Mary E. Glenn and Marina Cords (eds): The guenons: diversity and adaptation in African monkeys: Kluwer Academic/Plenum Publishers, New York, 2002. 438 pp

Primates (2004) 45:207210

DOI 10.1007/s10329-004-0081-0BOOK REVIEWNaofumi NakagawaMary E. Glenn and Marina Cords (eds):The guenons: diversity and adaptation in African monkeysKluwer Academic/Plenum Publishers, New York, 2002. 438 ppPublished online: 22 April 2004

Japan Monkey Centre and Springer-Verlag 2004As described in the preface by the editors (MaryE. Glenn and Marina Cords), The Guenons: Diversity

and Adaptation in African Monkeys is edited with full

knowledge of A Primate Radiation: Evolutionary Biology of the African Guenons. Therefore, this review will

compare The Guenons with A Primate Radiation

(Table 1).A Primate Radiation was the rst and last book

dedicated to guenon eld research, when it was published in 1988. In order to put together the progress of

guenon eld research after A Primate Radiation, the

two editors and Gautier-Hion organized a symposium

entitled The Genus Cercopithecus: an update at the

XVIII Congress of the International Primatological

Society in Adelaide, Australia in January 2001. The

Guenons stems from this symposium and attained the

status as the second and last book dedicated to guenon

eld research.As the book titles clearly tell us, the common theme

of these two books is to understand various aspects of

diversity in guenons in the framework of evolution.

Inevitably, the general composition of the two books is

similar. The Guenons is organized into the following

four parts: (1) Evolutionary Biology and Biogeography

(eight chapters); (2) Behavior (12 chapters); (3) Ecology

(three chapters), and (4) Conservation (three chapters).

A Primate Radiation is organized into three parts as

follows: (1) Guenons and the African environment: past

and present (six chapters); (2) Genetic and phonetic

characteristics: their use in phylogenetic reconstruction

(eight chapters); (3) Ecology and social behavior (ten

chapters). Part 1 and part 2 in the latter are merged into

part 1 in the former. This merger reects the fact that

some subjects, such as paleontology and morphology,

get little mention in The Guenons. Instead, part 3 in

A Primate Radiation is divided into part 2 and part 3

in The Guenons and part 4 entitled Conservation

was added to The Guenons.The list of the rst authors gives us a glimpse of the

generation shift of researchers when the dierences in

subjects are excluded. The names of four authorities of

guenon eld research (Telma T. Rowell, Thomas T.

Struhsaker, John F. Oates and Annie Gautier-Hion)

appear in A Primate Radiation, while none of them

are found in The Guenons. However, the large dierence in the list of rst authors is largely because the

editors of The Guenons positively opened up opportunities for young researchers (e.g., Kaplin, Detwiler,

Horsburgh, Windfelder, Macleod, Pazol, Forster and

Worch), and/or African researchers (Ukizintambara).

The rst editor, Mary E. Glenn, herself is a relatively

young researcher who completed her PhD in 1996 in

eld research of a Cercopithecus mona population, which

had been introduced to Grenada, West Indies. On the

other hand, the second editor, Marina Cords, one of ve

authors participating in the creation of both books, is a

senior researcher. When A Primate Radiation was

published, only 5 years had passed since Cords completed her PhD in eld research of Cercopithecus in the

Kakamega Forest, Kenya. Since then, Cords has become established as a prime researcher leading guenon

eld research. Therefore, she is well suited to put

together the recent progress of the guenon studies since

A Primate Radiation.In the preface to The Guenons, the editors clearly

dene guenons as monkeys in the genera, Allenopithecus,

Erythrocebus, Miopithecus, Cercopithecus, possibly in

response to criticism of A Primate Radiation by

Bennett (1991). Every one of the 26 chapters is highly

readable, which is partly because of the short length of

each chapter. The mean and standard deviation in the

number of pages per chapter is 15.5 and 4.5, respectively,

smaller than those of A Primate Radiation. EvenN. NakagawaDepartment of Nursing, Faculty of Nursing,

