9
Research Article Logging Activity Adversely Impacts Primate Diversity and Density in the Kwabre Rainforest of Ghana Emmanuel Danquah and Elvis Hackman Tetteh Faculty of Renewable Natural Resources, College of Agriculture and Natural Resources, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana Correspondence should be addressed to Emmanuel Danquah; [email protected] Received 24 March 2016; Revised 22 June 2016; Accepted 3 August 2016 Academic Editor: Ram Chander Sihag Copyright © 2016 E. Danquah and E. H. Tetteh. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Knowledge on the impacts of logging activity on inhabitant primate species in Kwabre Rainforest, Ghana, is vital for the develop- ment of a comprehensive conservation and management plan. With this background, primate density and diversity were recorded along line transects in logged and unlogged areas (strata) to assess the impact of logging activity on these parameters. Six distinct primate species were confirmed including Roloway monkey (Cercopithecus roloway, listed as endangered in the IUCN List of reat- ened Species), white-naped mangabey (Cercocebus lunulatus, vulnerable), and Geoffroy’s black-and-white colobus (Colobus vellero- sus, vulnerable). ere was a significant difference (Mann-Whitney test: = 36.0, < 0.01) in primate encounter rates between the logged and unlogged strata with higher species diversity in unlogged stratum ( = 2.91) compared to the logged stratum (= 1.44). Regression analysis indicated a significant effect ( 2 = 0.945, < 0.01) of logging on primate encounter rates. Our results suggest that logging activity can alter composition of primate communities. One option to forestall further forest degradation and its adverse effects on primates would be to grant the Kwabre Rainforest protected area status under Ghanaian law and manage it under an integrated conservation plan that includes neighbouring Ankasa Conservation Area in Ghana and Tano´ e Forest in Cote d’Ivoire. 1. Introduction e ability of many wildlife species to thrive in densely human populated areas depends largely on their level of tolerance for anthropogenic disturbances like deforestation and habitat fragmentation [1, 2]. Primates are believed to be suitable biological indicators for assessing the effects of log- ging on wildlife habitats due to their strong connection with forest cover and vegetative complexity [3–5]. Apart from their responses to changes in vegetation structure which makes them good indicators, primates were selected over other spe- cies because their habitat requirements are better known and can be sampled with relatively simple methods like transects [6, 7]. In Ghana, the Kwabre Rainforest is a unique community- owned forest and it is reported to host several primate species of international conservation importance, including the Roloway monkey (Cercopithecus roloway), white-naped mangabey (Cercocebus lunulatus), and Geoffroy’s black-and- white colobus (Colobus vellerosus) [8, 9]. ese species are listed on the International Union for the Conservation of Nature’s (IUCN) Red List of reatened Species [10] and Appendix I of the Convention on International Trade in Endangered Species (CITES) [11, 12]. Unfortunately, the Kwabre Rainforest is exposed to an increasing risk of defor- estation from illegal logging and farming activity. ese activ- ities, when unchecked, may adversely affect several species, particularly canopy dwelling primates. Existing studies of the impact of anthropogenic forest disturbance on primate popu- lations have provided valuable insights into (i) effects of selec- tive logging on primate density [13–18]; (ii) the role of habitat disturbances in diet selection and primate abundance [14, 19]; and (iii) behavioural and physiological responses of primates to habitat alteration [20, 21]. In Ghana, no one has yet under- taken a quantitative assessment of the impacts of logging on primate abundance. is information is however vital to understand the sensitivities and habitat requirements of the species in order to develop an informed management plan. e aim of this study was to examine the impact of logging activity on primate species in the Kwabre Rainforest Hindawi Publishing Corporation International Journal of Ecology Volume 2016, Article ID 7497326, 8 pages http://dx.doi.org/10.1155/2016/7497326

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Page 1: Research Article Logging Activity Adversely Impacts Primate Diversity …downloads.hindawi.com/journals/ijecol/2016/7497326.pdf · 2019-07-30 · Primate Diversity. Primate species

Research ArticleLogging Activity Adversely Impacts Primate Diversity andDensity in the Kwabre Rainforest of Ghana

Emmanuel Danquah and Elvis Hackman Tetteh

Faculty of Renewable Natural Resources College of Agriculture and Natural ResourcesKwame Nkrumah University of Science and Technology Kumasi Ghana

Correspondence should be addressed to Emmanuel Danquah emmanueldanquahgmailcom

Received 24 March 2016 Revised 22 June 2016 Accepted 3 August 2016

Academic Editor Ram Chander Sihag

Copyright copy 2016 E Danquah and E H TettehThis is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in anymedium provided the originalwork is properly cited

Knowledge on the impacts of logging activity on inhabitant primate species in Kwabre Rainforest Ghana is vital for the develop-ment of a comprehensive conservation and management plan With this background primate density and diversity were recordedalong line transects in logged and unlogged areas (strata) to assess the impact of logging activity on these parameters Six distinctprimate specieswere confirmed includingRolowaymonkey (Cercopithecus roloway listed as endangered in the IUCNList ofThreat-ened Species) white-napedmangabey (Cercocebus lunulatus vulnerable) and Geoffroyrsquos black-and-white colobus (Colobus vellero-sus vulnerable) There was a significant difference (Mann-Whitney 119880 test119880 = 360 119901 lt 001) in primate encounter rates betweenthe logged and unlogged strata with higher species diversity in unlogged stratum (119867 = 291) compared to the logged stratum (119867 =144) Regression analysis indicated a significant effect (1199032 = 0945 119901 lt 001) of logging on primate encounter rates Our resultssuggest that logging activity can alter composition of primate communities One option to forestall further forest degradation and itsadverse effects on primates would be to grant the Kwabre Rainforest protected area status under Ghanaian law andmanage it underan integrated conservation plan that includes neighbouring Ankasa Conservation Area in Ghana and Tanoe Forest in Cote drsquoIvoire

1 Introduction

The ability of many wildlife species to thrive in denselyhuman populated areas depends largely on their level oftolerance for anthropogenic disturbances like deforestationand habitat fragmentation [1 2] Primates are believed to besuitable biological indicators for assessing the effects of log-ging on wildlife habitats due to their strong connection withforest cover and vegetative complexity [3ndash5] Apart from theirresponses to changes in vegetation structure which makesthem good indicators primates were selected over other spe-cies because their habitat requirements are better known andcan be sampled with relatively simple methods like transects[6 7]

In Ghana the Kwabre Rainforest is a unique community-owned forest and it is reported to host several primatespecies of international conservation importance includingthe Roloway monkey (Cercopithecus roloway) white-napedmangabey (Cercocebus lunulatus) and Geoffroyrsquos black-and-white colobus (Colobus vellerosus) [8 9] These species are

listed on the International Union for the Conservation ofNaturersquos (IUCN) Red List of Threatened Species [10] andAppendix I of the Convention on International Trade inEndangered Species (CITES) [11 12] Unfortunately theKwabre Rainforest is exposed to an increasing risk of defor-estation from illegal logging and farming activityThese activ-ities when unchecked may adversely affect several speciesparticularly canopy dwelling primates Existing studies of theimpact of anthropogenic forest disturbance on primate popu-lations have provided valuable insights into (i) effects of selec-tive logging on primate density [13ndash18] (ii) the role of habitatdisturbances in diet selection and primate abundance [14 19]and (iii) behavioural and physiological responses of primatesto habitat alteration [20 21] In Ghana no one has yet under-taken a quantitative assessment of the impacts of loggingon primate abundance This information is however vital tounderstand the sensitivities and habitat requirements of thespecies in order to develop an informed management plan

The aim of this study was to examine the impact oflogging activity on primate species in the Kwabre Rainforest

Hindawi Publishing CorporationInternational Journal of EcologyVolume 2016 Article ID 7497326 8 pageshttpdxdoiorg10115520167497326

2 International Journal of Ecology

inwesternGhana Tomeet this aim censuses were conductedto (1) compare primate density and species compositionbetween the logged and unlogged strata and (2) evaluatethe effect of logging intensity on primate encounter ratesThe null hypothesis predicts no significant difference inprimate density and species composition between logged andunlogged areas Conclusions drawnwill contribute tomanag-ing primate conservation projects in this region and help todictate future logging programmes in other rainforests Thisstudy provides three important advantages over the earlierstudies One it focuses on different groups of primate speciesrather than just one species [22ndash24] Two it incorporatesin its design a control area (an unlogged stratum) that wascompletely without any logging activity This factor alloweda fairly objective assessment of the relative effects of loggingactivity on different primate species Lastly the study has bothlocal and regional relevance because the study area is a poten-tially key corridor between two designated national parksin Ghana and neighbouring Cote drsquoIvoire and this regionof southwestern Ghana could be one of the most importantareas for wildlife protection in West Africa

2 Materials and Methods

21 Study Area The Kwabre Rainforest Ghana (50 km2 lat5∘061015840ndash5∘161015840N long 2∘401015840ndash2∘471015840W Figure 1) is a community-owned swamp forest in the Western Region of Ghana andforms part of the Upper Guinean Forest Block It is locatedclose to the Ghana-Cote drsquoIvoire international border oppo-site to the Tanoe Forest The area forms part of a networkof forest reserves in southwestern Ghana which constituteGhanarsquos portion of the proposed transboundary elephantmigration corridor between Ghana and Ivory Coast [25] Inaddition the Kwabre Rainforest makes up a crucial corridorfor wildlife between the Ankasa Conservation Area in Ghanaand the Tanoe community-managed forest in Cote drsquoIvoire[9] (Figure 2) The area also forms part of the range ofseveral flagship endangered primates including the crownedmangabey Rolowaymonkey andMissWaldronrsquos red colobusnow considered extinct by primatologists [9 26]

Selective logging of timber species by chainsaw operatorsand bushmeat hunting perpetrated by people coming fromoutside the local communities is destroying the originalpristine habitat surrounding the Kwabre Rainforest areaMost of the logged areas are easily accessible from the mainTakoradi-Elubo highway (Figure 1) The area is also exposedto an increasing risk of deforestation from farming for cashcrops including rubber palm oil and cocoa logging andmining activity expanding fringe communities and humanencroachment on forest resources The recent discovery ofcrude oil off the coast of Western Region with its attendanthigh local immigration as a result of the influx of job seekershas increased the human population density in the area

22 Data Collection The study area was classified into loggedand unlogged strata (Figure 1) based on an initial reconnais-sance to map out the presence or absence of logging activityPrimate surveys were conducted in the two strata using line

transects A total of six 500m line transects (3 km) wereestablished in each stratum Transects were monitored con-secutively over a survey period of twoweeks in February 2014The survey period comprised alternating each field day witha nonfield day in order to stagger disturbance of survey teamon primate behaviour Thus a total of seven field days wererealized over the survey period resulting in a total of 21 kmof transects walked in each stratum for the entire study area

The starting point of each transect was determinedsystematically on a gridded map of the study area Theaverage distance between any two line transects was 3 kmLine transect surveys began early in themorning around 630am and lasted on average for 5-6 hours Primate calls wereused to access the presence and type of primate species inthe vicinity of the transects However only direct sightingsof primates were recorded All sightings where estimationof group size was difficult to assess were disregarded Whenprimateswere encountered the number of individuals (groupsize) species time GPS (Garmin GPSmap 62) locationand perpendicular distance to primate(s) were recorded Thedistance along transects was measured with a tape measureThe perpendicular ground distance from the transect centerline to an estimated central point directly beneath wherethe primates were initially sighted was also measured usinga tape measure Binoculars were used when necessary toconfirm species identity An index of logging activity per kmwas generated by recording the number of logged trees (treestumps) observed along each transect

23 DataAnalysis Primate densitywas calculated usingDIS-TANCE Version 41 software package [27] The best modelselection was based on the values of Akaikersquos InformationCriterion (AIC) and recommendations by [28] Encounterrates were calculated in the form of Kilometric Indices ofAbundance (KIA) where the number of recorded primatesand indicators of logging incidence are presented accordingto the distance walked during the surveyTheMann-Whitney119880 test was used to test for any significant difference in primateencounter rates between the logged and unlogged strata Pri-mate species richness and diversity for each stratum was cal-culated using EstimateSWin800 Version 800 software pack-age [29] Bootstrap Richness Estimator was used for speciesrichness and Shannon-Weiner index for species diversity

The effect of logging intensity on primate encounter rateswas tested using regression analysis in Canoco version 45[30] Statistical analyses using the program Spatial AnalysisinMacroecology [31] were conducted to correct for normalityand spatial autocorrelation

3 Results

31 Conservation Status of Primates at Kwabre Forest

Six Species of Diurnal PrimatesRolowaymonkey (Cercopithe-cus roloway) white-naped mangabey (Cercocebus lunulatus)Geoffroyrsquos black-and-white colobus (Colobus vellerosus) olivecolobus (Procolobus verus) lesser spot-nosedmonkey (Cerco-pithecus petaurista) and Lowersquosmonkey (Cercopithecus lowei)were recorded in the survey (Table 1)

International Journal of Ecology 3

(km)

Transects

Logged stratum

Kwabre Rainforest

RiversRoadsTowns

5250

N

Alenda Wharf

Anwiafutu

Kofi Gaman

Elubo

Amoakwasuazo

299840099840045

9984000∘W 2

99840099840040

9984000∘W

599840099840010

9984000∘N

599840099840015

9984000∘N

299840099840040

9984000∘W2

99840099840045

9984000∘W

599840099840015

9984000∘N

599840099840010

9984000∘N

Nigeria

Togo

CotedrsquoIvoire

BurkinaFaso

Beni

n

Gha

na

Figure 1 Map of Kwabre Rainforest showing the logged stratum

Rolowaymonkey is listed as an endangered species on theIUCN Threatened Species List white-naped mangabey andGeoffroyrsquos black-and-white colobus are listed as vulnerablespecies and olive colobus is listed as near-threatened species

[10] The spot-nosed monkey and Lowersquos monkey are con-sidered to be of least concern and are of local conservationimportance (Schedule 1) under Ghanaian law (LI 1284-Wildlife Conservation (Amendment) Regulations 1983)

4 International Journal of Ecology

N

(km)201050

Corridor routeInternational boundary

Protected areas

Ankasa Conservation Area

Kwabre Rainforest

RiversRoads

Cote drsquoIvoire Ghana

Nigeria

Togo

Beni

n

Gha

na

BurkinaFaso

CotedrsquoIvoire

Tanoeacute Forest

Figure 2 Map of the proposed transboundary elephant migrationcorridor between Ghana and Ivory Coast

Table 1 IUCN status of primate species found in the KwabreRainforest

Common name Scientific name IUCN statusRoloway monkey Cercopithecus roloway ENWhite-naped mangabey Cercocebus lunulatus VUBlack-and-white colobus Colobus vellerosus VUOlive colobus Procolobus verus NTSpot-nosed monkey Cercopithecus petaurista LCLowersquos monkey Cercopithecus lowei LCEN endangered VU vulnerable NT near threatened LC least concern

32 Primate Diversity Primate species composition variedacross the logged and unlogged strata but was not signifi-cantly different (Mann-Whitney 119880 test 119880 = 360 119901 gt 005)The unlogged stratum was found to be more diverse thanlogged stratum when various richness and diversity indices

Table 2 Primate species diversity index generated by Esti-mateSWin800

Stratum Shannon-Weiner mean Standard deviationLogged 144 022Unlogged 291 016

Table 3 Pooled primate density parameters estimated for the loggedand unlogged strata

Density parameters Loggedstratum

Unloggedstratum

Density (kmminus2) 34993 88368Percent coefficient ofvariation [CV ()] 2239 1064

Upper confidence limit (CL) 20529 68517Lower confidence limit (CL) 59647 113970

were applied to the data (Table 2) Comparably these indiceswere very low in the logged stratum

None of the species were unique to any of the definedlogging categories but the generally higher primate speciesrichness in the unlogged stratum in comparison to loggedstratum may reflect primatesrsquo general adaptation to matureforest systems with taller trees and denser canopy covers

33 Primate Density Primate density was significantly lower(less than 50) in the logged stratum compared to theunlogged stratum (Table 3) The half normal + cosine modelwithout truncation gave the best fit to the data Note that DIS-TANCE produces estimates with asymmetrical confidencelimits

There was also a significant difference in the individualprimate encounter rates (Mann-Whitney 119880 test 119880 = 360119901 lt 001) across the two categories of strata that islogged and unlogged (Table 4) The percentage of individ-ual primates encountered was considerably greater in theunlogged (73) than in logged (27) stratum howeverprimate group sizes for the same species were similar for bothstrata (Table 4) All species apart from the black-and-whitecolobus showed greater densities in the unlogged stratum

34 Relationship between Primate Density and Logging Inten-sity The number of primates encountered was inverselyrelated to logging intensity (1199032 = 0945119901 lt 001)Thehighestencounter rates of primates were observed in slightly loggedor unlogged forests (Figure 3)

