aremissing. In this study we provide life-history data onwestern gorillas (Gorilla gorilla) in order to investigatewhether increased frugivory can lead to differences inlife-history pace between closely related species within asingle genus.
Great apes mature slowly and have long life spans,making it difficult to obtain life-history data from wildpopulations [Knott, 2001] as most ape studies are tooshort to cover all stages of the life cycle. Long-termstudies are therefore needed to provide detailed apelife-history data for addressing such evolutionary andecological questions. Furthermore, population para-meters and life-history data have important conserva-tion implications in the light of the crisis now facinggreat apes [Tutin et al., 2005].
Gorillas are the largest living primates andthey are primarily herbivores [Doran-Sheehy et al.,2006; Robbins, 2007; Rogers et al., 2004]. Accord-ing to the risk-aversion model, they are assumed tomature much faster than other, more frugivorousapes and an ontogenetic analysis of captive Africanapes supports this assumption [Leigh & Shea,1996]. Moreover, comparison of some life-historyparameters with free-ranging chimpanzees (Pantroglodytes) and orangutans (Pongo spp.) supportsthe hypothesis of faster maturation of species witha more folivorous diet [Hill et al., 2001; Knott,2001; Wich et al., 2004]. Our current knowledgeabout gorilla life-history patterns comes predomi-nantly from one high-altitude mountain gorillapopulation and long-term study site (KarisokeResearch Center) located at the extreme range ofgorilla distribution in the Virunga Volcanoes[summarized in Robbins, 2007]—with preliminarydata available on Grauer’s gorillas [Yamagiwa &
Kahekwa, 2001]. However, western gorilla habitatdiffers from that of mountain gorillas: in lowlandforests terrestrial herbaceous vegetation occurs atlower densities and is more patchily distributed[e.g. Rogers et al., 2004]. Western gorillas are morefrugivorous than mountain gorillas with fruitingtrees being more abundant but showing largeseasonal variation in fruit availability [Masi,2007; Rogers et al., 2004]. Differences in resourceavailability combined with reduced folivory couldhave direct effects on western gorilla developmentleading to slower life histories [Doran & McNei-lage, 2001] and particularly to a later weaning age.
If such differences in life-history patterns be-tween western and mountain gorillas occur, then ageboundaries delimiting life-history classes (infants(INF), juvenile (JUV), subadults (SAD), adults) shouldconsequently differ between the two gorilla species.However, western gorilla researchers have typicallyadopted age boundaries from mountain gorillas(see Table I). This is simply owing to a lack of long-term field studies spanning a full generation meaningthat previous studies of western gorillas could onlyaccurately age immature gorillas that had been seensince birth, e.g. those of 1–2 years (yr) (or gorillas of upto 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 gorillastudies, researchers aged wild gorillas by makingcomparisons with captive individuals, potentially lea-ding to an underestimation of true age. Long-termdemographic data on known individuals provide theages associated with external and behavioral criteriathat demark the boundaries of life-history classes [e.g.Altmann et al., 1981].
Here, we investigate whether the physicalmaturation of western gorillas supports the risk-aversion hypothesis and is slower than that ofmountain gorillas. Secondly, we aim to assign theage boundaries for western gorilla life-historyclasses, which have previously been impossible toaccurately define owing to the lack of long-termstudies, and introduce techniques that will help tocompare physical maturation between differentgorilla populations. Finally, we discuss the implica-tions of our findings for the social structure,population growth and conservation of westernlowland gorillas.
METHODS
Observations were made at Mbeli Bai, a 12.9 halarge swampy clearing (‘‘bai’’ in the local language)in the Nouabale-Ndoki National Park, Republic ofCongo [see also Parnell, 2002a; Stokes et al., 2003].This pristine protected area has never been loggedand no illegal human activities have been recorded inthe study area since the start of the Mbeli Bai studyin 1995 (following pilot studies in 1993 and 1994). We
Western Gorilla Maturation and Life History Classes / 3
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Am. J. Primatol.