Kobe City College of Nursing,3-4 Gakuen-nishimachi, Nishi-ku,Kobe 651-2103, JapanE-mail: [email protected].: [phone]Fax: [phone]Table 1 Comparison between The Guenons: Diversity and Adaptation in African Monkeys and A Primate Radiation: Evolutionary

Biology of the African GuenonsTitle The guenons A primate radiationEditors Glenn ME, Cords M Gautier-Hion A, BourliereF, Gautier J-P, Kingdon JYear of publication 2002 1988Publisher Kluwer Academic/PlenumPublishersCambridge University PressPlace of publication New York, USA Cambridge, UK

Page numbers xvi + 438 pp viii + 567 pp

Size 6.59.7 in. 69 in.

Sections 1. Evolutionary biologyand biogeography1. Guenons and the African

environment: past and present2. Behavior 2. Genetic and phonetic

characteristics: their use in

phylogenetic reconstruction3. Ecology 3. Ecology and social behavior4. ConservationNo. of chapters (No. of reviews) 26 (4) 24 (16)

Mean no. of pages perchapter (SD, min.max.)15.5 (4.5, 1028) 20.2 (8.1, 639)No. of color plates 0 7

No. of photographs 1 17

Name of rst authors inalphabetical order(common authors in bold)Butynski TM, Chapman CA,Chism J, Colyn M, Cords M,Curtin SH, Detwiler KM, Disotell TR,Forster S, Glenn ME, Horsburgh KA,Isbell LA, Kaplin BA, Lamberrt J,Lawes MJ, Macleod MC, Gautier J-P,McGraw WS, Pazol K, Tosi AJ, Treves A,

Ukizintambara T, Windfelder TL,Worch EA, Zuberbuhler KButynski TM, Chism J, Colyn M,Cords M, Dutrillaux B, Fedigan L,Gautier J-P, Gautier-Hion A, Hamilton

AC, Kingdon J, Leakey M,Lernould J-M, Loireau J-N,Martin RD, Oates JF, Pickford M,Rowell TE, Ruvolo M, Struhsaker TT,Turner TTPrice (hardcover) US $139.50 US $120.00considering book size, the chapters in The Guenons

are more compact than those of the A Primate Radiation. Another reason is that each chapter in The

Guenons has a summary. Moreover, the epilogue by the

editors of The Guenons provides a well-written summary of all the chapters.Part I. Butynski (chapter 1) overviews the diversities

of the guenon, not only in morphology, ecology,

behavior, social organization, and thus species, but also

in taxonomic classication. The number of genera varies

from one to ve, and the number of species of guenons

varies from 23 to 36. He (and this book) adopts the

Grubb and Butynski et al. classication: four genera

(Allenopithecus, Erythrocebus, Miopithecus, Cercopithecus), 12 species groups, 23 species, and 55 subspecies.

Tosi et al. (chapter 2) show that the Y-chromosomal

patterns coincide with earlier karyotypic studies in

depicting a close relationship among three terrestrial

guenons (E. patas, C. aethiops, C. lhoesti group), which

are distinct from the arboreal guenons. Thus, on the

assumption that the earliest guenons were arboreal,

terrestriality appears to have originated only once

among the extant cercopithecins. The consensus tree of

simultaneous analysis of morphological, behavioral,

acoustical, and karyological data by Gautier et al.

