Stable Isotopes in Elephant Hair Document Migration Patterns and Diet Changes
Author(s): Thure E. Cerling, George Wittemyer, Henrik B. Rasmussen, Fritz Vollrath, Claire
E. Cerling, Todd J. Robinson, Iain Douglas-Hamilton
Source: Proceedings of the National Academy of Sciences of the United States of America,
Vol. 103, No. 2 (Jan. 10, 2006), pp. 371-373
Published by: National Academy of Sciences
Stable URL: http://www.jstor.org/stable/30048308 .
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Stable
patterns
in
isotopes
and
diet
elephant
changes
hair
document
migration
Thure E. Cerling*t*,George Wittemyers, HenrikB. Rasmussenl, FritzVollrathr1,ClaireE. Cerlingt, Todd J. Robinsont,
and lain Douglas-Hamiltonll
*Departmentof Geology and Geophysics,135 South 1460 East,Universityof Utah, Salt LakeCity,UT84112; tDepartment of Biology, 257 South 1400 East,
Universityof Utah, Salt LakeCity,UT84112; sUniversityof California,Berkeley,CA94720;$Department of Zoology, Oxford University,OxfordOX13PS,
United Kingdom;and lSaveThe ElephantsFoundation,Nairobi,Kenya
Contributedby Thure E.Cerling,November4, 2005
We use chronologies of stable isotopes measured from elephant
(Loxodonta africana) hair to determine migration patterns and
seasonal diet changes in elephants in and near Samburu National
Reserve in northern Kenya. Stable carbon isotopes record diet
changes, principallyenabling differentiation between browse and
tropical grasses, which use the C3and C4photosynthetic pathways,
respectively; stable nitrogen isotopes record regional patterns
related to aridity, offering insight into localized ranging behavior.
Isotopically identified range shifts were corroborated by global
positioning system radio tracking data of the studied individuals.
Comparisonof the stable isotope record in the hair of one migrant
individual with that of a resident population shows important
differences in feeding and ranging behavior over time. Our analysis indicates that differences are the result of excursions into
mesic environments coupled with intermittent crop raiding by the
migrant individual. Variation in diet, quantified by using stable
isotopes, can offer insight into diet-related wildlife behavior.
ment. Tail hairs from 35 elephants were collected over this
period duringimmobilizationoperationswhile the collarswere
beingfitted and for some, later,when collarbatterieswere being
changed or when the collarswere being removed.Of these 35
elephants,7 have a secure isotopic dietarychronologyover the
period from late 2000 and extendingthrough February2002;
GPS spatialinformationis availablefor all residentindividuals
fromJuly2001to July2002and fromFebruary2002to July2002
for the migrantB1013.We focus on comparingthe behaviorof
the migrantB1013to that of the residentSamburugroupduring
this time interval.
The elephants trackedin this study used both the semiarid
region in and aroundSamburuNationalReserve and the mesic
Imenti Forest on the flanks of Mt. Kenya.These two distinct
ecotones are <60 km apart and are located between 370 and 380
east, just north of the equator. The elevation of the semiarid
Sambururegion is -900 m above sea level and dominatedby
acacia-comiphorasavannaand scrub bushland.Rainfall aver13-carbon I 15-nitrogen I chronology I human-elephant conflict
ages ;350 mm per yearin this lowlandregionandoccursduring
biannualrainyseasons,whichgenerallytake place in April and
The
stableisotope ratiosof 13C/12C in hairrecordsthe diet of November.The elevationof the ImentiForestis -2,000 m above
Themammals(1-4). It is particularlyuseful in distinguishing sea level and is dominatedby evergreenand broad leaf deciddiets of C3 browse versus C4 grass in tropical regions (5-7) uous tree species. Rainfallin this region also occursbiannually
becauseof the largedifferencein 13C/12Cratiosbetweenplants and averages ~900 mm per year.
In this study,we used 10-daycompositenormalizeddifferenusing the C3 and C4 photosyntheticpathways,respectively.In
tial
vegetation index (NDVI) data, availablethroughSatellite
tropicalregions,the C3 pathwayis used primarilyby trees and
Probatoire
d'Observationde la Terre (SPOT), to determine
whereas
shrubs,
plants using the C4 pathway are principally
in season across the study area. NDVI is a remote
changes
grasses (8, 9).