Western Gorilla Maturation and Life History Classes / 5
collected data during nearly continuous monitoringby four principal investigators and assistants fromFebruary 1995 until July 2007 on 303 differentgorillas living in 61 social units (groups or solitarymales). We made observations with 15–45� tele-scopes from a platform overlooking the clearing.Gorillas were habituated to the presence of observerson the platform and were individually identified fromfeatures such as size, pelage, shape of ears and browridge and nose prints [Parnell, 2002b]. One advan-tage of studying gorillas at forest clearings lies in theaccumulation of demographic and life-history data ofmany different gorilla groups compared with onlyone or two groups followed in the forest. Limitationsof bai studies include the gaps between visits ofcertain gorilla groups, which may in some cases spanseveral months. These observational gaps can limitthe accurate assessment of developmental processes,exact birth dates, and hinder our ability to distin-guish ‘‘death’’ vs. ‘‘dispersal’’ away from the popula-tion in individuals that disappear from a group.However, it was often possible to limit the error inbirth date estimates to just a few weeks (see below).Of the 303 gorillas monitored, 59 were parousfemales and 32 were adult males (silverbacks) whenfirst observed (parous females and adult silverbacks(ASB) not considered in this study), whereas 110offspring were born during the study. The remaining102 gorillas were not fully adult when observed forthe first time, and their birth date was estimatedaccording to the procedure outlined below.
Age Estimation
Given the long period of immaturity in gorillas, astudy duration of 12.5 yr is too short to trackindividuals longitudinally from birth to adulthood,and to provide exact ages for mature gorillas. Wetherefore used a combination of (1) the assignment ofa reliable birth date based on observations of the firstappearance of a newborn to a known female(n 5 110), or the first sighting of a newborn in apreviously unknown group (carried ventrally, pinkcoloration; n 5 9), and (2) retrospective assignmentof age to immatures of unknown birth date bycomparing their physical maturation with indivi-duals of known age. For INF born during the study,age was estimated based on morphology and size ofthe INF, their behavior and that of their mother atfirst observation of the newborn [Nowell, 2005;Nowell & Fletcher, 2007; Parnell, 2002b]. Wecompiled a good record of the physical maturationand behavior of INF of known age and couldtherefore improve the precision of estimated birthdates, even for groups that were absent from theclearing for several months. In the second case, wedid not have accurate records of age, because theimmature gorillas were either born before the studybegan or transferred into the population. We therefore
assigned a birth date retrospectively using bothexternal morphology (e.g. body size, hair color, bodyproportions) and behavior (e.g. suckling behavior,proximity to and dependence on the mother) comparedwith gorillas of known age. This was not possible in thefirst 5 yr of the study, because we did not have anygorillas of known birth date for comparison. Wetherefore retrospectively aged all nonadult gorillas(n 5 93), identified both at the start of the study andthose that immigrated into the population, usingsupplementary data (e.g. field notes on physicalmaturation, photographs, 4200 hr of video footage).Retrospective classification will produce a degree oferror in age estimates owing to individual variation,and certain biological questions such as age at firstparturition can only be answered with data fromgorillas of known birth date. However, we argue that,given the objective of dividing a continuum of devel-opment into biologically meaningful classes, ourmethodology for assigning age boundaries to life-history classes is justified.
Life-History Classes and Their Age Boundaries
To define the boundaries of life-history classeswe first used morphological and behavioral criteriaand also assigned photographs of known individualsto the different classes (see below). Some classboundaries are easier to recognize in some animalsthan in others and there is much variation betweenindividuals [e.g. Strum, 1991]. Our definition of life-history classes follows Setchell and Lee [2004] andhas been adopted by various primatologists for anumber of different species. We did not distinguishbetween males and females before females wereconsidered adult (the blackback/female separation)(BB/AF) (Table II) because determining the sex ofgorillas at Mbeli Bai is almost impossible oncegorillas are no longer riding dorsal on the mother.