(chapter 4) shows monophyly of the C. lhoesti group

(C. lhoesti, C. preussi, C. solatus) and also supports the

hypothesis above. In contrast, the mitochondrial phylogeny of Disotell and Raaum (chapter 3) shows separate clades: one containing the Cercopithecus guenons

(excluding C. lhoesti) and E. patas, the other containingC. lhoesti (and M. talapoin). These data indicate at least

two origins of terrestriality. More importantly, their

dating analyses show that the Cercopithecus guenons

(excluding C. lhoesti) most likely began to diversify between 7.5 and 8.5 million years ago (mya), older than

those suggested by extrapolation from the fossil record(3.57 mya). Kaplin (chapter 5) proposes a new

hypothesis for maintenance of the current disjunct distribution pattern in the C. lhoesti group. C. lhoesti in

East Africa is separated by 2,000 km from C. preussi in

Cameroon and by 1,600 km from C. solatus in Gabon.C. preussi and C. solatus are separated by 600 km from

each other (Gautier et al.). The C. lhoesti group uniquely

adapts to a terrestrial lifestyle and reliance on the terrestrial herb layer in the forest oor. It is hypothesized

that the existence of grasslands and riverine or gallery

forest prevents these species from dispersing out of their

forest refugia. Colyn and Deleporte (chapter 6) analyze

biogeographic patterns of central African forest primates using a whole data set and six subsets of the data

on localities. The whole data set and two subsets of data

show four major biogeographic areas: South Congo (left

bank of Congo River), East Congo (right bank), West

Central (from the Atlantic Coast to the right bank of

Congo and Ubangi Rivers), and North Congo (right209bank, between Ubangi and Itimbiri Rivers). In addition,

the West Central region reveals an unsuspected complexity, with two subunits, South Ogooue (River) and

West Congo (west from Ubangi River), mixed with an

otherwise largely unresolved upstream zone partly with

hybrids. These results conrm the importance of riverine

barriers for the biogeography of Central African forest

primate communities. Detwiler (chapter 7) reports that

hybridization between C. ascanius and C. mitis occurred

more frequently at Gombe N.P., Tanzania, than at other

East African sites (e.g., Kibale, Budongo, Itwara in

Uganda, Kakamega in Kenya, and Mahale Mountains

in Tanzania). The high incidence of hybridization at

Gombe is attributed at least partly to Gombes topography, which concentrates guenon habitat into narrow,

blind-ended valleys. Under such circumstances, each

guenon social group tends to have relatively few conspecic neighbors with which to exchange migrants. The

mitochondrial phylogeny of Horsburgh et al. (chapter 8)

suggests that C. mona on Grenada was introduced from

SaoTome, o the west-central coast of Africa, rather

than directly from Africa.Part II. McGraw (chapter 9) suggests that correlations between positional behavior and morphology are

not straightforward among the guenons, and do not

always match patterns observed in other primate groups.

For example, neither climbing nor leaping was correlated with body size. This incongruity may be attributable to behavioral exibility both between and within

guenon species. Glenn et al. (chapter 10) rst conrms

the presence of relatively stable all-male group in the

genus Cercopithecus. C. mona in Grenada forms all-male

groups containing two to ve individuals. Maximum

lengths of individual tenure within habituated all-male

groups exceed 2 years. They also describe a copulation

call, which has not been reported in Cercopithecus except

for C. mona and C. solatus. Windfelder and Lwanga

(chapter 11) describes group ssion in C. ascanius. Two

daughter groups fought frequently just after ssion. The

larger daughter group continued to use the original

home range of the mother group whereas the smaller

daughter group shifted its home range. The displaced

daughter group increased daily travel distances as they

established a new territory, and no infants were born the

year after ssion. Treves and Baguma (chapter 12)

advocate the use of simple measures, like spatial proximity and vigilance levels, to evaluate the validity of van

Schaiks (1989) socio-ecological model. According to the

model, on the basis of female dispersal and contest

competition over food resources, C. ascanius, P. badius,

and A. pigra are classied as egalitarian/female-resident,

despotic/female-dispersing, and egalitarian/female-dispersing, respectively. The rst prediction that female

female spatial proximity is higher in female-resident C.

ascanius than in the female-dispersing P. badius or A.