Hair is a particularlyuseful indicatorof diet change (3, 4) sensingindexvalue calculatedas the ratiobetweenred andnear
because the isotope turnoverof mammaltissuesis high enough infraredreflection that is highlycorrelatedwith green (phototo resolveshort-termdiet changes.Recent advancesin method- syntheticallyactive) biomass (15, 16). Remotely sensed data
a direct measure of photosyntheticactivityover large
ology, progressedthrough the study of large mammalswith provide
controlleddiet changes(10, 11), allowsdetailed reconstruction spatial regions, offering advantagesover the classicallyused
of the diet historyof individuallarge mammalsin wild popula- point-sampledrainfalldatain areas,like the studyregion,where
weather stations are sparse.Isotope profilesfor each elephant
tions (12, 13).
In this study, we determine the growth rates and stable were compared with longitudinal 10-day NDVI records to
13C/12Cand 15N/14Nratios in elephanthair collected between determinethe impactof seasonalityon diet.
ratiosof elephanthairandplantmaterial
13C/12C and 15N/14N
2001and2004.We focuson the behaviorof a residentpopulation
of SamburuNational Reserve, NorthernKenya, for the time were measured on an isotope ratio mass spectrometerafter
combustion in a flow-throughmodified Carlo-Erba system.
periodof 2000to 2002.We comparestableisotope resultsof this
residentpopulationwith a migrantelephant(B1013)thatvisited Values are reportedusing the conventionalpermil (%o) notaSamburuReserve up to severaltimes each year. Differencesin tion, where
isotope ratiosbetween the residentindividualsand the migrant
513C = (((13C/12C)sample/ (13C/ 12C) standard)- 1).1,000,
indicate different behaviors,includingrapid migrationacross
long distancesby the migrantindividualand differencesin the and an analogousterminologydescribes15N/14Nratios. Stanfraction C4 biomass in the diet. The latter may be related to dardsare Vienna Pee Dee Belemnite
(VPDB) and air for 613C
seasonal crop raiding,which can be quantifiedby using stable and
respectively.Uncertaintiesfor average815Nvaluesfor
815N,
isotope ratios.
Materialsand Methods
Global Positioning System (GPS) radio collars were fitted to
elephants in SamburuNational Reserve, NorthernKenya,between 2001 and 2004 (14). Collarswere programmedto record
positionsat hourlyintervals,offeringdetailedrecordsof movewww.pnas.org/cgi/doi/10.1073/pnas.0509606102
Conflictof intereststatement: No conflictsdeclared.
Abbreviations:
normalized
differential
GPS,GlobalPositioning
NDVI,
System;
vegetation
index.
*Towhom correspondenceshould be addressed.E-mail:[email protected].
c 2006 by The NationalAcademyof Sciencesof the USA
PNAS I January10, 2006
I
vol. 103
no. 2
I
371-373
ECOLOGY
plants discussedin the text are reportedas the standarderror.
Isotope enrichmentbetweenhairand diet is ;3%o for both 813C
and 815N(7-9).
Elephanthairwas seriallysectionedin 5-mmintervalsbefore
stable isotope analysis.For one hairfromB1013,sectioningwas
performedat --1-mmintervalsfor detailedisotope profilesover
selectedintervals.Tailhairgrowthratesin Kenyaelephantswere
establishedin three ways: (i) using overlappingstable isotope
patternsin haircollectedfrom the same individualtwo or more
times (12); (ii) usingoverlappingisotope patternsfrom individualshavingsimilargeographicalrangesbut collectedat different
times(13);and(iii) usingisotopedataalongwithvisualsightings.
One individual,B1013,had only a singlehair thatwas collected
duringcollaringoperations;its growthrateof hairwascalibrated
by comparing 615Nvalues with visual sightings in Samburu
National Reserve.
Diet was estimatedusing the isotope turnoverpool model of
Ayliffeet al. (10, 12). We use end-membervaluesof -27%o and
-13%o for C3 and C4 plants, respectively,which represent
average ecosystem values for SamburuNational Reserve and
nearbyregions (7).