The developmental stages of wild western gorillashave been assumed to mirror that of mountain gorillas[Nowell, 2005] and our criteria represent a summary ofprevious definitions of life-history classes and themorphological and behavioral markers used in differentgorilla studies (Table I). Infancy ends when an animalcan survive maternal death. Although there are largeindividual differences (see ‘‘Results’’), the INF/JUVtransition is best described by life-history parameters,such as lactational weaning, which can be identified byfield observations. Between November 2002 and July2007 we noted every suckling event and assignedweaning age as the mid-point of visits before and aftersuckling termination [see also Nowell & Fletcher,2007]. We furthermore provide information on theminimum age of survival after the disappearance of amother and the minimum age of dispersal. The JUVperiod ends when puberty (SAD class) starts; however,that is difficult to determine without hormonal dataunless external signs, such as sexual swelling in
females (albeit small in gorillas) or ejaculation ofsemen in males, can be observed [Setchell & Lee,2004]. Puberty is considered to have ended once anindividual attains reproductive competence. Inmountain gorillas, nulliparous females go through a2-yr period of adolescent sterility [Harcourt et al.,1980]. Thus the AF class used for mountaingorillas includes nulliparous females because firstparturition occurs at a median age of 10 yr (range8.7–12.8) [Harcourt et al., 1981; Watts, 1991]. Forfemale gorillas born during our study, we noted whenwe first saw the small labial swellings and age at first
birth, to determine the boundary between SAD/AFaccordingly.
Delayed male maturation is the result of sexualdimorphism in gorillas [Leigh & Shea, 1995]. There-fore, gorilla researchers define additional classes formales that are fertile but are not yet fully grown. Wedefined the SAD/BB boundary as the same cut-offpoint as for SAD/AF. To support this assignment, wealso determined when males reached approximatelythe body length of an AF, which is one criterion forBB classification [Schaller, 1963]; however, thiscriteria from the early years at Karisoke has never
TABLE II. Mean Estimated Ages of Western Gorillas That Were Assigned, Using 201 Photographs, to DifferentLife-History Stages by Two Judges
Judge
Knownyear ofbirth
Life-historyclass
assigned
Numberof
differentgorillas
Samplesize(] of
photos)
Mean age (yr)of gorillas
assigned tolife-history
class
Standarderror(yr)
Minimum age(yr) of gorillas
assigned to life-history class
Maximum age(yr) of gorillas
assigned to life-history class
P-values ofMann–Whitney U-test of differencesbetween judgesa
1 No Juvenile 1 1 6.5 – 6.5 6.5 –2 No Juvenile 2 3 7.5 0.3 7.1 8.01 No Subadult 4 10 9.7 0.5 7.1 10.9 0.6592 No Subadult 4 13 10.4 0.3 6.5 11.51 No Blackback 10 34 11.8 0.2 10.7 14.6 0.2182 No Blackback 11 28 12.1 0.2 10.7 14.81 No Young
silverback6 23 16.2 0.2 14.8 18.2 0.382
2 No Youngsilverback
7 33 16.4 0.3 12.2 18.3
1 No Adultsilverback
6 42 20.0 0.3 17.4 23.6 0.159
2 No Adultsilverback
5 33 20.7 0.3 17.6 23.6
Photos were assigned according to external appearance of examples given in Figure 1 and morphological markers described in Table I and correspondinglynumber of gorillas assigned to life-history classes varied between two judges. P-values indicate if there were any significant differences between judges intheir 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 thestudy.aMann–Whitney U (MWU) exact test only applied when sample size was larger than three.
Am. J. Primatol.
Western Gorilla Maturation and Life History Classes / 7
been properly tested and others have grouped JUVand SAD into an old JUV class [Watts & Pusey,1993]. We used digital photogrammetry to measurethe body length of nonadult males and fully grownfemale gorillas [Breuer et al., 2007]. BetweenJanuary 2004 and July 2007 we took digital photo-graphs of gorillas standing perpendicular to thegorilla–camera axis and simultaneously measuredthe distance between gorilla and camera with a laserrange finder, and then calculated body length as theproduct of distance and pixel length [Breuer et al.,2007]. Young silverbacks (YSB) are larger and moremuscular than AF and start to develop a silver saddleand strong gluteal and nuchal muscles; however,their secondary sexual characteristics (e.g. silveringof saddle, development of sagittal crest) are not fullydeveloped and this process of maturation takesseveral years. YSB in western gorillas becomeincreasingly peripheral to a group and eventuallyleave to become solitary males [Parnell, 2002a;Robbins et al., 2004]. We therefore provide theearliest age at male emigration. Similar to othersexually dimorphic primate species [e.g. Altmannet al., 1981; Sigg et al., 1982; Watts, 1985], malegorillas are considered adult (ASB) with cessation oftheir growth in both body size and full developmentof secondary sexual characteristics (see details inTable I). Achievement of full body size in westerngorillas reflects competitive ability to acquire femalesand we therefore also provide the earliest age whenharems are formed.