4 Discussion

The results suggest that logging could negatively influenceprimate communities through the modification of primatedensity and species composition Therefore the null hypoth-esis of no significant difference in primate density and speciescomposition between logged and unlogged areas is rejectedSuch inference must however be made cautiously as logging

International Journal of Ecology 5

Table4En

coun

terrates

ofprim

ates

andloggingintensity

intheK

wabre

Rainforest

Stratumtr

ansects

Lowersquos

mon

key

Spot-nosed

mon

key

White-naped

mangabey

Roloway

mon

key

Olive

colobu

sBlack-and-white

colobu

sTo

tal

prim

ates

Prim

ates

perk

mLo

ggingintensity

perk

mLo

gged

10(0)

0(0)

0(0)

0(0)

0(0)

0(0)

00

102

1(11)

1(8)

0(0)

0(0)

0(0)

2(65)

309

43

0(0)

1(6)

0(0)

0(0)

1(3)

3(654)

247

34

1(8)

0(0)

1(5)

0(0)

0(0)

1(7)

206

75

2(79)

0(0)

0(0)

0(0)

1(4)

1(6)

267

66

1(6)

0(0)

0(0)

1(6)

1(3)

2(67)

286

5Mean

82

7050

60

33

57

256

7058

Total

4114

56

1052

128

3535

Unlogged

72(129)

1(10)

1(5)

0(0)

2(43)

1(7)

5014

08

3(10911)

2(911)

1(6)

1(6)

1(4)

0(0)

6619

09

1(7)

2(79)

1(3)

0(0)

1(5)

1(5)

3610

010

2(98)

1(8)

1(4)

2(43)

2(33)

2(65)

5315

011

4(118126)

3(869)

0(0)

1(5)

1(4)

1(7)

7622

012

2(68)

3(1197)

2(53)

1(4)

1(3)

1(5)

6117

0Mean

9086

43

44

36

58

570

160

Total

126

104

2622

2935

342

970

Num

bersou

tside

bracketsindicatethen

umbero

fprim

ateg

roup

sand

numbersin

bracketsindicategrou

psiz

esandlogged

trees

perk

m

6 International Journal of Ecology

minus25

0

25

5

75

10

125

15

175

20

225

Num

ber o

f prim

ates

per

km

minus2 0 2 4 6 8 10 12Logging activity per km

Y = 15974 minus 2137 lowast X + 064 lowast X2 R

2= 769

Figure 3 Relationship between encounter rates of primates andlogging intensity

may not be the only factor influencing primate species com-position and density Although both strata possess similartopography and vegetation type logged areas had recentlogging disturbances that resulted in reduced canopy coverand denser understory cover A factor that may have alsoinfluenced our findings could be the proximity of some fringecommunities to the forest edge During the study it wasobserved that logged areas were closer to fringe communitiesand farms making such areas more susceptible to humandisturbances such as poaching [17 32] Some of these differ-ences in human and ecological variables may have influencedour findings One reason that may have accounted for highernumbers of black-and-white colobuses in the logged stratumis that they are folivores [14] and as suchmay show preferencefor degraded areas where the open canopy permits growthof diverse understory Apart from changes in density anddiversity logging might have also affected the behaviour ofprimates [13 20 33] For instance primates exhibited extremeshyness including restricting calls in the logged stratumcompared to the unlogged stratum when teams encounteredprimate groups The apparent differences in the incidence ofalarm calls between groups ofmonkeys encountered betweenthe two strata could affect our census findings to a smallextent However previous studies on primate surveys [14 2434] have shown that many replications are needed at eachtransect before the group density estimates can be consideredreliable In the current study each transect was sampledmorethan once and this could increase the reliability of our results

Our study draws attention to matters of both nationaland international conservation concern The evidence ofunauthorized human activities recorded during this study

indicates clearly that the community-based managementsystem practiced at Kwabre Rainforest may not be effectivein preventing poaching and other illegal human activities inthe forest If current threats continue unabated then rapidpopulation decline of primates is expected in the near future

Given its considerably intact forest cover Ghana is in aposition to implement important forest conservation initia-tives in the subregion [35 36] Within Ghana the generalvicinity of the Kwabre Rainforest is very significant from aregional viewpoint because it constitutes part of a networkof forest reserves in southwestern Ghana which constitutesGhanarsquos portion of the proposed crucial corridor for wildlifebetween the Ankasa Conservation Area in Ghana and theTanoe Forest in Cote drsquoIvoire [9]

In this regional setting the future management of theKwabre corridor could be very important At present farmsand villages are flourishing along theKwabre corridor rapidlyincreasing local human pressure Concerns about the futureof Kwabre corridor are particularly important because inter-est to protect wildlife in the area has waned andKwabre Rain-forest could face a sudden increase in hunting logging andslash-and-burn farming Instead of acting as a communityforest buffer zone and possible faunal corridor between twokey international protected areas (Ankasa ConservationAreain Ghana and Tanoe Forest in neighbouring Cote drsquoIvoireFigure 2) the larger Kwabre corridor area could insteadbecome a major population sink for wildlife [13 37 38] Thiswould reinforce adverse edge effects and genetic isolationof the protected areas increasing the probability of localextinctions of species of conservation interest [39 40]

5 Conclusions and Recommendations

Kwabre Rainforest is an important site where careful wildlifemanagement can support major biodiversity conservationin Ghana hence more effort should be channeled intopreventing further habitat degradation of the larger KwabreRainforest corridor area One possibility would be to grantthe Kwabre Rainforest protected area status under Ghanaianlaw and to manage it under the umbrella of an integratedconservation plan that includes its two adjacent internationalprotected areas Such a plan can be achieved by designatingthe entire area as a biosphere reserve which would permitplanned development outside reserves while affording highprotection for protected areas [41] With effective long-term management this region of southwestern Ghana couldremain one of the most important areas for wildlife in WestAfrica

Competing Interests

The authors declare that there are no competing interestsregarding the publication of this paper

Acknowledgments

Many thanks are due to the traditional head and people ofKwabre

International Journal of Ecology 7

References

[1] B Czech P R Krausman and P K Devers ldquoEconomic asso-ciations among causes of species endangerment in the UnitedStatesrdquo BioScience vol 50 no 7 pp 593ndash601 2000

[2] D S Wilcove C H Mclellan and A P Dobson ldquoHabitatfragmentation in the temperate zonerdquo in Conservation BiologyThe Science of Scarcity and Species Richness M E Soule Ed pp237ndash256 Sinauer Associates Sunderland Mass USA 1998

[3] A G Chiarello ldquoDensity and population size of mammals inremnants of BrazilianAtlantic forestrdquoConservation Biology vol14 no 6 pp 1649ndash1657 2000

[4] RK Laidlaw ldquoEffects of habitat disturbance andprotected areasonmammals of PeninsularMalaysiardquoConservation Biology vol14 no 6 pp 1639ndash1648 2000

[5] M A Lopes and S F Ferrari ldquoEffects of human colonization onthe abundance and diversity of mammals in eastern BrazilianAmazoniardquo Conservation Biology vol 14 no 6 pp 1658ndash16652000

[6] E Carrillo G Wong and N A D Cuaron ldquoMonitoringmammal populations in Costa Rican protected areas underdifferent hunting restrictionsrdquo Conservation Biology vol 14 no6 pp 1580ndash1591 2000

[7] M Conroy and D Nichols ldquoDesigning a study to assessmammalian diversityrdquo in Measuring and Monitoring BiologicalDiversity StandardMethods forMammals DWilson R Cole JNichols R Rudran andM Foster Eds pp 41ndash49 SmithsonianInstitution Press London UK 1996

[8] WAPCA Annual Report West African Primate ConservationAction WAPCA Accra Ghana 2012

[9] D Osei R H Horwich and J M Pittman ldquoFirst sightings ofthe Roloway Monkey (Cercopithecus diana roloway) in Ghanain ten years and the status of other endangered primates inSouthwesternGhanardquoAfrican Primates vol 10 pp 25ndash40 2015

[10] The IUCN Red List ofThreatened Species Version 20152 2015httpwwwiucnredlistorg

[11] W S McGraw and J F Oates ldquoRoloway monkey Cercopithecusdiana roloway (Schreber 1774)rdquo in Primates in Peril TheWorldrsquos Most Endangered Primates 2012ndash2014 C Schwitzer RA Mittermeier A B Rylands et al Eds pp 14ndash16 IUCN SSCPrimate Specialist Group (PSG) International PrimatologicalSociety (IPS) Conservation International (CI) and BristolZoological Society Arlington Va USA 2014

[12] R A Mittermeier J Ratsimbazafy A B Rylands et al ldquoPri-mates in peril the worldrsquos 25 most endangered primates 2006ndash2008rdquo Primate Conservation vol 22 pp 1ndash40 2007

[13] D Swift ldquoThe consequences of logging on primate density anddiversity in Kibale National Park Ugandardquo Bioscience Horizonsvol 5 pp 1ndash6 2012

[14] C A Chapman L J Chapman L Naughton-Treves M JLawes and L R Mcdowell ldquoPredicting folivorous primateabundance validation of a nutritionalmodelrdquoAmerican Journalof Primatology vol 62 no 2 pp 55ndash69 2004

[15] J P Skorupa The effects of selective timber harvesting onrain-forest primates in Kibale Forest Uganda [PhD thesis]University of California Davis Davis Calif USA 1988

[16] T T Struhsaker Ecology of an African Rainforest Logging inKibale and the Conflict between Conservation and ExploitationUniversity Press of Florida Gainesville Fla USA 1997

[17] P Mayor P Perez-Pena M Bowler P E Puertas M Kirklandand R Bodmer ldquoEffects of selective logging on large mammal

populations in a remote indigenous territory in the northernperuvian amazonrdquo Ecology and Society vol 20 no 4 pp 36ndash44 2015

[18] A J Plumptre and V Reynolds ldquoThe effect of selective loggingon the primate populations in the Budongo Forest ReserveUgandardquo Journal of Applied Ecology vol 31 no 4 pp 631ndash6411994

[19] C Mammides M Cords and M K Peters ldquoEffects of habitatdisturbance and food supply on population densities of threeprimate species in theKakamega Forest KenyardquoAfrican Journalof Ecology vol 47 no 1 pp 87ndash96 2009

[20] C Schwitzer L Glatt K A-I Nekaris and J U GanzhornldquoResponses of animals to habitat alteration an overviewfocussing on primatesrdquo Endangered Species Research vol 14 no1 pp 31ndash38 2011

[21] R Rimbach A Link M Heistermann C Gomez-Posada NGalvis and E W Heymann ldquoEffects of logging hunting andforest fragment size on physiological stress levels of two sym-patric ateline primates in Colombiardquo Conservation Physiologyvol 1 no 1 Article ID cot031 pp 1ndash11 2013

[22] R F W Barnes K L Barnes M P T Alers and A Blom ldquoMandetermines the distribution of elephants in the rain forests ofnortheastern Gabonrdquo African Journal of Ecology vol 29 no 1pp 54ndash63 1991

[23] R F W Barnes K Beardsley F Michelmore K L Barnes M PT Alers andA Blom ldquoEstimating forest elephant numberswithdung counts and a geographic information systemrdquo Journal ofWildlife Management vol 61 no 4 pp 1384ndash1393 1997

[24] S A Lahm R F W Barnes K Beardsley and P CervinkaldquoA method for censusing the greater white-nosed monkey innortheastern Gabon using the population density gradient inrelation to roadsrdquo Journal of Tropical Ecology vol 14 no 5 pp629ndash643 1998

[25] L Sebogo and R F W Barnes ldquoAction plan for the manage-ment of trans-frontier elephant conservation corridors in WestAfricardquo Tech Rep IUCNAfESGOuagadougou Burkina Faso2003

[26] J F OatesM Abedi-LarteyW SMcGraw T T Struhsaker andG H Whitesides ldquoExtinction of a West African red colobusmonkeyrdquo Conservation Biology vol 14 no 5 pp 1526ndash15322000

[27] L Thomas J L Laake S Strindberg et al Distance 40 Release1 Research Unit for Wildlife Population Assessment Universityof St Andrews St Andrews Scotland 2002

[28] S T Buckland D R Anderson K P Burnham J L Laake DL Borchers and L Thomas Introduction to Distance SamplingEstimating Abundance of Biological Populations OxfordUniver-sity Press Oxford UK 2001

[29] R K Colewell EstimateS Statistical Estimation of SpeciesRichness and Shared Species from Samples Version 8 2006httppurloclcorgestimates

[30] C J F Ter Braak and P Imilauer Canoco Reference Manual andCanoDraw for Windows Userrsquos Guide Software for CanonicalCommunity Ordination (Version 45) Microcomputer PowerIthaca NY USA 2002

[31] T F L V B Rangel J A FDiniz-Filho and LM Bini ldquoTowardsan integrated computational tool for spatial analysis in macroe-cology and biogeographyrdquo Global Ecology and Biogeographyvol 15 no 4 pp 321ndash327 2006

[32] W F Laurance B M Croes L Tchignoumba et al ldquoImpactsof roads and hunting on central African rainforest mammalsrdquoConservation Biology vol 20 no 4 pp 1251ndash1261 2006

8 International Journal of Ecology

[33] C A Chapman S R Balcomb T R Gillespie J P Skorupa andT T Struhsaker ldquoLong-term effects of logging on African pri-mate communities a 28-year comparison from Kibale NationalPark Ugandardquo Conservation Biology vol 14 no 1 pp 207ndash2172000

[34] S A Lahm and J P Tezi ldquoAssessment of the communities ofmedium-sized and large arboreal and terrestrial mammals inthe Rabi-Toucan region of the Ngove-Ndogo Hunting Domainand southwestern Loango National Parkrdquo Bulletin of the Biolog-ical Society of Washington vol 12 pp 383ndash416 2006

[35] W F Laurance A AlonsoM Lee and P Campbell ldquoChallengesfor forest conservation in Gabon Central Africardquo Futures vol38 no 4 pp 454ndash470 2006

[36] A Kamdem-Toham AW Adeleke N D Burgess et al ldquoForestconservation in the Congo Basinrdquo Science vol 299 no 5605article 346 2003

[37] A J Novaro K H Redford and R E Bodmer ldquoEffect ofhunting in source-sink systems in theNeotropicsrdquoConservationBiology vol 14 no 3 pp 713ndash721 2000

[38] C A Peres ldquoSynergistic effects of subsistence hunting andhabitat fragmentation on amazonian forest vertebratesrdquoConser-vation Biology vol 15 no 6 pp 1490ndash1505 2001

[39] R Woodroffe and J R Ginsberg ldquoEdge effects and the extinc-tion of populations inside protected areasrdquo Science vol 280 no5372 pp 2126ndash2128 1998

[40] W F Laurance T E Lovejoy H L Vasconcelos et alldquoEcosystem decay of Amazonian forest fragments a 22-yearinvestigationrdquo Conservation Biology vol 16 no 3 pp 605ndash6182002

[41] A Kaus ldquoEnvironmental perceptions and social relations in theMapimı Biosphere Reserverdquo Conservation Biology vol 7 no 2pp 398ndash406 1993

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

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International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 2: Research Article Logging Activity Adversely Impacts Primate Diversity …downloads.hindawi.com/journals/ijecol/2016/7497326.pdf · 2019-07-30 · Primate Diversity. Primate species

2 International Journal of Ecology

inwesternGhana Tomeet this aim censuses were conductedto (1) compare primate density and species compositionbetween the logged and unlogged strata and (2) evaluatethe effect of logging intensity on primate encounter ratesThe null hypothesis predicts no significant difference inprimate density and species composition between logged andunlogged areas Conclusions drawnwill contribute tomanag-ing primate conservation projects in this region and help todictate future logging programmes in other rainforests Thisstudy provides three important advantages over the earlierstudies One it focuses on different groups of primate speciesrather than just one species [22ndash24] Two it incorporatesin its design a control area (an unlogged stratum) that wascompletely without any logging activity This factor alloweda fairly objective assessment of the relative effects of loggingactivity on different primate species Lastly the study has bothlocal and regional relevance because the study area is a poten-tially key corridor between two designated national parksin Ghana and neighbouring Cote drsquoIvoire and this regionof southwestern Ghana could be one of the most importantareas for wildlife protection in West Africa