pigra was not supported. However, the second prediction was supported: femalemale proximity is lower in

the female-resident species than in the female-dispersing

species because females should maintain higher levels of

proximity to adult males to acquire male tolerance and

protection in the female-dispersing species. The third

prediction, that vigilance level is higher in despoticP. badius than in egalitarian C. ascanius or A. pigra was

also supported. Isbell et al. (chapter 13) propose a new

hypothesis the limited dispersal hypothesis to explain

the multimale groups in C. aethiops. C. aethiops typically

live within narrow belts of vegetation along rivers, and

their group is usually bordered by only two groups. This

restricted conguration of the habitat and high cost of

dispersal favors multimale groups by limiting dispersal

options for males. Limited dispersal options increase the

genetic relatedness between immigrants and members of

their new groups, which selects against infanticidal

behavior by immigrant males. Exclusion of immigrant

males thus becomes unnecessary, resulting in multimale

groups. Cords (chapter 14) nds a close association between the number of males and the number of estrus

females in a group of C. mitis. However, its causal

relationship is unknown: estrus females attract males to

the group or the presence of males draws females into

estrus. Macleod et al. (chapter 15) suggest that dedicated

extragroup males in a C. mitis population are not able to

live for long enough to compensate for their extremely

low rate of mating success compared with group males.

An assay of the fecal steroid of wild C. mitis by Pazol

et al. is pioneering work providing corrected estimates

(162190 days) of gestation length, and supporting at

the hormonal level the idea that sexual behavior of females serves purposes, such as paternity confusion, that

are not directly related to reproduction. Chism and

Rogers (chapter 17) evaluate the importance of grooming as a behavioral mechanism fostering group cohesion

in E. patas, and conclude that this social behavior does

not serve the hypothesized function. Forster and Cords

(chapter 18) present the rst systematic data on mother

infant relations of C. mitis from forest guenons, and

there is no support for the idea that arboreality delays

the development of independence. Even earlier independence from the mother was attributed to low risk of

intra-group aggression and predation. Worch (chapter19) reveals that insectivory in C. ascanius and C. mitis

inhibit both social and solitary play by juveniles because

of movement through the canopy, a long daily travel

distance, long inter-individual distance, and extended

periods of infant clinging. Zuberbuhler (chapter 20)

examines the function of male loud calls of three guenon

species (C. diana, C. campbelli, C. petaurista). They

function not only as long suggested anti-predator

strategies (i.e., perception advertisement signals and

conspecic warning signals), but also possibly as indicators of male quality. The supporting evidence for the

latter is the occurrence of sexual dimorphisms of loud

calls, diurnal calling patterns, and the call usage in nonpredatory contexts.Part III. Lambert (chapter 21) introduces a new index

of the frequency of resource switching from one food

item to another to assess the interspecic dierence of

feeding behaviors. Overall, C. ascanius, C. mitis, and210Lophocebus albigena had higher frequencies of resource

switching than P. badius. This may help to explain the

coexistence of closely related cercopithecines in similar

trophic space. Chapman et al.s (chapter 22) interseasonal, intergroup, interdemic, interpopulational, and

interspecic dietary comparisons among arboreal Cercopithecus species documents interseasonal variation in

the plant parts used by a single group, showing that

intergroup variation is greater than interspecies variations in some cases. This result exemplies signicant

diet exibility. Curtins (chapter 23) feeding ecology onC. diana roloway is the rst systematic study for this

subspecies. However, the data were collected in 1976.