However, it should be noted that in the absenceof morphological data on body size (which aredifficult to obtain noninvasively) any comparisonbetween gorilla species should be treated as pre-liminary and we propose ways that will help to makesuch comparisons.
Photographic Assignment of Age Boundaries
We used photographs (taken between 16th April2004 and 16th August 2007) to improve the defini-tion of boundaries between classes that did not showmorphological discontinuity (INF/JUV, JUV/SAD,SAD/BB, BB/YSB, YSB/ASB). We assigned 201photographs of 53 different gorillas (covering ap-proximately all ages from 6 months (mo) to approxi-mately 24 yr) to life-history classes described above(see Fig. 1 and Table I). We only used photographs ofgorillas standing quadrupedal and perpendicular tothe gorilla–camera axis to avoid effect of bodyposture on appearance of coloration [Breuer et al.,2007]. This assignment was done on the basis ofexternal appearance using different morphologicalcues such as body proportions, muscle developments(gluteal and neck muscles) or the development ofsecondary sexual characters (arm hair, saddle colora-tion, sagittal crest). This assignment procedure wascarried out independently by two of the authors
(T. B. and M. B.-N. H.). We compared our resultswith those of two independent experienced gorillaobservers who were not familiar with the age of thestudy animals to verify that our assignment was notbiased by knowledge of the identity and age of thegorillas. All judges were familiar with the criteriadescribing gorilla life-history classes and we foundthat definitions of life-history stages were equalamong all four judges (Table I and Fig. 1). Wecalculated the boundaries between life-history classesusing binary logistical regression, with life-history
Fig. 1. Photos showing side profiles of gorillas of different life-history classes. The two photos in each row present a typicalexample 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)).
class of one of two neighboring classes as thedependent variable and age as the covariate. Ageboundaries were then calculated by solving thefollowing equation: y ¼ eaxþb
ð1þeaxþbÞwhere x is the age
boundary and a and b are estimated by maximumlikelihood using SPSS 13 for Windows (SPSS Inc.,Chicago, IL). We set y 5 0.5 as the cut-off point when agorilla should be assigned to the older class and roundresults to the nearest half year.
We found no statistical difference between theassignments of the independent and the authors’judgement, and thus took the average value of the ageboundary sets of both results (Table II). Gorillas thatwere photographed multiple times generally showedhigh consistency in class assignment when photoswere made within a short time interval. For thosecases with a large interval between two photographs,we often assigned nonadult gorillas to a differentcategory. Assignment of life-history classes by all fourjudges was very similar showing that it was generallyeasy to assign gorillas to different classes based solelyon 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 notassigned 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 knewthe year of birth (n 5 91 photos). Despite monitoringmany immature females, we had only one femalewhose age we knew at first parturition, because mostSAD and nulliparous females emigrated out of thestudy population (Mbeli Bai study, long-term data).Given the lack of data on accurate ages of AF, and thecorrespondingly small sample size, we could not applylogistic regression to define the age of the SAD/AFboundary, and the results on this particular age-classboundary should be treated with caution.
Unless otherwise stated we present results as yrand mo to the nearest month. All research, protocolsreported in this study were reviewed and approvedby the Congolese Ministry of Forest Economy andEnvironment and the Nouabale-Ndoki Project of theWildlife Conservation Society. We also confirm thatall research reported in this article adhered to theAmerican Society of Primatologists Principles for theEthical Treatment of Non-Human Primates and noanimal handling was involved in the study.
RESULTS
The youngest immature that survived the dis-persal or death of the mother was 4 yr old. Therewere three events in which a female transferred withher offspring following the death of the group’ssilverback and the mothers (n 5 2; one mothertransferred two times) remained with their offspringuntil these were 4 yr 11 mo and 5 yr 6 mo. Similarly,
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 anaverage 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 significantlylater than that for mountain gorillas (average: 3 yr5 mo (n 5 11), median: 3 yr 7 mo, range 2 yr 8 mo–5 yr2 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 amaximum age of 4 yr 3 mo to INF and theyoungest gorilla we assigned as JUV was 4 yr old(Table II). The INF/JUV boundary was best set at4 yr (summarized in Table III). Therefore, wepropose an age boundary for INF/JUV in westerngorillas of 4 yr.