2 Materials and Methods

21 Study Area The Kwabre Rainforest Ghana (50 km2 lat5∘061015840ndash5∘161015840N long 2∘401015840ndash2∘471015840W Figure 1) is a community-owned swamp forest in the Western Region of Ghana andforms part of the Upper Guinean Forest Block It is locatedclose to the Ghana-Cote drsquoIvoire international border oppo-site to the Tanoe Forest The area forms part of a networkof forest reserves in southwestern Ghana which constituteGhanarsquos portion of the proposed transboundary elephantmigration corridor between Ghana and Ivory Coast [25] Inaddition the Kwabre Rainforest makes up a crucial corridorfor wildlife between the Ankasa Conservation Area in Ghanaand the Tanoe community-managed forest in Cote drsquoIvoire[9] (Figure 2) The area also forms part of the range ofseveral flagship endangered primates including the crownedmangabey Rolowaymonkey andMissWaldronrsquos red colobusnow considered extinct by primatologists [9 26]

Selective logging of timber species by chainsaw operatorsand bushmeat hunting perpetrated by people coming fromoutside the local communities is destroying the originalpristine habitat surrounding the Kwabre Rainforest areaMost of the logged areas are easily accessible from the mainTakoradi-Elubo highway (Figure 1) The area is also exposedto an increasing risk of deforestation from farming for cashcrops including rubber palm oil and cocoa logging andmining activity expanding fringe communities and humanencroachment on forest resources The recent discovery ofcrude oil off the coast of Western Region with its attendanthigh local immigration as a result of the influx of job seekershas increased the human population density in the area

22 Data Collection The study area was classified into loggedand unlogged strata (Figure 1) based on an initial reconnais-sance to map out the presence or absence of logging activityPrimate surveys were conducted in the two strata using line

transects A total of six 500m line transects (3 km) wereestablished in each stratum Transects were monitored con-secutively over a survey period of twoweeks in February 2014The survey period comprised alternating each field day witha nonfield day in order to stagger disturbance of survey teamon primate behaviour Thus a total of seven field days wererealized over the survey period resulting in a total of 21 kmof transects walked in each stratum for the entire study area

The starting point of each transect was determinedsystematically on a gridded map of the study area Theaverage distance between any two line transects was 3 kmLine transect surveys began early in themorning around 630am and lasted on average for 5-6 hours Primate calls wereused to access the presence and type of primate species inthe vicinity of the transects However only direct sightingsof primates were recorded All sightings where estimationof group size was difficult to assess were disregarded Whenprimateswere encountered the number of individuals (groupsize) species time GPS (Garmin GPSmap 62) locationand perpendicular distance to primate(s) were recorded Thedistance along transects was measured with a tape measureThe perpendicular ground distance from the transect centerline to an estimated central point directly beneath wherethe primates were initially sighted was also measured usinga tape measure Binoculars were used when necessary toconfirm species identity An index of logging activity per kmwas generated by recording the number of logged trees (treestumps) observed along each transect

23 DataAnalysis Primate densitywas calculated usingDIS-TANCE Version 41 software package [27] The best modelselection was based on the values of Akaikersquos InformationCriterion (AIC) and recommendations by [28] Encounterrates were calculated in the form of Kilometric Indices ofAbundance (KIA) where the number of recorded primatesand indicators of logging incidence are presented accordingto the distance walked during the surveyTheMann-Whitney119880 test was used to test for any significant difference in primateencounter rates between the logged and unlogged strata Pri-mate species richness and diversity for each stratum was cal-culated using EstimateSWin800 Version 800 software pack-age [29] Bootstrap Richness Estimator was used for speciesrichness and Shannon-Weiner index for species diversity

The effect of logging intensity on primate encounter rateswas tested using regression analysis in Canoco version 45[30] Statistical analyses using the program Spatial AnalysisinMacroecology [31] were conducted to correct for normalityand spatial autocorrelation

3 Results

31 Conservation Status of Primates at Kwabre Forest

Six Species of Diurnal PrimatesRolowaymonkey (Cercopithe-cus roloway) white-naped mangabey (Cercocebus lunulatus)Geoffroyrsquos black-and-white colobus (Colobus vellerosus) olivecolobus (Procolobus verus) lesser spot-nosedmonkey (Cerco-pithecus petaurista) and Lowersquosmonkey (Cercopithecus lowei)were recorded in the survey (Table 1)

International Journal of Ecology 3

(km)

Transects

Logged stratum

Kwabre Rainforest

RiversRoadsTowns

5250

N

Alenda Wharf

Anwiafutu

Kofi Gaman

Elubo

Amoakwasuazo

299840099840045

9984000∘W 2

99840099840040

9984000∘W

599840099840010

9984000∘N

599840099840015

9984000∘N

299840099840040

9984000∘W2

99840099840045

9984000∘W

599840099840015

9984000∘N

599840099840010

9984000∘N

Nigeria

Togo

CotedrsquoIvoire

BurkinaFaso

Beni

n

Gha

na

Figure 1 Map of Kwabre Rainforest showing the logged stratum

Rolowaymonkey is listed as an endangered species on theIUCN Threatened Species List white-naped mangabey andGeoffroyrsquos black-and-white colobus are listed as vulnerablespecies and olive colobus is listed as near-threatened species

[10] The spot-nosed monkey and Lowersquos monkey are con-sidered to be of least concern and are of local conservationimportance (Schedule 1) under Ghanaian law (LI 1284-Wildlife Conservation (Amendment) Regulations 1983)

4 International Journal of Ecology

N

(km)201050

Corridor routeInternational boundary

Protected areas

Ankasa Conservation Area

Kwabre Rainforest

RiversRoads

Cote drsquoIvoire Ghana

Nigeria

Togo

Beni

n

Gha

na

BurkinaFaso

CotedrsquoIvoire

Tanoeacute Forest

Figure 2 Map of the proposed transboundary elephant migrationcorridor between Ghana and Ivory Coast

Table 1 IUCN status of primate species found in the KwabreRainforest

Common name Scientific name IUCN statusRoloway monkey Cercopithecus roloway ENWhite-naped mangabey Cercocebus lunulatus VUBlack-and-white colobus Colobus vellerosus VUOlive colobus Procolobus verus NTSpot-nosed monkey Cercopithecus petaurista LCLowersquos monkey Cercopithecus lowei LCEN endangered VU vulnerable NT near threatened LC least concern

32 Primate Diversity Primate species composition variedacross the logged and unlogged strata but was not signifi-cantly different (Mann-Whitney 119880 test 119880 = 360 119901 gt 005)The unlogged stratum was found to be more diverse thanlogged stratum when various richness and diversity indices

Table 2 Primate species diversity index generated by Esti-mateSWin800

Stratum Shannon-Weiner mean Standard deviationLogged 144 022Unlogged 291 016

Table 3 Pooled primate density parameters estimated for the loggedand unlogged strata

Density parameters Loggedstratum

Unloggedstratum

Density (kmminus2) 34993 88368Percent coefficient ofvariation [CV ()] 2239 1064

Upper confidence limit (CL) 20529 68517Lower confidence limit (CL) 59647 113970

were applied to the data (Table 2) Comparably these indiceswere very low in the logged stratum

None of the species were unique to any of the definedlogging categories but the generally higher primate speciesrichness in the unlogged stratum in comparison to loggedstratum may reflect primatesrsquo general adaptation to matureforest systems with taller trees and denser canopy covers

33 Primate Density Primate density was significantly lower(less than 50) in the logged stratum compared to theunlogged stratum (Table 3) The half normal + cosine modelwithout truncation gave the best fit to the data Note that DIS-TANCE produces estimates with asymmetrical confidencelimits

There was also a significant difference in the individualprimate encounter rates (Mann-Whitney 119880 test 119880 = 360119901 lt 001) across the two categories of strata that islogged and unlogged (Table 4) The percentage of individ-ual primates encountered was considerably greater in theunlogged (73) than in logged (27) stratum howeverprimate group sizes for the same species were similar for bothstrata (Table 4) All species apart from the black-and-whitecolobus showed greater densities in the unlogged stratum

34 Relationship between Primate Density and Logging Inten-sity The number of primates encountered was inverselyrelated to logging intensity (1199032 = 0945119901 lt 001)Thehighestencounter rates of primates were observed in slightly loggedor unlogged forests (Figure 3)

4 Discussion

The results suggest that logging could negatively influenceprimate communities through the modification of primatedensity and species composition Therefore the null hypoth-esis of no significant difference in primate density and speciescomposition between logged and unlogged areas is rejectedSuch inference must however be made cautiously as logging

International Journal of Ecology 5

Table4En

coun

terrates

ofprim

ates

andloggingintensity

intheK

wabre

Rainforest

Stratumtr

ansects

Lowersquos

mon

key

Spot-nosed

mon

key

White-naped

mangabey

Roloway

mon

key

Olive

colobu

sBlack-and-white

colobu

sTo

tal

prim

ates

Prim

ates

perk

mLo

ggingintensity

perk

mLo

gged

10(0)

0(0)

0(0)

0(0)

0(0)

0(0)

00

102

1(11)

1(8)

0(0)

0(0)

0(0)

2(65)

309

43

0(0)

1(6)

0(0)

0(0)

1(3)

3(654)

247

34

1(8)

0(0)

1(5)

0(0)

0(0)

1(7)

206

75

2(79)

0(0)

0(0)

0(0)

1(4)

1(6)

267

66

1(6)

0(0)

0(0)

1(6)

1(3)

2(67)

286

5Mean

82

7050

60

33

57

256

7058

Total

4114

56

1052

128

3535

Unlogged

72(129)

1(10)

1(5)

0(0)

2(43)

1(7)

5014

08

3(10911)

2(911)

1(6)

1(6)

1(4)

0(0)

6619

09

1(7)

2(79)

1(3)

0(0)

1(5)

1(5)

3610

010

2(98)

1(8)

1(4)

2(43)

2(33)

2(65)

5315

011

4(118126)

3(869)

0(0)

1(5)

1(4)

1(7)

7622

012

2(68)

3(1197)

2(53)

1(4)

1(3)

1(5)

6117

0Mean

9086

43

44

36

58

570

160

Total

126

104

2622

2935

342

970

Num

bersou

tside

bracketsindicatethen

umbero

fprim

ateg

roup

sand

numbersin

bracketsindicategrou

psiz

esandlogged

trees

perk

m

6 International Journal of Ecology

minus25

0

25

5

75

10

125

15

175

20

225

Num

ber o

f prim

ates

per

km

minus2 0 2 4 6 8 10 12Logging activity per km

Y = 15974 minus 2137 lowast X + 064 lowast X2 R

2= 769

Figure 3 Relationship between encounter rates of primates andlogging intensity

may not be the only factor influencing primate species com-position and density Although both strata possess similartopography and vegetation type logged areas had recentlogging disturbances that resulted in reduced canopy coverand denser understory cover A factor that may have alsoinfluenced our findings could be the proximity of some fringecommunities to the forest edge During the study it wasobserved that logged areas were closer to fringe communitiesand farms making such areas more susceptible to humandisturbances such as poaching [17 32] Some of these differ-ences in human and ecological variables may have influencedour findings One reason that may have accounted for highernumbers of black-and-white colobuses in the logged stratumis that they are folivores [14] and as suchmay show preferencefor degraded areas where the open canopy permits growthof diverse understory Apart from changes in density anddiversity logging might have also affected the behaviour ofprimates [13 20 33] For instance primates exhibited extremeshyness including restricting calls in the logged stratumcompared to the unlogged stratum when teams encounteredprimate groups The apparent differences in the incidence ofalarm calls between groups ofmonkeys encountered betweenthe two strata could affect our census findings to a smallextent However previous studies on primate surveys [14 2434] have shown that many replications are needed at eachtransect before the group density estimates can be consideredreliable In the current study each transect was sampledmorethan once and this could increase the reliability of our results

Our study draws attention to matters of both nationaland international conservation concern The evidence ofunauthorized human activities recorded during this study

indicates clearly that the community-based managementsystem practiced at Kwabre Rainforest may not be effectivein preventing poaching and other illegal human activities inthe forest If current threats continue unabated then rapidpopulation decline of primates is expected in the near future

Given its considerably intact forest cover Ghana is in aposition to implement important forest conservation initia-tives in the subregion [35 36] Within Ghana the generalvicinity of the Kwabre Rainforest is very significant from aregional viewpoint because it constitutes part of a networkof forest reserves in southwestern Ghana which constitutesGhanarsquos portion of the proposed crucial corridor for wildlifebetween the Ankasa Conservation Area in Ghana and theTanoe Forest in Cote drsquoIvoire [9]

In this regional setting the future management of theKwabre corridor could be very important At present farmsand villages are flourishing along theKwabre corridor rapidlyincreasing local human pressure Concerns about the futureof Kwabre corridor are particularly important because inter-est to protect wildlife in the area has waned andKwabre Rain-forest could face a sudden increase in hunting logging andslash-and-burn farming Instead of acting as a communityforest buffer zone and possible faunal corridor between twokey international protected areas (Ankasa ConservationAreain Ghana and Tanoe Forest in neighbouring Cote drsquoIvoireFigure 2) the larger Kwabre corridor area could insteadbecome a major population sink for wildlife [13 37 38] Thiswould reinforce adverse edge effects and genetic isolationof the protected areas increasing the probability of localextinctions of species of conservation interest [39 40]

5 Conclusions and Recommendations

Kwabre Rainforest is an important site where careful wildlifemanagement can support major biodiversity conservationin Ghana hence more effort should be channeled intopreventing further habitat degradation of the larger KwabreRainforest corridor area One possibility would be to grantthe Kwabre Rainforest protected area status under Ghanaianlaw and to manage it under the umbrella of an integratedconservation plan that includes its two adjacent internationalprotected areas Such a plan can be achieved by designatingthe entire area as a biosphere reserve which would permitplanned development outside reserves while affording highprotection for protected areas [41] With effective long-term management this region of southwestern Ghana couldremain one of the most important areas for wildlife in WestAfrica

Competing Interests

The authors declare that there are no competing interestsregarding the publication of this paper

Acknowledgments

Many thanks are due to the traditional head and people ofKwabre

International Journal of Ecology 7

References

[1] B Czech P R Krausman and P K Devers ldquoEconomic asso-ciations among causes of species endangerment in the UnitedStatesrdquo BioScience vol 50 no 7 pp 593ndash601 2000

[2] D S Wilcove C H Mclellan and A P Dobson ldquoHabitatfragmentation in the temperate zonerdquo in Conservation BiologyThe Science of Scarcity and Species Richness M E Soule Ed pp237ndash256 Sinauer Associates Sunderland Mass USA 1998

[3] A G Chiarello ldquoDensity and population size of mammals inremnants of BrazilianAtlantic forestrdquoConservation Biology vol14 no 6 pp 1649ndash1657 2000

[4] RK Laidlaw ldquoEffects of habitat disturbance andprotected areasonmammals of PeninsularMalaysiardquoConservation Biology vol14 no 6 pp 1639ndash1648 2000

[5] M A Lopes and S F Ferrari ldquoEffects of human colonization onthe abundance and diversity of mammals in eastern BrazilianAmazoniardquo Conservation Biology vol 14 no 6 pp 1658ndash16652000

[6] E Carrillo G Wong and N A D Cuaron ldquoMonitoringmammal populations in Costa Rican protected areas underdifferent hunting restrictionsrdquo Conservation Biology vol 14 no6 pp 1580ndash1591 2000

[7] M Conroy and D Nichols ldquoDesigning a study to assessmammalian diversityrdquo in Measuring and Monitoring BiologicalDiversity StandardMethods forMammals DWilson R Cole JNichols R Rudran andM Foster Eds pp 41ndash49 SmithsonianInstitution Press London UK 1996

[8] WAPCA Annual Report West African Primate ConservationAction WAPCA Accra Ghana 2012

[9] D Osei R H Horwich and J M Pittman ldquoFirst sightings ofthe Roloway Monkey (Cercopithecus diana roloway) in Ghanain ten years and the status of other endangered primates inSouthwesternGhanardquoAfrican Primates vol 10 pp 25ndash40 2015

[10] The IUCN Red List ofThreatened Species Version 20152 2015httpwwwiucnredlistorg

[11] W S McGraw and J F Oates ldquoRoloway monkey Cercopithecusdiana roloway (Schreber 1774)rdquo in Primates in Peril TheWorldrsquos Most Endangered Primates 2012ndash2014 C Schwitzer RA Mittermeier A B Rylands et al Eds pp 14ndash16 IUCN SSCPrimate Specialist Group (PSG) International PrimatologicalSociety (IPS) Conservation International (CI) and BristolZoological Society Arlington Va USA 2014

[12] R A Mittermeier J Ratsimbazafy A B Rylands et al ldquoPri-mates in peril the worldrsquos 25 most endangered primates 2006ndash2008rdquo Primate Conservation vol 22 pp 1ndash40 2007

[13] D Swift ldquoThe consequences of logging on primate density anddiversity in Kibale National Park Ugandardquo Bioscience Horizonsvol 5 pp 1ndash6 2012