Much of the diet of C. diana roloway occurs in the terminal branch niche of large emergent trees (arthropods,

young leaves, fruits, and seeds) and in the large woody

climbers (juicy climber fruits, insects).Part IV. Lawes (chapter 24) reveals that C. mitis

vanished in fragmented small forests (<150 ha) in

KwaZulu-Natal, South Africa. Ironically, this is considered to be caused by C. mitiss dietary exibility,

which reduced the need to move among forest fragments. Lawes simulation analysis suggests corridors

signicantly improve their metapopulation persistence in

the long term. Ukizintambara and Thebaud (chapter 25)

conduct statistical analyses to assess relationships between species-specic variables (e.g., area of occupancy,

major food types, IUCN threat category, body size) of

Cercopithecus and country-specic socio-economic

variables (e.g., human population density, GNP, % of

protected areas). The results indicate that small-bodied

Cercopithecus with restricted distribution and specialized

habitat requirements and dietary preferences are the

most threatened because they occur in countries with

high human population density and with very small

protected areas. Butynski (chapter 26) overviews the

status, threats, and recommendations for conservation

of guenons. As a result of high levels of hunting and

forest loss and degradation, six species (C. diana, C.

erythrogaster, C. preussi, C. scalateri and C. erythrotis)

and 12 subspecies of guenons are threatened by extinction.A Primate Radiation includes as many as 16 review

articles of broad theoretical issues by authorities. These

reviews, which summarize the progress of the studies on

each topic, are informative and invaluable. The overall

eect is enhanced by color plates of Jonathan Kingdons

wonderful paintings and by many photos.In contrast, The Guenons includes only four reviews, including two overviews by Butyinski (rst and

last chapters), and Lawes review (chapter 24) of earlier

work by himself and co-workers. The only full-edged

review is by Isbell et al. (chapter 13). Reviews that

summarize the progress of guenon studies published

after A Primate Radiation, especially on topics with

much progress (e.g., polyspecic association, and seed

dispersal), would have added greatly to The Guenons.However, papers in this book make us realize the

remarkable progress of guenon studies since A Primate

Radiation. First, new research elds have exploited

areas such as Lope, Makande, Gabon, and Salonga,

DRC (Chapman et al.); Nyungwe, Rwanda (Kaplin);

Ta, Ivory Coast (McGraw and Zuberbuhler); Grand

Etang, Grenada (Glenn et al.); and Cape Vidal, South

Africa (Macleod et al.). Second, close observations of

social behavior, such as interaction between mother and

infant, and play, have become possible in old research

elds, such as Kakamega, Kenya (Forster and Cords)

and Kibale, Uganda (Worch). Third, new methodological techniques/indices have been developed as follows:

analyses of Y-chromosome (Tosi et al.) and mitochondria DNA (Disotel and Raaum); fecal steroid assay

(Pazol et al.); geographical information system (GIS)

analysis (Ukizintambara and Thebaud); and resource

switching (Lambert). Fourth, studies that strongly re-

ect recent trends, such as van Schaiks (1989) sociological model (Treves and Baguma) and conservation

(Lawes, Ukizintambara and Thebaud) have been conducted. Lastly, new hypotheses have been proposed in

Tosi et al., Kaplin, Isbell et al. and Zuberbuhler (see

above in details).It goes without saying that new hypotheses and new

methodological techniques/indices as described above

need further examination of their validity and/or applicability. Exploitation of new research elds and longterm studies will enhance such opportunities. The more

detailed data that emerge, the more we can know about

the guenons. On the other hand, the more we can know

about the guenons, the more diculty there may be to

nd common characteristics of guenons, even in

one species, other than variation, exibility, and

diversity. However, high levels of hunting and habitat

loss may cause guenons to become locally extinct, and if

so we may lose the diversity of guenons, and nally nd

the common characteristics of guenons. How tragic such

a scenario is!ReferencesBennett EL (1991) Book review of A Primate Radiation: Evolutionary Biology of the African Guenons. Int J Primatol 12:185

190Gautier-Hion A, Bouliere F, Gautier J-P, Kingdon J (eds) (1988) A

primate radiation: evolutionary biology of the African guenons.

Cambridge University Press, Cambridgevan Schaik CP (1989) The ecology of social relationships amongst

female primates. In: Standen V, Foley RA (eds) Comparative

socioecology. Blackwell, Oxford, pp 195218