Boundaries to SAD were solely described byphoto assignment. We found substantial overlapbetween the JUV and SAD classes for both judges(Table II). We determined a boundary of 7 yr 7 moand proposed 7.5 yr as the JUV/SAD boundary inwestern gorillas (Table III). The female of known agewas seen three times with labial swellings between9 yr 6 mo and 10 yr 3 mo, which is 2 yr later than inmountain gorillas (7–7.5 yr) [Harcourt et al., 1980].She had her first baby at 11 yr 5 mo. This age of firstparturition falls within the upper range for moun-tain gorillas (average: 10 yr 3 mo, range 8 yr8 mo–12 yr 10 mo) [Gerald, 1995]. Two females ofknown age did not have offspring when theytransferred out of the population at the ages of 9 yr3 mo and 9 yr 11 mo. On the basis of these fieldobservations, we tentatively suggest the designationof the SAD/AF boundary as 10 yr.
The youngest male to attain the approximatebody length of an AF was 10 yr 8 mo old (Fig. 2).Photo assignment showed that there was almost nooverlap between SAD and BB; thus, the boundarybetween the two classes was estimated to be 11 yr7 mo (Table III). We therefore designate the SAD/BBboundary at an age of 11 yr.
The minimum age (estimated retrospectively) ofa BB was 10 yr 8 mo and the maximum was 14 yr10 mo. Photographs of males ranging from 12 yr 2 moto 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 wasfirst seen making visits to Mbeli Bai without hisformer group had an estimated age of 13 yr 7 moand we propose that YSB class starts at age 14 yr butalso realize that there are large interindividualdifferences when males become silver. The youngestmale classified as fully grown was estimated to be17 yr 5 mo old. We estimated the YSB/ASB boundaryas 18 yr 2 mo (Table III). Therefore, we propose thatthe ASB class begins at age 18 yr (compared with15 yr in mountain gorillas) as this corresponds to theestimated age a male can acquire a female [Breuer,unpublished data].
Am. J. Primatol.
Western Gorilla Maturation and Life History Classes / 9
Reassigning Age Boundaries of WesternGorilla Life-History Classes
Estimating age in free-ranging primates im-proves with observer experience and duration of thestudy, and age boundaries of life-history classes haveoften been re-assessed and refined when knowledgeof the physical maturation of wild primates improved[Altmann et al., 1977, 1981; Sigg et al., 1982].Here, we have revised the age boundaries of life-history classes in western gorillas using long-term
demographic data from Mbeli Bai (Table I and Fig.3). Therefore, we propose that these new ageboundaries can be tested at other field studies usingsimilar behavioral and morphological criteria. How-ever, these boundaries should not always be con-sidered as clear cut-off points between age classesbut rather an estimated age around which a transi-tion occurs (e.g. JUV/SAD, BB/YSB, etc.). It ispossible that the development may be faster at sitesthat are more similar to the habitat of mountaingorillas (e.g. secondary forests with higher herbdensity). However, our site constitutes a largeswampy clearing with superabundant aquatic herbs,and so perhaps already presents a representativeassessment of life-history boundaries for westerngorillas.
Assigning Photographs to Different Life-History Classes
Currently we have empirical data on individualsof known age ranging from 1 to 12.5 yr. Ourprocedure allowed us to assign age to gorillas olderthan 12.5 yr and we have used retrospective aging toassign an age boundary to silverbacks. In spite ofpractical difficulties in accurately assessing andcomparing gorilla sizes owing to different distancesof the gorillas from the observer, photo assignmentshowed interobserver reliability between judgesfamiliar or unfamiliar with the identity and age ofthe study animals. This method can reliably be used
Fig. 2. Body length growth of male western gorillas. Thehorizontal graded bar indicates the range of adult female bodylength (range: 72.3–74.8 cm) also measured by photogrammetry[Breuer et al., 2007]. Data points are from males with knownbirth dates and in the cases of gorillas older than 12 yr of knownyear of birth. The same individual can contribute multiple datapoints.