[14] C A Chapman L J Chapman L Naughton-Treves M JLawes and L R Mcdowell ldquoPredicting folivorous primateabundance validation of a nutritionalmodelrdquoAmerican Journalof Primatology vol 62 no 2 pp 55ndash69 2004

[15] J P Skorupa The effects of selective timber harvesting onrain-forest primates in Kibale Forest Uganda [PhD thesis]University of California Davis Davis Calif USA 1988

[16] T T Struhsaker Ecology of an African Rainforest Logging inKibale and the Conflict between Conservation and ExploitationUniversity Press of Florida Gainesville Fla USA 1997

[17] P Mayor P Perez-Pena M Bowler P E Puertas M Kirklandand R Bodmer ldquoEffects of selective logging on large mammal

populations in a remote indigenous territory in the northernperuvian amazonrdquo Ecology and Society vol 20 no 4 pp 36ndash44 2015

[18] A J Plumptre and V Reynolds ldquoThe effect of selective loggingon the primate populations in the Budongo Forest ReserveUgandardquo Journal of Applied Ecology vol 31 no 4 pp 631ndash6411994

[19] C Mammides M Cords and M K Peters ldquoEffects of habitatdisturbance and food supply on population densities of threeprimate species in theKakamega Forest KenyardquoAfrican Journalof Ecology vol 47 no 1 pp 87ndash96 2009

[20] C Schwitzer L Glatt K A-I Nekaris and J U GanzhornldquoResponses of animals to habitat alteration an overviewfocussing on primatesrdquo Endangered Species Research vol 14 no1 pp 31ndash38 2011

[21] R Rimbach A Link M Heistermann C Gomez-Posada NGalvis and E W Heymann ldquoEffects of logging hunting andforest fragment size on physiological stress levels of two sym-patric ateline primates in Colombiardquo Conservation Physiologyvol 1 no 1 Article ID cot031 pp 1ndash11 2013

[22] R F W Barnes K L Barnes M P T Alers and A Blom ldquoMandetermines the distribution of elephants in the rain forests ofnortheastern Gabonrdquo African Journal of Ecology vol 29 no 1pp 54ndash63 1991

[23] R F W Barnes K Beardsley F Michelmore K L Barnes M PT Alers andA Blom ldquoEstimating forest elephant numberswithdung counts and a geographic information systemrdquo Journal ofWildlife Management vol 61 no 4 pp 1384ndash1393 1997

[24] S A Lahm R F W Barnes K Beardsley and P CervinkaldquoA method for censusing the greater white-nosed monkey innortheastern Gabon using the population density gradient inrelation to roadsrdquo Journal of Tropical Ecology vol 14 no 5 pp629ndash643 1998

[25] L Sebogo and R F W Barnes ldquoAction plan for the manage-ment of trans-frontier elephant conservation corridors in WestAfricardquo Tech Rep IUCNAfESGOuagadougou Burkina Faso2003

[26] J F OatesM Abedi-LarteyW SMcGraw T T Struhsaker andG H Whitesides ldquoExtinction of a West African red colobusmonkeyrdquo Conservation Biology vol 14 no 5 pp 1526ndash15322000

[27] L Thomas J L Laake S Strindberg et al Distance 40 Release1 Research Unit for Wildlife Population Assessment Universityof St Andrews St Andrews Scotland 2002

[28] S T Buckland D R Anderson K P Burnham J L Laake DL Borchers and L Thomas Introduction to Distance SamplingEstimating Abundance of Biological Populations OxfordUniver-sity Press Oxford UK 2001

[29] R K Colewell EstimateS Statistical Estimation of SpeciesRichness and Shared Species from Samples Version 8 2006httppurloclcorgestimates

[30] C J F Ter Braak and P Imilauer Canoco Reference Manual andCanoDraw for Windows Userrsquos Guide Software for CanonicalCommunity Ordination (Version 45) Microcomputer PowerIthaca NY USA 2002

[31] T F L V B Rangel J A FDiniz-Filho and LM Bini ldquoTowardsan integrated computational tool for spatial analysis in macroe-cology and biogeographyrdquo Global Ecology and Biogeographyvol 15 no 4 pp 321ndash327 2006

[32] W F Laurance B M Croes L Tchignoumba et al ldquoImpactsof roads and hunting on central African rainforest mammalsrdquoConservation Biology vol 20 no 4 pp 1251ndash1261 2006

8 International Journal of Ecology

[33] C A Chapman S R Balcomb T R Gillespie J P Skorupa andT T Struhsaker ldquoLong-term effects of logging on African pri-mate communities a 28-year comparison from Kibale NationalPark Ugandardquo Conservation Biology vol 14 no 1 pp 207ndash2172000

[34] S A Lahm and J P Tezi ldquoAssessment of the communities ofmedium-sized and large arboreal and terrestrial mammals inthe Rabi-Toucan region of the Ngove-Ndogo Hunting Domainand southwestern Loango National Parkrdquo Bulletin of the Biolog-ical Society of Washington vol 12 pp 383ndash416 2006

[35] W F Laurance A AlonsoM Lee and P Campbell ldquoChallengesfor forest conservation in Gabon Central Africardquo Futures vol38 no 4 pp 454ndash470 2006

[36] A Kamdem-Toham AW Adeleke N D Burgess et al ldquoForestconservation in the Congo Basinrdquo Science vol 299 no 5605article 346 2003

[37] A J Novaro K H Redford and R E Bodmer ldquoEffect ofhunting in source-sink systems in theNeotropicsrdquoConservationBiology vol 14 no 3 pp 713ndash721 2000

[38] C A Peres ldquoSynergistic effects of subsistence hunting andhabitat fragmentation on amazonian forest vertebratesrdquoConser-vation Biology vol 15 no 6 pp 1490ndash1505 2001

[39] R Woodroffe and J R Ginsberg ldquoEdge effects and the extinc-tion of populations inside protected areasrdquo Science vol 280 no5372 pp 2126ndash2128 1998

[40] W F Laurance T E Lovejoy H L Vasconcelos et alldquoEcosystem decay of Amazonian forest fragments a 22-yearinvestigationrdquo Conservation Biology vol 16 no 3 pp 605ndash6182002

[41] A Kaus ldquoEnvironmental perceptions and social relations in theMapimı Biosphere Reserverdquo Conservation Biology vol 7 no 2pp 398ndash406 1993

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 3: Research Article Logging Activity Adversely Impacts Primate Diversity …downloads.hindawi.com/journals/ijecol/2016/7497326.pdf · 2019-07-30 · Primate Diversity. Primate species

International Journal of Ecology 3

(km)

Transects

Logged stratum

Kwabre Rainforest

RiversRoadsTowns

5250

N

Alenda Wharf

Anwiafutu

Kofi Gaman

Elubo

Amoakwasuazo

299840099840045

9984000∘W 2

99840099840040

9984000∘W

599840099840010

9984000∘N

599840099840015

9984000∘N

299840099840040

9984000∘W2

99840099840045

9984000∘W

599840099840015

9984000∘N

599840099840010

9984000∘N

Nigeria

Togo

CotedrsquoIvoire

BurkinaFaso

Beni

n

Gha

na

Figure 1 Map of Kwabre Rainforest showing the logged stratum

Rolowaymonkey is listed as an endangered species on theIUCN Threatened Species List white-naped mangabey andGeoffroyrsquos black-and-white colobus are listed as vulnerablespecies and olive colobus is listed as near-threatened species

[10] The spot-nosed monkey and Lowersquos monkey are con-sidered to be of least concern and are of local conservationimportance (Schedule 1) under Ghanaian law (LI 1284-Wildlife Conservation (Amendment) Regulations 1983)

4 International Journal of Ecology

N

(km)201050

Corridor routeInternational boundary

Protected areas

Ankasa Conservation Area

Kwabre Rainforest

RiversRoads

Cote drsquoIvoire Ghana

Nigeria

Togo

Beni

n

Gha

na

BurkinaFaso

CotedrsquoIvoire

Tanoeacute Forest

Figure 2 Map of the proposed transboundary elephant migrationcorridor between Ghana and Ivory Coast

Table 1 IUCN status of primate species found in the KwabreRainforest

Common name Scientific name IUCN statusRoloway monkey Cercopithecus roloway ENWhite-naped mangabey Cercocebus lunulatus VUBlack-and-white colobus Colobus vellerosus VUOlive colobus Procolobus verus NTSpot-nosed monkey Cercopithecus petaurista LCLowersquos monkey Cercopithecus lowei LCEN endangered VU vulnerable NT near threatened LC least concern

32 Primate Diversity Primate species composition variedacross the logged and unlogged strata but was not signifi-cantly different (Mann-Whitney 119880 test 119880 = 360 119901 gt 005)The unlogged stratum was found to be more diverse thanlogged stratum when various richness and diversity indices

Table 2 Primate species diversity index generated by Esti-mateSWin800

Stratum Shannon-Weiner mean Standard deviationLogged 144 022Unlogged 291 016

Table 3 Pooled primate density parameters estimated for the loggedand unlogged strata

Density parameters Loggedstratum

Unloggedstratum

Density (kmminus2) 34993 88368Percent coefficient ofvariation [CV ()] 2239 1064

Upper confidence limit (CL) 20529 68517Lower confidence limit (CL) 59647 113970

were applied to the data (Table 2) Comparably these indiceswere very low in the logged stratum

None of the species were unique to any of the definedlogging categories but the generally higher primate speciesrichness in the unlogged stratum in comparison to loggedstratum may reflect primatesrsquo general adaptation to matureforest systems with taller trees and denser canopy covers

33 Primate Density Primate density was significantly lower(less than 50) in the logged stratum compared to theunlogged stratum (Table 3) The half normal + cosine modelwithout truncation gave the best fit to the data Note that DIS-TANCE produces estimates with asymmetrical confidencelimits

There was also a significant difference in the individualprimate encounter rates (Mann-Whitney 119880 test 119880 = 360119901 lt 001) across the two categories of strata that islogged and unlogged (Table 4) The percentage of individ-ual primates encountered was considerably greater in theunlogged (73) than in logged (27) stratum howeverprimate group sizes for the same species were similar for bothstrata (Table 4) All species apart from the black-and-whitecolobus showed greater densities in the unlogged stratum

34 Relationship between Primate Density and Logging Inten-sity The number of primates encountered was inverselyrelated to logging intensity (1199032 = 0945119901 lt 001)Thehighestencounter rates of primates were observed in slightly loggedor unlogged forests (Figure 3)

4 Discussion

The results suggest that logging could negatively influenceprimate communities through the modification of primatedensity and species composition Therefore the null hypoth-esis of no significant difference in primate density and speciescomposition between logged and unlogged areas is rejectedSuch inference must however be made cautiously as logging

International Journal of Ecology 5

Table4En

coun

terrates

ofprim

ates

andloggingintensity

intheK

wabre

Rainforest

Stratumtr

ansects

Lowersquos

mon

key

Spot-nosed

mon

key

White-naped

mangabey

Roloway

mon

key

Olive

colobu

sBlack-and-white

colobu

sTo

tal

prim

ates

Prim

ates

perk

mLo

ggingintensity

perk

mLo

gged

10(0)

0(0)

0(0)

0(0)

0(0)

0(0)

00

102

1(11)

1(8)

0(0)

0(0)

0(0)

2(65)

309

43

0(0)

1(6)

0(0)

0(0)

1(3)

3(654)

247

34

1(8)

0(0)

1(5)

0(0)

0(0)

1(7)

206

75

2(79)

0(0)

0(0)

0(0)

1(4)

1(6)

267

66

1(6)

0(0)

0(0)

1(6)

1(3)

2(67)

286

5Mean

82

7050

60

33

57

256

7058

Total

4114

56

1052

128

3535

Unlogged

72(129)

1(10)

1(5)

0(0)

2(43)

1(7)

5014

08

3(10911)

2(911)

1(6)

1(6)

1(4)

0(0)

6619

09

1(7)

2(79)

1(3)

0(0)

1(5)

1(5)

3610

010

2(98)

1(8)

1(4)

2(43)

2(33)

2(65)

5315

011

4(118126)

3(869)

0(0)

1(5)

1(4)

1(7)

7622

012

2(68)

3(1197)

2(53)

1(4)

1(3)

1(5)

6117

0Mean

9086

43

44

36

58

570

160

Total

126

104

2622

2935

342

970

Num

bersou

tside

bracketsindicatethen

umbero

fprim

ateg

roup

sand

numbersin

bracketsindicategrou

psiz

esandlogged

trees

perk

m

6 International Journal of Ecology

minus25

0

25

5

75

10

125

15

175

20

225

Num

ber o

f prim

ates

per

km

minus2 0 2 4 6 8 10 12Logging activity per km

Y = 15974 minus 2137 lowast X + 064 lowast X2 R

2= 769

Figure 3 Relationship between encounter rates of primates andlogging intensity

may not be the only factor influencing primate species com-position and density Although both strata possess similartopography and vegetation type logged areas had recentlogging disturbances that resulted in reduced canopy coverand denser understory cover A factor that may have alsoinfluenced our findings could be the proximity of some fringecommunities to the forest edge During the study it wasobserved that logged areas were closer to fringe communitiesand farms making such areas more susceptible to humandisturbances such as poaching [17 32] Some of these differ-ences in human and ecological variables may have influencedour findings One reason that may have accounted for highernumbers of black-and-white colobuses in the logged stratumis that they are folivores [14] and as suchmay show preferencefor degraded areas where the open canopy permits growthof diverse understory Apart from changes in density anddiversity logging might have also affected the behaviour ofprimates [13 20 33] For instance primates exhibited extremeshyness including restricting calls in the logged stratumcompared to the unlogged stratum when teams encounteredprimate groups The apparent differences in the incidence ofalarm calls between groups ofmonkeys encountered betweenthe two strata could affect our census findings to a smallextent However previous studies on primate surveys [14 2434] have shown that many replications are needed at eachtransect before the group density estimates can be consideredreliable In the current study each transect was sampledmorethan once and this could increase the reliability of our results

Our study draws attention to matters of both nationaland international conservation concern The evidence ofunauthorized human activities recorded during this study

indicates clearly that the community-based managementsystem practiced at Kwabre Rainforest may not be effectivein preventing poaching and other illegal human activities inthe forest If current threats continue unabated then rapidpopulation decline of primates is expected in the near future

Given its considerably intact forest cover Ghana is in aposition to implement important forest conservation initia-tives in the subregion [35 36] Within Ghana the generalvicinity of the Kwabre Rainforest is very significant from aregional viewpoint because it constitutes part of a networkof forest reserves in southwestern Ghana which constitutesGhanarsquos portion of the proposed crucial corridor for wildlifebetween the Ankasa Conservation Area in Ghana and theTanoe Forest in Cote drsquoIvoire [9]

In this regional setting the future management of theKwabre corridor could be very important At present farmsand villages are flourishing along theKwabre corridor rapidlyincreasing local human pressure Concerns about the futureof Kwabre corridor are particularly important because inter-est to protect wildlife in the area has waned andKwabre Rain-forest could face a sudden increase in hunting logging andslash-and-burn farming Instead of acting as a communityforest buffer zone and possible faunal corridor between twokey international protected areas (Ankasa ConservationAreain Ghana and Tanoe Forest in neighbouring Cote drsquoIvoireFigure 2) the larger Kwabre corridor area could insteadbecome a major population sink for wildlife [13 37 38] Thiswould reinforce adverse edge effects and genetic isolationof the protected areas increasing the probability of localextinctions of species of conservation interest [39 40]

5 Conclusions and Recommendations

Kwabre Rainforest is an important site where careful wildlifemanagement can support major biodiversity conservationin Ghana hence more effort should be channeled intopreventing further habitat degradation of the larger KwabreRainforest corridor area One possibility would be to grantthe Kwabre Rainforest protected area status under Ghanaianlaw and to manage it under the umbrella of an integratedconservation plan that includes its two adjacent internationalprotected areas Such a plan can be achieved by designatingthe entire area as a biosphere reserve which would permitplanned development outside reserves while affording highprotection for protected areas [41] With effective long-term management this region of southwestern Ghana couldremain one of the most important areas for wildlife in WestAfrica

Competing Interests

The authors declare that there are no competing interestsregarding the publication of this paper

Acknowledgments

Many thanks are due to the traditional head and people ofKwabre

International Journal of Ecology 7

References

[1] B Czech P R Krausman and P K Devers ldquoEconomic asso-ciations among causes of species endangerment in the UnitedStatesrdquo BioScience vol 50 no 7 pp 593ndash601 2000

[2] D S Wilcove C H Mclellan and A P Dobson ldquoHabitatfragmentation in the temperate zonerdquo in Conservation BiologyThe Science of Scarcity and Species Richness M E Soule Ed pp237ndash256 Sinauer Associates Sunderland Mass USA 1998