Resultsand Discussion
GrowthRatesof ElephantHair.Hair growthrates for male and
femaleelephantsare 0.55 + 0.11mm/day(9 hairsfrom5 individuals) and 0.81 + 0.13 (23 hairsfrom 11 individuals),respectively,
and are significantly
different(ANOVA,P < 0.0001).Withinone
individual,thegrowthrateof differenthairsmayvarybyupto 30%,
but growthratesfor a givenhairappearsto be constantto within
forequids(10, 11).
5-10%,whichagreeswithpreviousobservations
The overallrangein tailhairgrowthratesis from0.4to 1.1mmper
day,with single hair lengthssometimesexceeding500 mm, thus
preservingdiet or migrationinformationfor periodsoften exceeding 1 year for a singlehair.
Spatial Distributionand Stable Isotope Ratios. GPS radio collars
A
0.5-
NDVI
0.40.30.2
15
B
10
615N
5
C
-20
613C
- 60
- 50
-25- 40
D
- 30
Diet
(%C4)
- 20
- 10
- 0
1 Jan
1 Apr
1 Jul
1Oct
1 Jan
1 Apr
I Jl
10ct
IJan
2001
2000
Date
Fig. 1. NDVIand stable isotope record of B1013 compared with other
elephants. (A) Average 10-day composite NDVIvalues for the SamburuNational Reserveregion from 2001through 2002, where elevated values indicate
increased vegetative productivityoccurringduring wet seasons. (B) 815Nof
hair from B1013 (black line; n = 83) and observations of B1013 in Samburu
National Reserve(blackrectangles;n = 17) during 2001 and 2002 compared
with the range of average values of 6'5N(+2o; gray region; n = 520) in hairs
of six resident elephants of Samburu National Reserve. Chronology was
established as described in the text. Eachaverage value (with standard deviation) of the SamburuNational Reserveresidents was averaged during the
10-day intervalscoinciding with NDVIcomposite data. (C)813Cfrom hair of
B1013 (open circles;n = 83) compared with the average 813C (+20; gray
region; n = 520) values of hair from six resident elephants of Samburu
National Reserve.(D) EstimatedC4component of diet of B1013 (open circles;
n = 83) compared with the average of six resident elephants of Samburu
National Reserve.Grayarea shows the diet (+2o- gray region, n = 520) of six
resident elephants of SamburuNational Reserve.Diet as percent C4biomass
was estimated as in ref. 12.
werefittedto the sevenelephants(fourfemale,threemale)of this
studyin SamburuNationalReservein NorthernKenyain 2001and
2002 (14). Six of the sevenelephantswerevisuallyobservedto be
in SamburuNationalReserveor in the immediatevicinityduring
the observationperiodfrom early2001to July2002,and thiswas
thisgroupconstitutesthe
withthe GPSinformation;
corroborated
Sambururesidentelephants.However,one elephant,an '40-yearold bullelephant(B1013),collaredon February3, 2002,hada very
differentmovementhistorythan the Sambururesidentelephants
for the periodfrom February2002 to July2002.The GPS collar
recorded the hourly positions of B1013's movementsbetween
February3, 2002andJuly18, 2002,whenthe collarfailed.Unfortunately,B1013wasshotandkilledshortlythereafter,anda second
haircouldnot be recovered.Duringthisperiod,B1013madethree
majortrips,shiftingfrom the aridlowlandsof SamburuNational
Reserveto the mesicImentiuplandforestnearMt. Kenyaor vice
versa.Theperiodsspentin the lowlandscorrespondto the mid-and highlandsof the Aberdaresand Mt. Kenya region have s15N
laterainyseason,andperiodsspentin theforestwereduringthedry values averaging1.7 + 0.5%o(n = 21), whereasthose in xeric
season.Each rangeshift was accomplishedin <15 h, coveringa lowlandsof SamburuNational Reserve average 7.9 + 0.7%o
straight-linedistanceover 40 km, a behaviorpatterndescribedas (n = 14); these valuesare significantlydifferent(ANOVA;P <
"streaking"(14). It is assumedthat B1013 moved in the same 0.0001). Enrichmentin 615Nfor hair compared with diet is
patternin 2001,whenthe isotopedata are availablefroma single -3%o, suggestingthat equilibrium615N values for these two
hair,as fromFebruary2002to July2002,whenthe GPS data are regionsshouldbe -5%o and 11%o,respectively.Moving as he
did between the two regions, B1013 never attained isotope
available.