TABLE III. Results From Logistic Regression of Photo Assignment to Reveal Age Boundaries Between DifferentLife-History Classes
to assign gorillas of unknown ages to different life-history classes. However, when morphology changesgradually, the application of photogrammetry tomeasure body length can provide more preciseestimates of age than other physical characteris-tics—body length is difficult to take into accountwhen assigning photos to life-history classes. Suchcontinuous monitoring of known-aged gorillas willalso help identifying growth spurts and modes ofdevelopment [e.g. Leigh & Bernstein, 2006].
Owing to the fact that some criteria (e.g. agewhen males reach AF size) for the different bound-aries for mountain gorillas have never been tested, itwould be important to apply photogrammetry andphoto assignment to the Virunga gorillas (albeit thismight be difficult owing to the dense vegetation),who have been monitored for several decades, to seehow well such assignment fits with the currentlyused age boundaries in mountain gorillas. Also theapplication of video images might help make theclassification of gorillas and other primates intodifferent life stages easier. Such comparative studiesof different gorilla populations would test ourconclusions on the slower development of westerngorillas. In addition, there is little consensus in theuse of life-history classes in the well-studied moun-tain gorillas and some classes have been poorlydefined. For example, although some consider allmales over 12 yr of age to be adult or silverbacks [e.g.Robbins, 2007; Williamson & Gerald-Steklis, 2001],others make the distinction between YSB andmature silverbacks that are not fully grown until15 yr of age [Watts, 1990; Watts & Pusey, 1993].These caveats should be recognized in the light ofour comparison with western gorillas and we urgefuture studies on both species to follow standardizedage-class definitions such as that we have presentedhere to facilitate comparative analyses.
Comparison Between Western and MountainGorillas
The later weaning age in western gorillascompared with mountain gorillas is supported byan average increase of 16 mo in the duration ofsuckling. The results presented here and during an
earlier investigation show that western gorilla INFare not weaned before the age of 4 yr, whentermination of suckling bouts by the mother peaks[Nowell & Fletcher, 2007]. The INF/JUV boundarydetermined by our photo assignment was similar tothe weaning age and the minimum age we observed agorilla to survive the death of its mother. Althoughthe cessation of suckling is a more obvious milestonethat delimits a life-history class, we confirm thatother boundaries, particularly during adolescence(e.g. JUV/SAD boundary), are more fluid [Setchell &Lee, 2004]. Correspondingly, JUV and SAD moun-tain gorillas have been pooled as adolescents forsome data analyses [Watts & Pusey, 1993]. Wetherefore need more behavioral data to confirm ourestimate of the JUV/SAD boundary that is currentlybased solely on the photo assignment. We assignedthe age of the SAD/BB boundary to 11 yr and foundthat males attain AF size at around 11 yr of age.Similarly, males do not attain the size of AF untilthey are at least 10 yr old in Bwindi [Robbins,personal communication] where mountain gorillasconsume more fruits than in the Virungas [Robbins,2007]. Although the body length criterion remains tobe tested for mountain gorillas, the development ofsecondary sexual characters (e.g. longer arm hairs ofmales) is not obvious before the age of 11 yr inwestern gorillas. This event is assumed to happenmuch earlier in life in mountain gorillas (Table I).The slower maturation in known-aged males up tothe BB age suggests that this likely leads to a laterage of growth cessation in western gorilla silverbackscompared with mountain gorillas. Males becomesolitary when they are considered YSB and appearnot to be fully grown until the age of approximately18 yr when they are able to acquire females,compared with mountain gorillas that are consideredfully grown at 15–16 yr [Watts, 1990]. Also gorillas inBwindi Impenetrable National Park, Uganda, appearto develop more slowly than mountain gorillasmonitored in the Virunga Volcanoes [Robbins, per-sonal communication]. Continuous monitoring isneeded to assess the accuracy of this age boundaryfor ASB. Our limited data on age at parturition of AFand age of visible sexual swellings suggest a later ageat parturition (although it is possible that we may
Fig. 3. Developmental stages (life-history classes) in the life cycle of mountain gorillas (MG) and western gorillas (WG).
Am. J. Primatol.
Western Gorilla Maturation and Life History Classes / 11
have missed the first appearance of these smallsexual swellings and a miscarriage owing to theobservation gaps of groups). However, more data areneeded from SAD and AF of known age in order toconfirm the age boundary of 10 yr proposed here.