[3] A G Chiarello ldquoDensity and population size of mammals inremnants of BrazilianAtlantic forestrdquoConservation Biology vol14 no 6 pp 1649ndash1657 2000

[4] RK Laidlaw ldquoEffects of habitat disturbance andprotected areasonmammals of PeninsularMalaysiardquoConservation Biology vol14 no 6 pp 1639ndash1648 2000

[5] M A Lopes and S F Ferrari ldquoEffects of human colonization onthe abundance and diversity of mammals in eastern BrazilianAmazoniardquo Conservation Biology vol 14 no 6 pp 1658ndash16652000

[6] E Carrillo G Wong and N A D Cuaron ldquoMonitoringmammal populations in Costa Rican protected areas underdifferent hunting restrictionsrdquo Conservation Biology vol 14 no6 pp 1580ndash1591 2000

[7] M Conroy and D Nichols ldquoDesigning a study to assessmammalian diversityrdquo in Measuring and Monitoring BiologicalDiversity StandardMethods forMammals DWilson R Cole JNichols R Rudran andM Foster Eds pp 41ndash49 SmithsonianInstitution Press London UK 1996

[8] WAPCA Annual Report West African Primate ConservationAction WAPCA Accra Ghana 2012

[9] D Osei R H Horwich and J M Pittman ldquoFirst sightings ofthe Roloway Monkey (Cercopithecus diana roloway) in Ghanain ten years and the status of other endangered primates inSouthwesternGhanardquoAfrican Primates vol 10 pp 25ndash40 2015

[10] The IUCN Red List ofThreatened Species Version 20152 2015httpwwwiucnredlistorg

[11] W S McGraw and J F Oates ldquoRoloway monkey Cercopithecusdiana roloway (Schreber 1774)rdquo in Primates in Peril TheWorldrsquos Most Endangered Primates 2012ndash2014 C Schwitzer RA Mittermeier A B Rylands et al Eds pp 14ndash16 IUCN SSCPrimate Specialist Group (PSG) International PrimatologicalSociety (IPS) Conservation International (CI) and BristolZoological Society Arlington Va USA 2014

[12] R A Mittermeier J Ratsimbazafy A B Rylands et al ldquoPri-mates in peril the worldrsquos 25 most endangered primates 2006ndash2008rdquo Primate Conservation vol 22 pp 1ndash40 2007

[13] D Swift ldquoThe consequences of logging on primate density anddiversity in Kibale National Park Ugandardquo Bioscience Horizonsvol 5 pp 1ndash6 2012

[14] C A Chapman L J Chapman L Naughton-Treves M JLawes and L R Mcdowell ldquoPredicting folivorous primateabundance validation of a nutritionalmodelrdquoAmerican Journalof Primatology vol 62 no 2 pp 55ndash69 2004

[15] J P Skorupa The effects of selective timber harvesting onrain-forest primates in Kibale Forest Uganda [PhD thesis]University of California Davis Davis Calif USA 1988

[16] T T Struhsaker Ecology of an African Rainforest Logging inKibale and the Conflict between Conservation and ExploitationUniversity Press of Florida Gainesville Fla USA 1997

[17] P Mayor P Perez-Pena M Bowler P E Puertas M Kirklandand R Bodmer ldquoEffects of selective logging on large mammal

populations in a remote indigenous territory in the northernperuvian amazonrdquo Ecology and Society vol 20 no 4 pp 36ndash44 2015

[18] A J Plumptre and V Reynolds ldquoThe effect of selective loggingon the primate populations in the Budongo Forest ReserveUgandardquo Journal of Applied Ecology vol 31 no 4 pp 631ndash6411994

[19] C Mammides M Cords and M K Peters ldquoEffects of habitatdisturbance and food supply on population densities of threeprimate species in theKakamega Forest KenyardquoAfrican Journalof Ecology vol 47 no 1 pp 87ndash96 2009

[20] C Schwitzer L Glatt K A-I Nekaris and J U GanzhornldquoResponses of animals to habitat alteration an overviewfocussing on primatesrdquo Endangered Species Research vol 14 no1 pp 31ndash38 2011

[21] R Rimbach A Link M Heistermann C Gomez-Posada NGalvis and E W Heymann ldquoEffects of logging hunting andforest fragment size on physiological stress levels of two sym-patric ateline primates in Colombiardquo Conservation Physiologyvol 1 no 1 Article ID cot031 pp 1ndash11 2013

[22] R F W Barnes K L Barnes M P T Alers and A Blom ldquoMandetermines the distribution of elephants in the rain forests ofnortheastern Gabonrdquo African Journal of Ecology vol 29 no 1pp 54ndash63 1991

[23] R F W Barnes K Beardsley F Michelmore K L Barnes M PT Alers andA Blom ldquoEstimating forest elephant numberswithdung counts and a geographic information systemrdquo Journal ofWildlife Management vol 61 no 4 pp 1384ndash1393 1997

[24] S A Lahm R F W Barnes K Beardsley and P CervinkaldquoA method for censusing the greater white-nosed monkey innortheastern Gabon using the population density gradient inrelation to roadsrdquo Journal of Tropical Ecology vol 14 no 5 pp629ndash643 1998

[25] L Sebogo and R F W Barnes ldquoAction plan for the manage-ment of trans-frontier elephant conservation corridors in WestAfricardquo Tech Rep IUCNAfESGOuagadougou Burkina Faso2003

[26] J F OatesM Abedi-LarteyW SMcGraw T T Struhsaker andG H Whitesides ldquoExtinction of a West African red colobusmonkeyrdquo Conservation Biology vol 14 no 5 pp 1526ndash15322000

[27] L Thomas J L Laake S Strindberg et al Distance 40 Release1 Research Unit for Wildlife Population Assessment Universityof St Andrews St Andrews Scotland 2002

[28] S T Buckland D R Anderson K P Burnham J L Laake DL Borchers and L Thomas Introduction to Distance SamplingEstimating Abundance of Biological Populations OxfordUniver-sity Press Oxford UK 2001

[29] R K Colewell EstimateS Statistical Estimation of SpeciesRichness and Shared Species from Samples Version 8 2006httppurloclcorgestimates

[30] C J F Ter Braak and P Imilauer Canoco Reference Manual andCanoDraw for Windows Userrsquos Guide Software for CanonicalCommunity Ordination (Version 45) Microcomputer PowerIthaca NY USA 2002

[31] T F L V B Rangel J A FDiniz-Filho and LM Bini ldquoTowardsan integrated computational tool for spatial analysis in macroe-cology and biogeographyrdquo Global Ecology and Biogeographyvol 15 no 4 pp 321ndash327 2006

[32] W F Laurance B M Croes L Tchignoumba et al ldquoImpactsof roads and hunting on central African rainforest mammalsrdquoConservation Biology vol 20 no 4 pp 1251ndash1261 2006

8 International Journal of Ecology

[33] C A Chapman S R Balcomb T R Gillespie J P Skorupa andT T Struhsaker ldquoLong-term effects of logging on African pri-mate communities a 28-year comparison from Kibale NationalPark Ugandardquo Conservation Biology vol 14 no 1 pp 207ndash2172000

[34] S A Lahm and J P Tezi ldquoAssessment of the communities ofmedium-sized and large arboreal and terrestrial mammals inthe Rabi-Toucan region of the Ngove-Ndogo Hunting Domainand southwestern Loango National Parkrdquo Bulletin of the Biolog-ical Society of Washington vol 12 pp 383ndash416 2006

[35] W F Laurance A AlonsoM Lee and P Campbell ldquoChallengesfor forest conservation in Gabon Central Africardquo Futures vol38 no 4 pp 454ndash470 2006

[36] A Kamdem-Toham AW Adeleke N D Burgess et al ldquoForestconservation in the Congo Basinrdquo Science vol 299 no 5605article 346 2003

[37] A J Novaro K H Redford and R E Bodmer ldquoEffect ofhunting in source-sink systems in theNeotropicsrdquoConservationBiology vol 14 no 3 pp 713ndash721 2000

[38] C A Peres ldquoSynergistic effects of subsistence hunting andhabitat fragmentation on amazonian forest vertebratesrdquoConser-vation Biology vol 15 no 6 pp 1490ndash1505 2001

[39] R Woodroffe and J R Ginsberg ldquoEdge effects and the extinc-tion of populations inside protected areasrdquo Science vol 280 no5372 pp 2126ndash2128 1998

[40] W F Laurance T E Lovejoy H L Vasconcelos et alldquoEcosystem decay of Amazonian forest fragments a 22-yearinvestigationrdquo Conservation Biology vol 16 no 3 pp 605ndash6182002

[41] A Kaus ldquoEnvironmental perceptions and social relations in theMapimı Biosphere Reserverdquo Conservation Biology vol 7 no 2pp 398ndash406 1993

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 4: Research Article Logging Activity Adversely Impacts Primate Diversity …downloads.hindawi.com/journals/ijecol/2016/7497326.pdf · 2019-07-30 · Primate Diversity. Primate species

4 International Journal of Ecology

N

(km)201050

Corridor routeInternational boundary

Protected areas

Ankasa Conservation Area

Kwabre Rainforest

RiversRoads

Cote drsquoIvoire Ghana

Nigeria

Togo

Beni

n

Gha

na

BurkinaFaso

CotedrsquoIvoire

Tanoeacute Forest

Figure 2 Map of the proposed transboundary elephant migrationcorridor between Ghana and Ivory Coast

Table 1 IUCN status of primate species found in the KwabreRainforest

Common name Scientific name IUCN statusRoloway monkey Cercopithecus roloway ENWhite-naped mangabey Cercocebus lunulatus VUBlack-and-white colobus Colobus vellerosus VUOlive colobus Procolobus verus NTSpot-nosed monkey Cercopithecus petaurista LCLowersquos monkey Cercopithecus lowei LCEN endangered VU vulnerable NT near threatened LC least concern

32 Primate Diversity Primate species composition variedacross the logged and unlogged strata but was not signifi-cantly different (Mann-Whitney 119880 test 119880 = 360 119901 gt 005)The unlogged stratum was found to be more diverse thanlogged stratum when various richness and diversity indices

Table 2 Primate species diversity index generated by Esti-mateSWin800

Stratum Shannon-Weiner mean Standard deviationLogged 144 022Unlogged 291 016

Table 3 Pooled primate density parameters estimated for the loggedand unlogged strata

Density parameters Loggedstratum

Unloggedstratum

Density (kmminus2) 34993 88368Percent coefficient ofvariation [CV ()] 2239 1064

Upper confidence limit (CL) 20529 68517Lower confidence limit (CL) 59647 113970

were applied to the data (Table 2) Comparably these indiceswere very low in the logged stratum

None of the species were unique to any of the definedlogging categories but the generally higher primate speciesrichness in the unlogged stratum in comparison to loggedstratum may reflect primatesrsquo general adaptation to matureforest systems with taller trees and denser canopy covers

33 Primate Density Primate density was significantly lower(less than 50) in the logged stratum compared to theunlogged stratum (Table 3) The half normal + cosine modelwithout truncation gave the best fit to the data Note that DIS-TANCE produces estimates with asymmetrical confidencelimits

There was also a significant difference in the individualprimate encounter rates (Mann-Whitney 119880 test 119880 = 360119901 lt 001) across the two categories of strata that islogged and unlogged (Table 4) The percentage of individ-ual primates encountered was considerably greater in theunlogged (73) than in logged (27) stratum howeverprimate group sizes for the same species were similar for bothstrata (Table 4) All species apart from the black-and-whitecolobus showed greater densities in the unlogged stratum

34 Relationship between Primate Density and Logging Inten-sity The number of primates encountered was inverselyrelated to logging intensity (1199032 = 0945119901 lt 001)Thehighestencounter rates of primates were observed in slightly loggedor unlogged forests (Figure 3)

4 Discussion

The results suggest that logging could negatively influenceprimate communities through the modification of primatedensity and species composition Therefore the null hypoth-esis of no significant difference in primate density and speciescomposition between logged and unlogged areas is rejectedSuch inference must however be made cautiously as logging

International Journal of Ecology 5

Table4En

coun

terrates

ofprim

ates

andloggingintensity

intheK

wabre

Rainforest

Stratumtr

ansects

Lowersquos

mon

key

Spot-nosed

mon

key

White-naped

mangabey

Roloway

mon

key

Olive

colobu

sBlack-and-white

colobu

sTo

tal

prim

ates

Prim

ates

perk

mLo

ggingintensity

perk

mLo

gged

10(0)

0(0)

0(0)

0(0)

0(0)

0(0)

00

102

1(11)

1(8)

0(0)

0(0)

0(0)

2(65)

309

43

0(0)

1(6)

0(0)

0(0)

1(3)

3(654)

247

34

1(8)

0(0)

1(5)

0(0)

0(0)

1(7)

206

75

2(79)

0(0)

0(0)

0(0)

1(4)

1(6)

267

66

1(6)

0(0)

0(0)

1(6)

1(3)

2(67)

286

5Mean

82

7050

60

33

57

256

7058

Total

4114

56

1052

128

3535

Unlogged

72(129)

1(10)

1(5)

0(0)

2(43)

1(7)

5014

08

3(10911)

2(911)

1(6)

1(6)

1(4)

0(0)

6619

09

1(7)

2(79)

1(3)

0(0)

1(5)

1(5)

3610

010

2(98)

1(8)

1(4)

2(43)

2(33)

2(65)

5315

011

4(118126)

3(869)

0(0)

1(5)

1(4)

1(7)

7622

012

2(68)

3(1197)

2(53)

1(4)

1(3)

1(5)

6117

0Mean

9086

43

44

36

58

570

160

Total

126

104

2622

2935

342

970

Num

bersou

tside

bracketsindicatethen

umbero

fprim

ateg

roup

sand

numbersin

bracketsindicategrou

psiz

esandlogged

trees

perk

m

6 International Journal of Ecology

minus25

0

25

5

75

10

125

15

175

20

225

Num

ber o

f prim

ates

per

km

minus2 0 2 4 6 8 10 12Logging activity per km

Y = 15974 minus 2137 lowast X + 064 lowast X2 R

2= 769

Figure 3 Relationship between encounter rates of primates andlogging intensity

may not be the only factor influencing primate species com-position and density Although both strata possess similartopography and vegetation type logged areas had recentlogging disturbances that resulted in reduced canopy coverand denser understory cover A factor that may have alsoinfluenced our findings could be the proximity of some fringecommunities to the forest edge During the study it wasobserved that logged areas were closer to fringe communitiesand farms making such areas more susceptible to humandisturbances such as poaching [17 32] Some of these differ-ences in human and ecological variables may have influencedour findings One reason that may have accounted for highernumbers of black-and-white colobuses in the logged stratumis that they are folivores [14] and as suchmay show preferencefor degraded areas where the open canopy permits growthof diverse understory Apart from changes in density anddiversity logging might have also affected the behaviour ofprimates [13 20 33] For instance primates exhibited extremeshyness including restricting calls in the logged stratumcompared to the unlogged stratum when teams encounteredprimate groups The apparent differences in the incidence ofalarm calls between groups ofmonkeys encountered betweenthe two strata could affect our census findings to a smallextent However previous studies on primate surveys [14 2434] have shown that many replications are needed at eachtransect before the group density estimates can be consideredreliable In the current study each transect was sampledmorethan once and this could increase the reliability of our results

Our study draws attention to matters of both nationaland international conservation concern The evidence ofunauthorized human activities recorded during this study

indicates clearly that the community-based managementsystem practiced at Kwabre Rainforest may not be effectivein preventing poaching and other illegal human activities inthe forest If current threats continue unabated then rapidpopulation decline of primates is expected in the near future

Given its considerably intact forest cover Ghana is in aposition to implement important forest conservation initia-tives in the subregion [35 36] Within Ghana the generalvicinity of the Kwabre Rainforest is very significant from aregional viewpoint because it constitutes part of a networkof forest reserves in southwestern Ghana which constitutesGhanarsquos portion of the proposed crucial corridor for wildlifebetween the Ankasa Conservation Area in Ghana and theTanoe Forest in Cote drsquoIvoire [9]

In this regional setting the future management of theKwabre corridor could be very important At present farmsand villages are flourishing along theKwabre corridor rapidlyincreasing local human pressure Concerns about the futureof Kwabre corridor are particularly important because inter-est to protect wildlife in the area has waned andKwabre Rain-forest could face a sudden increase in hunting logging andslash-and-burn farming Instead of acting as a communityforest buffer zone and possible faunal corridor between twokey international protected areas (Ankasa ConservationAreain Ghana and Tanoe Forest in neighbouring Cote drsquoIvoireFigure 2) the larger Kwabre corridor area could insteadbecome a major population sink for wildlife [13 37 38] Thiswould reinforce adverse edge effects and genetic isolationof the protected areas increasing the probability of localextinctions of species of conservation interest [39 40]

5 Conclusions and Recommendations

Kwabre Rainforest is an important site where careful wildlifemanagement can support major biodiversity conservationin Ghana hence more effort should be channeled intopreventing further habitat degradation of the larger KwabreRainforest corridor area One possibility would be to grantthe Kwabre Rainforest protected area status under Ghanaianlaw and to manage it under the umbrella of an integratedconservation plan that includes its two adjacent internationalprotected areas Such a plan can be achieved by designatingthe entire area as a biosphere reserve which would permitplanned development outside reserves while affording highprotection for protected areas [41] With effective long-term management this region of southwestern Ghana couldremain one of the most important areas for wildlife in WestAfrica

Competing Interests

The authors declare that there are no competing interestsregarding the publication of this paper

Acknowledgments

Many thanks are due to the traditional head and people ofKwabre

International Journal of Ecology 7

References

[1] B Czech P R Krausman and P K Devers ldquoEconomic asso-ciations among causes of species endangerment in the UnitedStatesrdquo BioScience vol 50 no 7 pp 593ndash601 2000

[2] D S Wilcove C H Mclellan and A P Dobson ldquoHabitatfragmentation in the temperate zonerdquo in Conservation BiologyThe Science of Scarcity and Species Richness M E Soule Ed pp237ndash256 Sinauer Associates Sunderland Mass USA 1998

[3] A G Chiarello ldquoDensity and population size of mammals inremnants of BrazilianAtlantic forestrdquoConservation Biology vol14 no 6 pp 1649ndash1657 2000

[4] RK Laidlaw ldquoEffects of habitat disturbance andprotected areasonmammals of PeninsularMalaysiardquoConservation Biology vol14 no 6 pp 1639ndash1648 2000

[5] M A Lopes and S F Ferrari ldquoEffects of human colonization onthe abundance and diversity of mammals in eastern BrazilianAmazoniardquo Conservation Biology vol 14 no 6 pp 1658ndash16652000

[6] E Carrillo G Wong and N A D Cuaron ldquoMonitoringmammal populations in Costa Rican protected areas underdifferent hunting restrictionsrdquo Conservation Biology vol 14 no6 pp 1580ndash1591 2000

[7] M Conroy and D Nichols ldquoDesigning a study to assessmammalian diversityrdquo in Measuring and Monitoring BiologicalDiversity StandardMethods forMammals DWilson R Cole JNichols R Rudran andM Foster Eds pp 41ndash49 SmithsonianInstitution Press London UK 1996

[8] WAPCA Annual Report West African Primate ConservationAction WAPCA Accra Ghana 2012

[9] D Osei R H Horwich and J M Pittman ldquoFirst sightings ofthe Roloway Monkey (Cercopithecus diana roloway) in Ghanain ten years and the status of other endangered primates inSouthwesternGhanardquoAfrican Primates vol 10 pp 25ndash40 2015

[10] The IUCN Red List ofThreatened Species Version 20152 2015httpwwwiucnredlistorg

[11] W S McGraw and J F Oates ldquoRoloway monkey Cercopithecusdiana roloway (Schreber 1774)rdquo in Primates in Peril TheWorldrsquos Most Endangered Primates 2012ndash2014 C Schwitzer RA Mittermeier A B Rylands et al Eds pp 14ndash16 IUCN SSCPrimate Specialist Group (PSG) International PrimatologicalSociety (IPS) Conservation International (CI) and BristolZoological Society Arlington Va USA 2014

[12] R A Mittermeier J Ratsimbazafy A B Rylands et al ldquoPri-mates in peril the worldrsquos 25 most endangered primates 2006ndash2008rdquo Primate Conservation vol 22 pp 1ndash40 2007

[13] D Swift ldquoThe consequences of logging on primate density anddiversity in Kibale National Park Ugandardquo Bioscience Horizonsvol 5 pp 1ndash6 2012

[14] C A Chapman L J Chapman L Naughton-Treves M JLawes and L R Mcdowell ldquoPredicting folivorous primateabundance validation of a nutritionalmodelrdquoAmerican Journalof Primatology vol 62 no 2 pp 55ndash69 2004

[15] J P Skorupa The effects of selective timber harvesting onrain-forest primates in Kibale Forest Uganda [PhD thesis]University of California Davis Davis Calif USA 1988

[16] T T Struhsaker Ecology of an African Rainforest Logging inKibale and the Conflict between Conservation and ExploitationUniversity Press of Florida Gainesville Fla USA 1997

[17] P Mayor P Perez-Pena M Bowler P E Puertas M Kirklandand R Bodmer ldquoEffects of selective logging on large mammal

populations in a remote indigenous territory in the northernperuvian amazonrdquo Ecology and Society vol 20 no 4 pp 36ndash44 2015

[18] A J Plumptre and V Reynolds ldquoThe effect of selective loggingon the primate populations in the Budongo Forest ReserveUgandardquo Journal of Applied Ecology vol 31 no 4 pp 631ndash6411994

[19] C Mammides M Cords and M K Peters ldquoEffects of habitatdisturbance and food supply on population densities of threeprimate species in theKakamega Forest KenyardquoAfrican Journalof Ecology vol 47 no 1 pp 87ndash96 2009

[20] C Schwitzer L Glatt K A-I Nekaris and J U GanzhornldquoResponses of animals to habitat alteration an overviewfocussing on primatesrdquo Endangered Species Research vol 14 no1 pp 31ndash38 2011

[21] R Rimbach A Link M Heistermann C Gomez-Posada NGalvis and E W Heymann ldquoEffects of logging hunting andforest fragment size on physiological stress levels of two sym-patric ateline primates in Colombiardquo Conservation Physiologyvol 1 no 1 Article ID cot031 pp 1ndash11 2013

[22] R F W Barnes K L Barnes M P T Alers and A Blom ldquoMandetermines the distribution of elephants in the rain forests ofnortheastern Gabonrdquo African Journal of Ecology vol 29 no 1pp 54ndash63 1991

[23] R F W Barnes K Beardsley F Michelmore K L Barnes M PT Alers andA Blom ldquoEstimating forest elephant numberswithdung counts and a geographic information systemrdquo Journal ofWildlife Management vol 61 no 4 pp 1384ndash1393 1997

[24] S A Lahm R F W Barnes K Beardsley and P CervinkaldquoA method for censusing the greater white-nosed monkey innortheastern Gabon using the population density gradient inrelation to roadsrdquo Journal of Tropical Ecology vol 14 no 5 pp629ndash643 1998

[25] L Sebogo and R F W Barnes ldquoAction plan for the manage-ment of trans-frontier elephant conservation corridors in WestAfricardquo Tech Rep IUCNAfESGOuagadougou Burkina Faso2003

[26] J F OatesM Abedi-LarteyW SMcGraw T T Struhsaker andG H Whitesides ldquoExtinction of a West African red colobusmonkeyrdquo Conservation Biology vol 14 no 5 pp 1526ndash15322000

[27] L Thomas J L Laake S Strindberg et al Distance 40 Release1 Research Unit for Wildlife Population Assessment Universityof St Andrews St Andrews Scotland 2002

[28] S T Buckland D R Anderson K P Burnham J L Laake DL Borchers and L Thomas Introduction to Distance SamplingEstimating Abundance of Biological Populations OxfordUniver-sity Press Oxford UK 2001

[29] R K Colewell EstimateS Statistical Estimation of SpeciesRichness and Shared Species from Samples Version 8 2006httppurloclcorgestimates

[30] C J F Ter Braak and P Imilauer Canoco Reference Manual andCanoDraw for Windows Userrsquos Guide Software for CanonicalCommunity Ordination (Version 45) Microcomputer PowerIthaca NY USA 2002

[31] T F L V B Rangel J A FDiniz-Filho and LM Bini ldquoTowardsan integrated computational tool for spatial analysis in macroe-cology and biogeographyrdquo Global Ecology and Biogeographyvol 15 no 4 pp 321ndash327 2006

[32] W F Laurance B M Croes L Tchignoumba et al ldquoImpactsof roads and hunting on central African rainforest mammalsrdquoConservation Biology vol 20 no 4 pp 1251ndash1261 2006

8 International Journal of Ecology

[33] C A Chapman S R Balcomb T R Gillespie J P Skorupa andT T Struhsaker ldquoLong-term effects of logging on African pri-mate communities a 28-year comparison from Kibale NationalPark Ugandardquo Conservation Biology vol 14 no 1 pp 207ndash2172000

[34] S A Lahm and J P Tezi ldquoAssessment of the communities ofmedium-sized and large arboreal and terrestrial mammals inthe Rabi-Toucan region of the Ngove-Ndogo Hunting Domainand southwestern Loango National Parkrdquo Bulletin of the Biolog-ical Society of Washington vol 12 pp 383ndash416 2006

[35] W F Laurance A AlonsoM Lee and P Campbell ldquoChallengesfor forest conservation in Gabon Central Africardquo Futures vol38 no 4 pp 454ndash470 2006

[36] A Kamdem-Toham AW Adeleke N D Burgess et al ldquoForestconservation in the Congo Basinrdquo Science vol 299 no 5605article 346 2003

[37] A J Novaro K H Redford and R E Bodmer ldquoEffect ofhunting in source-sink systems in theNeotropicsrdquoConservationBiology vol 14 no 3 pp 713ndash721 2000

[38] C A Peres ldquoSynergistic effects of subsistence hunting andhabitat fragmentation on amazonian forest vertebratesrdquoConser-vation Biology vol 15 no 6 pp 1490ndash1505 2001

[39] R Woodroffe and J R Ginsberg ldquoEdge effects and the extinc-tion of populations inside protected areasrdquo Science vol 280 no5372 pp 2126ndash2128 1998

[40] W F Laurance T E Lovejoy H L Vasconcelos et alldquoEcosystem decay of Amazonian forest fragments a 22-yearinvestigationrdquo Conservation Biology vol 16 no 3 pp 605ndash6182002

[41] A Kaus ldquoEnvironmental perceptions and social relations in theMapimı Biosphere Reserverdquo Conservation Biology vol 7 no 2pp 398ndash406 1993

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 5: Research Article Logging Activity Adversely Impacts Primate Diversity …downloads.hindawi.com/journals/ijecol/2016/7497326.pdf · 2019-07-30 · Primate Diversity. Primate species

International Journal of Ecology 5

Table4En

coun

terrates

ofprim

ates

andloggingintensity

intheK

wabre

Rainforest

Stratumtr

ansects

Lowersquos

mon

key

Spot-nosed

mon

key

White-naped

mangabey

Roloway

mon

key

Olive

colobu

sBlack-and-white

colobu

sTo

tal

prim

ates

Prim

ates

perk

mLo

ggingintensity

perk

mLo

gged

10(0)

0(0)

0(0)

0(0)

0(0)

0(0)

00

102

1(11)

1(8)

0(0)

0(0)

0(0)

2(65)

309

43

0(0)

1(6)

0(0)

0(0)

1(3)

3(654)

247

34

1(8)

0(0)

1(5)

0(0)

0(0)

1(7)

206

75

2(79)

0(0)

0(0)

0(0)

1(4)

1(6)

267

66

1(6)

0(0)

0(0)

1(6)

1(3)

2(67)

286

5Mean

82

7050

60

33

57

256

7058

Total

4114

56

1052

128

3535

Unlogged

72(129)

1(10)

1(5)

0(0)

2(43)

1(7)

5014

08

3(10911)

2(911)

1(6)

1(6)

1(4)

0(0)

6619

09

1(7)

2(79)

1(3)

0(0)

1(5)

1(5)

3610

010

2(98)

1(8)

1(4)

2(43)

2(33)

2(65)

5315

011

4(118126)

3(869)

0(0)

1(5)

1(4)

1(7)

7622

012

2(68)

3(1197)

2(53)

1(4)

1(3)

1(5)

6117

0Mean

9086

43

44

36

58

570

160

Total

126

104

2622

2935

342

970

Num

bersou

tside

bracketsindicatethen

umbero

fprim

ateg

roup

sand

numbersin

bracketsindicategrou

psiz

esandlogged

trees

perk

m

6 International Journal of Ecology

minus25

0

25

5

75

10

125

15

175

20

225

Num

ber o

f prim

ates

per

km

minus2 0 2 4 6 8 10 12Logging activity per km

Y = 15974 minus 2137 lowast X + 064 lowast X2 R

2= 769

Figure 3 Relationship between encounter rates of primates andlogging intensity

may not be the only factor influencing primate species com-position and density Although both strata possess similartopography and vegetation type logged areas had recentlogging disturbances that resulted in reduced canopy coverand denser understory cover A factor that may have alsoinfluenced our findings could be the proximity of some fringecommunities to the forest edge During the study it wasobserved that logged areas were closer to fringe communitiesand farms making such areas more susceptible to humandisturbances such as poaching [17 32] Some of these differ-ences in human and ecological variables may have influencedour findings One reason that may have accounted for highernumbers of black-and-white colobuses in the logged stratumis that they are folivores [14] and as suchmay show preferencefor degraded areas where the open canopy permits growthof diverse understory Apart from changes in density anddiversity logging might have also affected the behaviour ofprimates [13 20 33] For instance primates exhibited extremeshyness including restricting calls in the logged stratumcompared to the unlogged stratum when teams encounteredprimate groups The apparent differences in the incidence ofalarm calls between groups ofmonkeys encountered betweenthe two strata could affect our census findings to a smallextent However previous studies on primate surveys [14 2434] have shown that many replications are needed at eachtransect before the group density estimates can be consideredreliable In the current study each transect was sampledmorethan once and this could increase the reliability of our results

Our study draws attention to matters of both nationaland international conservation concern The evidence ofunauthorized human activities recorded during this study

indicates clearly that the community-based managementsystem practiced at Kwabre Rainforest may not be effectivein preventing poaching and other illegal human activities inthe forest If current threats continue unabated then rapidpopulation decline of primates is expected in the near future

Given its considerably intact forest cover Ghana is in aposition to implement important forest conservation initia-tives in the subregion [35 36] Within Ghana the generalvicinity of the Kwabre Rainforest is very significant from aregional viewpoint because it constitutes part of a networkof forest reserves in southwestern Ghana which constitutesGhanarsquos portion of the proposed crucial corridor for wildlifebetween the Ankasa Conservation Area in Ghana and theTanoe Forest in Cote drsquoIvoire [9]

In this regional setting the future management of theKwabre corridor could be very important At present farmsand villages are flourishing along theKwabre corridor rapidlyincreasing local human pressure Concerns about the futureof Kwabre corridor are particularly important because inter-est to protect wildlife in the area has waned andKwabre Rain-forest could face a sudden increase in hunting logging andslash-and-burn farming Instead of acting as a communityforest buffer zone and possible faunal corridor between twokey international protected areas (Ankasa ConservationAreain Ghana and Tanoe Forest in neighbouring Cote drsquoIvoireFigure 2) the larger Kwabre corridor area could insteadbecome a major population sink for wildlife [13 37 38] Thiswould reinforce adverse edge effects and genetic isolationof the protected areas increasing the probability of localextinctions of species of conservation interest [39 40]

5 Conclusions and Recommendations

Kwabre Rainforest is an important site where careful wildlifemanagement can support major biodiversity conservationin Ghana hence more effort should be channeled intopreventing further habitat degradation of the larger KwabreRainforest corridor area One possibility would be to grantthe Kwabre Rainforest protected area status under Ghanaianlaw and to manage it under the umbrella of an integratedconservation plan that includes its two adjacent internationalprotected areas Such a plan can be achieved by designatingthe entire area as a biosphere reserve which would permitplanned development outside reserves while affording highprotection for protected areas [41] With effective long-term management this region of southwestern Ghana couldremain one of the most important areas for wildlife in WestAfrica

Competing Interests

The authors declare that there are no competing interestsregarding the publication of this paper

Acknowledgments

Many thanks are due to the traditional head and people ofKwabre

International Journal of Ecology 7

References

[1] B Czech P R Krausman and P K Devers ldquoEconomic asso-ciations among causes of species endangerment in the UnitedStatesrdquo BioScience vol 50 no 7 pp 593ndash601 2000

[2] D S Wilcove C H Mclellan and A P Dobson ldquoHabitatfragmentation in the temperate zonerdquo in Conservation BiologyThe Science of Scarcity and Species Richness M E Soule Ed pp237ndash256 Sinauer Associates Sunderland Mass USA 1998

[3] A G Chiarello ldquoDensity and population size of mammals inremnants of BrazilianAtlantic forestrdquoConservation Biology vol14 no 6 pp 1649ndash1657 2000

[4] RK Laidlaw ldquoEffects of habitat disturbance andprotected areasonmammals of PeninsularMalaysiardquoConservation Biology vol14 no 6 pp 1639ndash1648 2000