Implications for Life-History Theory, SocialOrganization and Conservation
Our findings provide support for the ‘‘risk-aver-sion’’ hypothesis and the prediction of slower develop-ment of western gorillas owing to greater frugivory,stronger seasonality in the habitat, lower herb densityor the rarity of weaning foods [Doran & McNeilage,2001; Nowell & Fletcher, 2008]. Although slowerimmature growth and later weaning age do notnecessarily lead to later age at parturition or age atmaturity (owing to different modes of life histories)[Leigh & Bernstein, 2006], our data indicate that thismay be the case in our population. Other aspects ofwestern gorilla biology such as arboreality, large dailyranges [Doran-Sheehy et al., 2004; Remis, 1995] andincreased foraging complexity (including cognitiveskills for locating ripe fruits) can potentially reducethe allocation of energy to physical maturation [vanSchaik & Deaner, 2003; Walker et al., 2006; Zihlmanet al., 2007]. Detailed studies on energy gains andoverall energy balance are currently under way thatwill help to explicitly test these predictions [Masi,unpublished manuscript].
In addition, primates that face increased preda-tion risk are assumed to grow faster because smallerindividuals are considered at higher risk [Janson &van Schaik, 1993]. In contrast to mountain gorillas,western gorillas face leopard predation risks but theexact degree is unknown [Robbins et al., 2004].Current life history of mountain gorillas could alsoreflect adaptation to predation pressures in the pastso that we were not able to test whether westerngorilla life history has evolved under increasingpredation risk.
A slower life history and longer period ofdependency of immature western gorillas could haveimportant consequences for other aspects of westerngorilla biology. A minimum tenure of 18 yr isrequired for the son of the group’s silverback (whowill then be around 36 yr) to reach maturity. Givenhigh levels of male–male competition and thesubsequent impacts on male longevity and tenurelength, slower life history will impact on theprobability of father–son multimale group forming.If male tenure length is shorter than a male’s age tomature, age-graded groups are unlikely to develop.This scenario could provide an alternative explana-tion for the lack of multimale (kin) groups in westerngorillas compared with mountain gorillas [see alter-native explanation in Harcourt & Stewart, 2007].
The later weaning age (higher ratio of lactationto gestation) and the predominance of one-male
groups in western gorillas could signal increasedinfanticide risk because INF in multimale mountaingorilla groups face lower risks of being killed by asilverback than do one-male groups [Robbins et al.,2007]. Infanticide and predation risk (and otherfactors such as fallen from trees) can cause theobserved high INF mortality rates [more than 50% toweaning age: Breuer, unpublished results; Robbinset al., 2004] of western gorillas at Mbeli Bai.
Recently, western gorillas have been re-classi-fied from endangered to critically endangered on theIUCN Red List, in response to the escalating rates ofdecline owing to Ebola and commercial huntingacross much of their range in the last two decades[Tutin et al., 2005]. Slower development and thepotential for higher mortality compared with moun-tain gorillas will negatively affect their intrinsic rateof increase and their potential for recovery frompopulation crashes. These are therefore importantvariables to incorporate into models of populationdynamics and species-level conservation strategies.This study has provided insights into the potentialimplications of slower life history for westerngorillas, emphasizing the importance of long-termstudies in providing accurate baseline demographicand life-history data of undisturbed primate popula-tions in assessing the vulnerability of populations tothese threats.
ACKNOWLEDGMENTS
Our sincere thanks go to the Ministere del’Economie Forestiere et de l’Environnement forpermission to work in the Nouabale-Ndoki NationalPark and the staff of Wildlife Conservation Society’sCongo Program for crucial logistical and adminis-trative support. We are grateful to many differentresearch assistants who helped to collect data atMbeli and to Roger Mundry for the statistical advice.We thank Damien Caillaud and Shelly Masi for theassignment of gorilla photos and Shelly Masi, MarthaRobbins, Olaf Thalmann and Liz Williamson fortheir helpful comments on an earlier version of thismanuscript. Thanks to Andrew Robbins for the helpwith the demographic database. This researchproject was reviewed and approved by the Congolesegovernment and the Nouabale-Ndoki Project of theWildlife Conservation Society.
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