[5] M A Lopes and S F Ferrari ldquoEffects of human colonization onthe abundance and diversity of mammals in eastern BrazilianAmazoniardquo Conservation Biology vol 14 no 6 pp 1658ndash16652000

[6] E Carrillo G Wong and N A D Cuaron ldquoMonitoringmammal populations in Costa Rican protected areas underdifferent hunting restrictionsrdquo Conservation Biology vol 14 no6 pp 1580ndash1591 2000

[7] M Conroy and D Nichols ldquoDesigning a study to assessmammalian diversityrdquo in Measuring and Monitoring BiologicalDiversity StandardMethods forMammals DWilson R Cole JNichols R Rudran andM Foster Eds pp 41ndash49 SmithsonianInstitution Press London UK 1996

[8] WAPCA Annual Report West African Primate ConservationAction WAPCA Accra Ghana 2012

[9] D Osei R H Horwich and J M Pittman ldquoFirst sightings ofthe Roloway Monkey (Cercopithecus diana roloway) in Ghanain ten years and the status of other endangered primates inSouthwesternGhanardquoAfrican Primates vol 10 pp 25ndash40 2015

[10] The IUCN Red List ofThreatened Species Version 20152 2015httpwwwiucnredlistorg

[11] W S McGraw and J F Oates ldquoRoloway monkey Cercopithecusdiana roloway (Schreber 1774)rdquo in Primates in Peril TheWorldrsquos Most Endangered Primates 2012ndash2014 C Schwitzer RA Mittermeier A B Rylands et al Eds pp 14ndash16 IUCN SSCPrimate Specialist Group (PSG) International PrimatologicalSociety (IPS) Conservation International (CI) and BristolZoological Society Arlington Va USA 2014

[12] R A Mittermeier J Ratsimbazafy A B Rylands et al ldquoPri-mates in peril the worldrsquos 25 most endangered primates 2006ndash2008rdquo Primate Conservation vol 22 pp 1ndash40 2007

[13] D Swift ldquoThe consequences of logging on primate density anddiversity in Kibale National Park Ugandardquo Bioscience Horizonsvol 5 pp 1ndash6 2012

[14] C A Chapman L J Chapman L Naughton-Treves M JLawes and L R Mcdowell ldquoPredicting folivorous primateabundance validation of a nutritionalmodelrdquoAmerican Journalof Primatology vol 62 no 2 pp 55ndash69 2004

[15] J P Skorupa The effects of selective timber harvesting onrain-forest primates in Kibale Forest Uganda [PhD thesis]University of California Davis Davis Calif USA 1988

[16] T T Struhsaker Ecology of an African Rainforest Logging inKibale and the Conflict between Conservation and ExploitationUniversity Press of Florida Gainesville Fla USA 1997

[17] P Mayor P Perez-Pena M Bowler P E Puertas M Kirklandand R Bodmer ldquoEffects of selective logging on large mammal

populations in a remote indigenous territory in the northernperuvian amazonrdquo Ecology and Society vol 20 no 4 pp 36ndash44 2015

[18] A J Plumptre and V Reynolds ldquoThe effect of selective loggingon the primate populations in the Budongo Forest ReserveUgandardquo Journal of Applied Ecology vol 31 no 4 pp 631ndash6411994

[19] C Mammides M Cords and M K Peters ldquoEffects of habitatdisturbance and food supply on population densities of threeprimate species in theKakamega Forest KenyardquoAfrican Journalof Ecology vol 47 no 1 pp 87ndash96 2009

[20] C Schwitzer L Glatt K A-I Nekaris and J U GanzhornldquoResponses of animals to habitat alteration an overviewfocussing on primatesrdquo Endangered Species Research vol 14 no1 pp 31ndash38 2011

[21] R Rimbach A Link M Heistermann C Gomez-Posada NGalvis and E W Heymann ldquoEffects of logging hunting andforest fragment size on physiological stress levels of two sym-patric ateline primates in Colombiardquo Conservation Physiologyvol 1 no 1 Article ID cot031 pp 1ndash11 2013

[22] R F W Barnes K L Barnes M P T Alers and A Blom ldquoMandetermines the distribution of elephants in the rain forests ofnortheastern Gabonrdquo African Journal of Ecology vol 29 no 1pp 54ndash63 1991

[23] R F W Barnes K Beardsley F Michelmore K L Barnes M PT Alers andA Blom ldquoEstimating forest elephant numberswithdung counts and a geographic information systemrdquo Journal ofWildlife Management vol 61 no 4 pp 1384ndash1393 1997

[24] S A Lahm R F W Barnes K Beardsley and P CervinkaldquoA method for censusing the greater white-nosed monkey innortheastern Gabon using the population density gradient inrelation to roadsrdquo Journal of Tropical Ecology vol 14 no 5 pp629ndash643 1998

[25] L Sebogo and R F W Barnes ldquoAction plan for the manage-ment of trans-frontier elephant conservation corridors in WestAfricardquo Tech Rep IUCNAfESGOuagadougou Burkina Faso2003

[26] J F OatesM Abedi-LarteyW SMcGraw T T Struhsaker andG H Whitesides ldquoExtinction of a West African red colobusmonkeyrdquo Conservation Biology vol 14 no 5 pp 1526ndash15322000

[27] L Thomas J L Laake S Strindberg et al Distance 40 Release1 Research Unit for Wildlife Population Assessment Universityof St Andrews St Andrews Scotland 2002

[28] S T Buckland D R Anderson K P Burnham J L Laake DL Borchers and L Thomas Introduction to Distance SamplingEstimating Abundance of Biological Populations OxfordUniver-sity Press Oxford UK 2001

[29] R K Colewell EstimateS Statistical Estimation of SpeciesRichness and Shared Species from Samples Version 8 2006httppurloclcorgestimates

[30] C J F Ter Braak and P Imilauer Canoco Reference Manual andCanoDraw for Windows Userrsquos Guide Software for CanonicalCommunity Ordination (Version 45) Microcomputer PowerIthaca NY USA 2002

[31] T F L V B Rangel J A FDiniz-Filho and LM Bini ldquoTowardsan integrated computational tool for spatial analysis in macroe-cology and biogeographyrdquo Global Ecology and Biogeographyvol 15 no 4 pp 321ndash327 2006

[32] W F Laurance B M Croes L Tchignoumba et al ldquoImpactsof roads and hunting on central African rainforest mammalsrdquoConservation Biology vol 20 no 4 pp 1251ndash1261 2006

8 International Journal of Ecology

[33] C A Chapman S R Balcomb T R Gillespie J P Skorupa andT T Struhsaker ldquoLong-term effects of logging on African pri-mate communities a 28-year comparison from Kibale NationalPark Ugandardquo Conservation Biology vol 14 no 1 pp 207ndash2172000

[34] S A Lahm and J P Tezi ldquoAssessment of the communities ofmedium-sized and large arboreal and terrestrial mammals inthe Rabi-Toucan region of the Ngove-Ndogo Hunting Domainand southwestern Loango National Parkrdquo Bulletin of the Biolog-ical Society of Washington vol 12 pp 383ndash416 2006

[35] W F Laurance A AlonsoM Lee and P Campbell ldquoChallengesfor forest conservation in Gabon Central Africardquo Futures vol38 no 4 pp 454ndash470 2006

[36] A Kamdem-Toham AW Adeleke N D Burgess et al ldquoForestconservation in the Congo Basinrdquo Science vol 299 no 5605article 346 2003

[37] A J Novaro K H Redford and R E Bodmer ldquoEffect ofhunting in source-sink systems in theNeotropicsrdquoConservationBiology vol 14 no 3 pp 713ndash721 2000

[38] C A Peres ldquoSynergistic effects of subsistence hunting andhabitat fragmentation on amazonian forest vertebratesrdquoConser-vation Biology vol 15 no 6 pp 1490ndash1505 2001

[39] R Woodroffe and J R Ginsberg ldquoEdge effects and the extinc-tion of populations inside protected areasrdquo Science vol 280 no5372 pp 2126ndash2128 1998

[40] W F Laurance T E Lovejoy H L Vasconcelos et alldquoEcosystem decay of Amazonian forest fragments a 22-yearinvestigationrdquo Conservation Biology vol 16 no 3 pp 605ndash6182002

[41] A Kaus ldquoEnvironmental perceptions and social relations in theMapimı Biosphere Reserverdquo Conservation Biology vol 7 no 2pp 398ndash406 1993

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 6: Research Article Logging Activity Adversely Impacts Primate Diversity …downloads.hindawi.com/journals/ijecol/2016/7497326.pdf · 2019-07-30 · Primate Diversity. Primate species

6 International Journal of Ecology

minus25

0

25

5

75

10

125

15

175

20

225

Num

ber o

f prim

ates

per

km

minus2 0 2 4 6 8 10 12Logging activity per km

Y = 15974 minus 2137 lowast X + 064 lowast X2 R

2= 769

Figure 3 Relationship between encounter rates of primates andlogging intensity

may not be the only factor influencing primate species com-position and density Although both strata possess similartopography and vegetation type logged areas had recentlogging disturbances that resulted in reduced canopy coverand denser understory cover A factor that may have alsoinfluenced our findings could be the proximity of some fringecommunities to the forest edge During the study it wasobserved that logged areas were closer to fringe communitiesand farms making such areas more susceptible to humandisturbances such as poaching [17 32] Some of these differ-ences in human and ecological variables may have influencedour findings One reason that may have accounted for highernumbers of black-and-white colobuses in the logged stratumis that they are folivores [14] and as suchmay show preferencefor degraded areas where the open canopy permits growthof diverse understory Apart from changes in density anddiversity logging might have also affected the behaviour ofprimates [13 20 33] For instance primates exhibited extremeshyness including restricting calls in the logged stratumcompared to the unlogged stratum when teams encounteredprimate groups The apparent differences in the incidence ofalarm calls between groups ofmonkeys encountered betweenthe two strata could affect our census findings to a smallextent However previous studies on primate surveys [14 2434] have shown that many replications are needed at eachtransect before the group density estimates can be consideredreliable In the current study each transect was sampledmorethan once and this could increase the reliability of our results

Our study draws attention to matters of both nationaland international conservation concern The evidence ofunauthorized human activities recorded during this study

indicates clearly that the community-based managementsystem practiced at Kwabre Rainforest may not be effectivein preventing poaching and other illegal human activities inthe forest If current threats continue unabated then rapidpopulation decline of primates is expected in the near future

Given its considerably intact forest cover Ghana is in aposition to implement important forest conservation initia-tives in the subregion [35 36] Within Ghana the generalvicinity of the Kwabre Rainforest is very significant from aregional viewpoint because it constitutes part of a networkof forest reserves in southwestern Ghana which constitutesGhanarsquos portion of the proposed crucial corridor for wildlifebetween the Ankasa Conservation Area in Ghana and theTanoe Forest in Cote drsquoIvoire [9]

In this regional setting the future management of theKwabre corridor could be very important At present farmsand villages are flourishing along theKwabre corridor rapidlyincreasing local human pressure Concerns about the futureof Kwabre corridor are particularly important because inter-est to protect wildlife in the area has waned andKwabre Rain-forest could face a sudden increase in hunting logging andslash-and-burn farming Instead of acting as a communityforest buffer zone and possible faunal corridor between twokey international protected areas (Ankasa ConservationAreain Ghana and Tanoe Forest in neighbouring Cote drsquoIvoireFigure 2) the larger Kwabre corridor area could insteadbecome a major population sink for wildlife [13 37 38] Thiswould reinforce adverse edge effects and genetic isolationof the protected areas increasing the probability of localextinctions of species of conservation interest [39 40]

5 Conclusions and Recommendations

Kwabre Rainforest is an important site where careful wildlifemanagement can support major biodiversity conservationin Ghana hence more effort should be channeled intopreventing further habitat degradation of the larger KwabreRainforest corridor area One possibility would be to grantthe Kwabre Rainforest protected area status under Ghanaianlaw and to manage it under the umbrella of an integratedconservation plan that includes its two adjacent internationalprotected areas Such a plan can be achieved by designatingthe entire area as a biosphere reserve which would permitplanned development outside reserves while affording highprotection for protected areas [41] With effective long-term management this region of southwestern Ghana couldremain one of the most important areas for wildlife in WestAfrica

Competing Interests

The authors declare that there are no competing interestsregarding the publication of this paper

Acknowledgments

Many thanks are due to the traditional head and people ofKwabre

International Journal of Ecology 7

References

[1] B Czech P R Krausman and P K Devers ldquoEconomic asso-ciations among causes of species endangerment in the UnitedStatesrdquo BioScience vol 50 no 7 pp 593ndash601 2000

[2] D S Wilcove C H Mclellan and A P Dobson ldquoHabitatfragmentation in the temperate zonerdquo in Conservation BiologyThe Science of Scarcity and Species Richness M E Soule Ed pp237ndash256 Sinauer Associates Sunderland Mass USA 1998

[3] A G Chiarello ldquoDensity and population size of mammals inremnants of BrazilianAtlantic forestrdquoConservation Biology vol14 no 6 pp 1649ndash1657 2000

[4] RK Laidlaw ldquoEffects of habitat disturbance andprotected areasonmammals of PeninsularMalaysiardquoConservation Biology vol14 no 6 pp 1639ndash1648 2000

[5] M A Lopes and S F Ferrari ldquoEffects of human colonization onthe abundance and diversity of mammals in eastern BrazilianAmazoniardquo Conservation Biology vol 14 no 6 pp 1658ndash16652000

[6] E Carrillo G Wong and N A D Cuaron ldquoMonitoringmammal populations in Costa Rican protected areas underdifferent hunting restrictionsrdquo Conservation Biology vol 14 no6 pp 1580ndash1591 2000

[7] M Conroy and D Nichols ldquoDesigning a study to assessmammalian diversityrdquo in Measuring and Monitoring BiologicalDiversity StandardMethods forMammals DWilson R Cole JNichols R Rudran andM Foster Eds pp 41ndash49 SmithsonianInstitution Press London UK 1996

[8] WAPCA Annual Report West African Primate ConservationAction WAPCA Accra Ghana 2012

[9] D Osei R H Horwich and J M Pittman ldquoFirst sightings ofthe Roloway Monkey (Cercopithecus diana roloway) in Ghanain ten years and the status of other endangered primates inSouthwesternGhanardquoAfrican Primates vol 10 pp 25ndash40 2015

[10] The IUCN Red List ofThreatened Species Version 20152 2015httpwwwiucnredlistorg

[11] W S McGraw and J F Oates ldquoRoloway monkey Cercopithecusdiana roloway (Schreber 1774)rdquo in Primates in Peril TheWorldrsquos Most Endangered Primates 2012ndash2014 C Schwitzer RA Mittermeier A B Rylands et al Eds pp 14ndash16 IUCN SSCPrimate Specialist Group (PSG) International PrimatologicalSociety (IPS) Conservation International (CI) and BristolZoological Society Arlington Va USA 2014

[12] R A Mittermeier J Ratsimbazafy A B Rylands et al ldquoPri-mates in peril the worldrsquos 25 most endangered primates 2006ndash2008rdquo Primate Conservation vol 22 pp 1ndash40 2007

[13] D Swift ldquoThe consequences of logging on primate density anddiversity in Kibale National Park Ugandardquo Bioscience Horizonsvol 5 pp 1ndash6 2012

[14] C A Chapman L J Chapman L Naughton-Treves M JLawes and L R Mcdowell ldquoPredicting folivorous primateabundance validation of a nutritionalmodelrdquoAmerican Journalof Primatology vol 62 no 2 pp 55ndash69 2004

[15] J P Skorupa The effects of selective timber harvesting onrain-forest primates in Kibale Forest Uganda [PhD thesis]University of California Davis Davis Calif USA 1988

[16] T T Struhsaker Ecology of an African Rainforest Logging inKibale and the Conflict between Conservation and ExploitationUniversity Press of Florida Gainesville Fla USA 1997

[17] P Mayor P Perez-Pena M Bowler P E Puertas M Kirklandand R Bodmer ldquoEffects of selective logging on large mammal

populations in a remote indigenous territory in the northernperuvian amazonrdquo Ecology and Society vol 20 no 4 pp 36ndash44 2015

[18] A J Plumptre and V Reynolds ldquoThe effect of selective loggingon the primate populations in the Budongo Forest ReserveUgandardquo Journal of Applied Ecology vol 31 no 4 pp 631ndash6411994

[19] C Mammides M Cords and M K Peters ldquoEffects of habitatdisturbance and food supply on population densities of threeprimate species in theKakamega Forest KenyardquoAfrican Journalof Ecology vol 47 no 1 pp 87ndash96 2009

[20] C Schwitzer L Glatt K A-I Nekaris and J U GanzhornldquoResponses of animals to habitat alteration an overviewfocussing on primatesrdquo Endangered Species Research vol 14 no1 pp 31ndash38 2011

[21] R Rimbach A Link M Heistermann C Gomez-Posada NGalvis and E W Heymann ldquoEffects of logging hunting andforest fragment size on physiological stress levels of two sym-patric ateline primates in Colombiardquo Conservation Physiologyvol 1 no 1 Article ID cot031 pp 1ndash11 2013

[22] R F W Barnes K L Barnes M P T Alers and A Blom ldquoMandetermines the distribution of elephants in the rain forests ofnortheastern Gabonrdquo African Journal of Ecology vol 29 no 1pp 54ndash63 1991

[23] R F W Barnes K Beardsley F Michelmore K L Barnes M PT Alers andA Blom ldquoEstimating forest elephant numberswithdung counts and a geographic information systemrdquo Journal ofWildlife Management vol 61 no 4 pp 1384ndash1393 1997

[24] S A Lahm R F W Barnes K Beardsley and P CervinkaldquoA method for censusing the greater white-nosed monkey innortheastern Gabon using the population density gradient inrelation to roadsrdquo Journal of Tropical Ecology vol 14 no 5 pp629ndash643 1998

[25] L Sebogo and R F W Barnes ldquoAction plan for the manage-ment of trans-frontier elephant conservation corridors in WestAfricardquo Tech Rep IUCNAfESGOuagadougou Burkina Faso2003

[26] J F OatesM Abedi-LarteyW SMcGraw T T Struhsaker andG H Whitesides ldquoExtinction of a West African red colobusmonkeyrdquo Conservation Biology vol 14 no 5 pp 1526ndash15322000

[27] L Thomas J L Laake S Strindberg et al Distance 40 Release1 Research Unit for Wildlife Population Assessment Universityof St Andrews St Andrews Scotland 2002

[28] S T Buckland D R Anderson K P Burnham J L Laake DL Borchers and L Thomas Introduction to Distance SamplingEstimating Abundance of Biological Populations OxfordUniver-sity Press Oxford UK 2001

[29] R K Colewell EstimateS Statistical Estimation of SpeciesRichness and Shared Species from Samples Version 8 2006httppurloclcorgestimates

[30] C J F Ter Braak and P Imilauer Canoco Reference Manual andCanoDraw for Windows Userrsquos Guide Software for CanonicalCommunity Ordination (Version 45) Microcomputer PowerIthaca NY USA 2002

[31] T F L V B Rangel J A FDiniz-Filho and LM Bini ldquoTowardsan integrated computational tool for spatial analysis in macroe-cology and biogeographyrdquo Global Ecology and Biogeographyvol 15 no 4 pp 321ndash327 2006

[32] W F Laurance B M Croes L Tchignoumba et al ldquoImpactsof roads and hunting on central African rainforest mammalsrdquoConservation Biology vol 20 no 4 pp 1251ndash1261 2006

8 International Journal of Ecology

[33] C A Chapman S R Balcomb T R Gillespie J P Skorupa andT T Struhsaker ldquoLong-term effects of logging on African pri-mate communities a 28-year comparison from Kibale NationalPark Ugandardquo Conservation Biology vol 14 no 1 pp 207ndash2172000

[34] S A Lahm and J P Tezi ldquoAssessment of the communities ofmedium-sized and large arboreal and terrestrial mammals inthe Rabi-Toucan region of the Ngove-Ndogo Hunting Domainand southwestern Loango National Parkrdquo Bulletin of the Biolog-ical Society of Washington vol 12 pp 383ndash416 2006

[35] W F Laurance A AlonsoM Lee and P Campbell ldquoChallengesfor forest conservation in Gabon Central Africardquo Futures vol38 no 4 pp 454ndash470 2006

[36] A Kamdem-Toham AW Adeleke N D Burgess et al ldquoForestconservation in the Congo Basinrdquo Science vol 299 no 5605article 346 2003

[37] A J Novaro K H Redford and R E Bodmer ldquoEffect ofhunting in source-sink systems in theNeotropicsrdquoConservationBiology vol 14 no 3 pp 713ndash721 2000

[38] C A Peres ldquoSynergistic effects of subsistence hunting andhabitat fragmentation on amazonian forest vertebratesrdquoConser-vation Biology vol 15 no 6 pp 1490ndash1505 2001

[39] R Woodroffe and J R Ginsberg ldquoEdge effects and the extinc-tion of populations inside protected areasrdquo Science vol 280 no5372 pp 2126ndash2128 1998

[40] W F Laurance T E Lovejoy H L Vasconcelos et alldquoEcosystem decay of Amazonian forest fragments a 22-yearinvestigationrdquo Conservation Biology vol 16 no 3 pp 605ndash6182002

[41] A Kaus ldquoEnvironmental perceptions and social relations in theMapimı Biosphere Reserverdquo Conservation Biology vol 7 no 2pp 398ndash406 1993

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 7: Research Article Logging Activity Adversely Impacts Primate Diversity …downloads.hindawi.com/journals/ijecol/2016/7497326.pdf · 2019-07-30 · Primate Diversity. Primate species

International Journal of Ecology 7

References

[1] B Czech P R Krausman and P K Devers ldquoEconomic asso-ciations among causes of species endangerment in the UnitedStatesrdquo BioScience vol 50 no 7 pp 593ndash601 2000

[2] D S Wilcove C H Mclellan and A P Dobson ldquoHabitatfragmentation in the temperate zonerdquo in Conservation BiologyThe Science of Scarcity and Species Richness M E Soule Ed pp237ndash256 Sinauer Associates Sunderland Mass USA 1998

[3] A G Chiarello ldquoDensity and population size of mammals inremnants of BrazilianAtlantic forestrdquoConservation Biology vol14 no 6 pp 1649ndash1657 2000

[4] RK Laidlaw ldquoEffects of habitat disturbance andprotected areasonmammals of PeninsularMalaysiardquoConservation Biology vol14 no 6 pp 1639ndash1648 2000

[5] M A Lopes and S F Ferrari ldquoEffects of human colonization onthe abundance and diversity of mammals in eastern BrazilianAmazoniardquo Conservation Biology vol 14 no 6 pp 1658ndash16652000

[6] E Carrillo G Wong and N A D Cuaron ldquoMonitoringmammal populations in Costa Rican protected areas underdifferent hunting restrictionsrdquo Conservation Biology vol 14 no6 pp 1580ndash1591 2000

[7] M Conroy and D Nichols ldquoDesigning a study to assessmammalian diversityrdquo in Measuring and Monitoring BiologicalDiversity StandardMethods forMammals DWilson R Cole JNichols R Rudran andM Foster Eds pp 41ndash49 SmithsonianInstitution Press London UK 1996

[8] WAPCA Annual Report West African Primate ConservationAction WAPCA Accra Ghana 2012

[9] D Osei R H Horwich and J M Pittman ldquoFirst sightings ofthe Roloway Monkey (Cercopithecus diana roloway) in Ghanain ten years and the status of other endangered primates inSouthwesternGhanardquoAfrican Primates vol 10 pp 25ndash40 2015

[10] The IUCN Red List ofThreatened Species Version 20152 2015httpwwwiucnredlistorg

[11] W S McGraw and J F Oates ldquoRoloway monkey Cercopithecusdiana roloway (Schreber 1774)rdquo in Primates in Peril TheWorldrsquos Most Endangered Primates 2012ndash2014 C Schwitzer RA Mittermeier A B Rylands et al Eds pp 14ndash16 IUCN SSCPrimate Specialist Group (PSG) International PrimatologicalSociety (IPS) Conservation International (CI) and BristolZoological Society Arlington Va USA 2014

[12] R A Mittermeier J Ratsimbazafy A B Rylands et al ldquoPri-mates in peril the worldrsquos 25 most endangered primates 2006ndash2008rdquo Primate Conservation vol 22 pp 1ndash40 2007

[13] D Swift ldquoThe consequences of logging on primate density anddiversity in Kibale National Park Ugandardquo Bioscience Horizonsvol 5 pp 1ndash6 2012

[14] C A Chapman L J Chapman L Naughton-Treves M JLawes and L R Mcdowell ldquoPredicting folivorous primateabundance validation of a nutritionalmodelrdquoAmerican Journalof Primatology vol 62 no 2 pp 55ndash69 2004

[15] J P Skorupa The effects of selective timber harvesting onrain-forest primates in Kibale Forest Uganda [PhD thesis]University of California Davis Davis Calif USA 1988

[16] T T Struhsaker Ecology of an African Rainforest Logging inKibale and the Conflict between Conservation and ExploitationUniversity Press of Florida Gainesville Fla USA 1997

[17] P Mayor P Perez-Pena M Bowler P E Puertas M Kirklandand R Bodmer ldquoEffects of selective logging on large mammal

populations in a remote indigenous territory in the northernperuvian amazonrdquo Ecology and Society vol 20 no 4 pp 36ndash44 2015

[18] A J Plumptre and V Reynolds ldquoThe effect of selective loggingon the primate populations in the Budongo Forest ReserveUgandardquo Journal of Applied Ecology vol 31 no 4 pp 631ndash6411994

[19] C Mammides M Cords and M K Peters ldquoEffects of habitatdisturbance and food supply on population densities of threeprimate species in theKakamega Forest KenyardquoAfrican Journalof Ecology vol 47 no 1 pp 87ndash96 2009

[20] C Schwitzer L Glatt K A-I Nekaris and J U GanzhornldquoResponses of animals to habitat alteration an overviewfocussing on primatesrdquo Endangered Species Research vol 14 no1 pp 31ndash38 2011

[21] R Rimbach A Link M Heistermann C Gomez-Posada NGalvis and E W Heymann ldquoEffects of logging hunting andforest fragment size on physiological stress levels of two sym-patric ateline primates in Colombiardquo Conservation Physiologyvol 1 no 1 Article ID cot031 pp 1ndash11 2013

[22] R F W Barnes K L Barnes M P T Alers and A Blom ldquoMandetermines the distribution of elephants in the rain forests ofnortheastern Gabonrdquo African Journal of Ecology vol 29 no 1pp 54ndash63 1991

[23] R F W Barnes K Beardsley F Michelmore K L Barnes M PT Alers andA Blom ldquoEstimating forest elephant numberswithdung counts and a geographic information systemrdquo Journal ofWildlife Management vol 61 no 4 pp 1384ndash1393 1997

[24] S A Lahm R F W Barnes K Beardsley and P CervinkaldquoA method for censusing the greater white-nosed monkey innortheastern Gabon using the population density gradient inrelation to roadsrdquo Journal of Tropical Ecology vol 14 no 5 pp629ndash643 1998

[25] L Sebogo and R F W Barnes ldquoAction plan for the manage-ment of trans-frontier elephant conservation corridors in WestAfricardquo Tech Rep IUCNAfESGOuagadougou Burkina Faso2003

[26] J F OatesM Abedi-LarteyW SMcGraw T T Struhsaker andG H Whitesides ldquoExtinction of a West African red colobusmonkeyrdquo Conservation Biology vol 14 no 5 pp 1526ndash15322000

[27] L Thomas J L Laake S Strindberg et al Distance 40 Release1 Research Unit for Wildlife Population Assessment Universityof St Andrews St Andrews Scotland 2002

[28] S T Buckland D R Anderson K P Burnham J L Laake DL Borchers and L Thomas Introduction to Distance SamplingEstimating Abundance of Biological Populations OxfordUniver-sity Press Oxford UK 2001

[29] R K Colewell EstimateS Statistical Estimation of SpeciesRichness and Shared Species from Samples Version 8 2006httppurloclcorgestimates

[30] C J F Ter Braak and P Imilauer Canoco Reference Manual andCanoDraw for Windows Userrsquos Guide Software for CanonicalCommunity Ordination (Version 45) Microcomputer PowerIthaca NY USA 2002

[31] T F L V B Rangel J A FDiniz-Filho and LM Bini ldquoTowardsan integrated computational tool for spatial analysis in macroe-cology and biogeographyrdquo Global Ecology and Biogeographyvol 15 no 4 pp 321ndash327 2006

[32] W F Laurance B M Croes L Tchignoumba et al ldquoImpactsof roads and hunting on central African rainforest mammalsrdquoConservation Biology vol 20 no 4 pp 1251ndash1261 2006

8 International Journal of Ecology

[33] C A Chapman S R Balcomb T R Gillespie J P Skorupa andT T Struhsaker ldquoLong-term effects of logging on African pri-mate communities a 28-year comparison from Kibale NationalPark Ugandardquo Conservation Biology vol 14 no 1 pp 207ndash2172000

[34] S A Lahm and J P Tezi ldquoAssessment of the communities ofmedium-sized and large arboreal and terrestrial mammals inthe Rabi-Toucan region of the Ngove-Ndogo Hunting Domainand southwestern Loango National Parkrdquo Bulletin of the Biolog-ical Society of Washington vol 12 pp 383ndash416 2006

[35] W F Laurance A AlonsoM Lee and P Campbell ldquoChallengesfor forest conservation in Gabon Central Africardquo Futures vol38 no 4 pp 454ndash470 2006

[36] A Kamdem-Toham AW Adeleke N D Burgess et al ldquoForestconservation in the Congo Basinrdquo Science vol 299 no 5605article 346 2003

[37] A J Novaro K H Redford and R E Bodmer ldquoEffect ofhunting in source-sink systems in theNeotropicsrdquoConservationBiology vol 14 no 3 pp 713ndash721 2000

[38] C A Peres ldquoSynergistic effects of subsistence hunting andhabitat fragmentation on amazonian forest vertebratesrdquoConser-vation Biology vol 15 no 6 pp 1490ndash1505 2001

[39] R Woodroffe and J R Ginsberg ldquoEdge effects and the extinc-tion of populations inside protected areasrdquo Science vol 280 no5372 pp 2126ndash2128 1998

[40] W F Laurance T E Lovejoy H L Vasconcelos et alldquoEcosystem decay of Amazonian forest fragments a 22-yearinvestigationrdquo Conservation Biology vol 16 no 3 pp 605ndash6182002

[41] A Kaus ldquoEnvironmental perceptions and social relations in theMapimı Biosphere Reserverdquo Conservation Biology vol 7 no 2pp 398ndash406 1993

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 8: Research Article Logging Activity Adversely Impacts Primate Diversity …downloads.hindawi.com/journals/ijecol/2016/7497326.pdf · 2019-07-30 · Primate Diversity. Primate species

8 International Journal of Ecology

[33] C A Chapman S R Balcomb T R Gillespie J P Skorupa andT T Struhsaker ldquoLong-term effects of logging on African pri-mate communities a 28-year comparison from Kibale NationalPark Ugandardquo Conservation Biology vol 14 no 1 pp 207ndash2172000

[34] S A Lahm and J P Tezi ldquoAssessment of the communities ofmedium-sized and large arboreal and terrestrial mammals inthe Rabi-Toucan region of the Ngove-Ndogo Hunting Domainand southwestern Loango National Parkrdquo Bulletin of the Biolog-ical Society of Washington vol 12 pp 383ndash416 2006

[35] W F Laurance A AlonsoM Lee and P Campbell ldquoChallengesfor forest conservation in Gabon Central Africardquo Futures vol38 no 4 pp 454ndash470 2006

[36] A Kamdem-Toham AW Adeleke N D Burgess et al ldquoForestconservation in the Congo Basinrdquo Science vol 299 no 5605article 346 2003

[37] A J Novaro K H Redford and R E Bodmer ldquoEffect ofhunting in source-sink systems in theNeotropicsrdquoConservationBiology vol 14 no 3 pp 713ndash721 2000

[38] C A Peres ldquoSynergistic effects of subsistence hunting andhabitat fragmentation on amazonian forest vertebratesrdquoConser-vation Biology vol 15 no 6 pp 1490ndash1505 2001

[39] R Woodroffe and J R Ginsberg ldquoEdge effects and the extinc-tion of populations inside protected areasrdquo Science vol 280 no5372 pp 2126ndash2128 1998

[40] W F Laurance T E Lovejoy H L Vasconcelos et alldquoEcosystem decay of Amazonian forest fragments a 22-yearinvestigationrdquo Conservation Biology vol 16 no 3 pp 605ndash6182002

[41] A Kaus ldquoEnvironmental perceptions and social relations in theMapimı Biosphere Reserverdquo Conservation Biology vol 7 no 2pp 398ndash406 1993

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

Page 9: Research Article Logging Activity Adversely Impacts Primate Diversity …downloads.hindawi.com/journals/ijecol/2016/7497326.pdf · 2019-07-30 · Primate Diversity. Primate species

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

EcosystemsJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MeteorologyAdvances in

EcologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental Chemistry

Atmospheric SciencesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Geological ResearchJournal of

EarthquakesJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BiodiversityInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of