of equilibriumwith the environmentin either region. Thus, the
Stable isotope analysesat 5-mm intervals(613Cand S15N)
the hair collected on February3, 2002 showedthat this individ- movementdata and the isotope data showthat B1013 occupied
ual occupiedtwo isotopicallydistinctregions(Fig. 1B).The 6s5N the highlands(wherethe 815Nvaluesare low) in the dry season,
records environmentalinformation,including s15Nvalues re- and in the rainyseason he moved to the lowlands,where 615N
lated to regionalvegetation. The hair segmentswith elevated values are elevated.
15N values (from 8%o to 10.5%o) corresponded to values
observed in resident elephants of SamburuNational Reserve
(averagell%o for the same time period). Plants in the mesic
372
I www.pnas.org/cgi/doi/10.1073/pnas.0509606102
SeasonalDiet Changes.Accordingto the chronologyestablished
of C4grass.
here,B1013hadfourperiodsof increasedconsumption
Cerlinget al.
40
Date (2001)
1 Jun
35
I
1 Jul
30
Hours
Outside
Imenti
Forest
L
-
20
613Chair
10
I
1 Oct
I
calculated 6'3Cdlet
,
15
- -
6l3Char,,
-15 -
25
1 Sept
1 Aug
I
estimated %C4
-20 -
613Cdiet
5
-25
0
0 1 2 3 4 5 6 7 8 9 1011 121314151617181920212223
50
Hourof day
estimated
Fig. 2. Histogramof hours spent by B1013 outside Imenti Forest. In total,
2,179 h of GPSpositions were recorded when B1013 was in or around the
Imenti Forest. During this period, 236 h of GPSpositions (10.8%) were recorded outside the designated forest boundaries in areas dense with subsistence farming. Being essentiallyon the equator, the sun risesand sets at 6:30
every day with little variation.All but 2 of the 236 h spent outside the Imenti
Forestwere during night hours during this interval.
Threeof theseperiodswereassociatedwithwetseasonsandperiods
of elevatedremotelysensedNDVI values,representingincreased
vegetativeproductivity.In general,Africanelephantshave a diet
dominatedbybrowse(6) andconsumegrassonlyas awindfallwhen
it is in new growth.Theseperiodsof grassconsumptionoccurred
whenB1013wasobservedin SamburuNationalReserveandwhen
NDVI valuesexceeded0.3. Thispatternof elevatedC4consumption duringwet seasonswas comparablewith observedpatternsin
residentSamburuelephants(Fig.1C);duringtheseintervals,B1013
had similarC4grassconsumptionas the othersix elephants.The
single exceptionis the highestC4 consumptionpeak, which occurredduringthe dryseasonbetweenJune18andAugust16,2001.
By comparison,the other six elephantshad a low fractionof C4
grass consumptionduringthis dry season. Duringthis interval,
whileB1013was in the ImentiForest,averageNDVI was low,yet
C4grassesmadeup 36%of the diet integratedover this interval,
withpeakvaluesapproaching
50%C4biomass.NDVIin theImenti
regionwasbelowtheyearlyaveragefromJune11 to November21,
with the dry seasonperiodwhen vegetative
2001, corresponding
productivityis decreased.
GPS trackingdata fromthe subsequentperiodspentin Imenti
revealsthat,while in residenceof the ImentiForest,B1013was
outsidethe forestreserveboundariesonlyduringnighttimehours
(Fig.2). Mostelephantcropraidingoccursat night,apparentlyto
avoid human interaction(17, 18). Subsistencefarmingoccurs
adjacentto the ImentiForest(19),andthisregion,aroundthe time
of the data collection,was one of the majorcropraidingconflict
zones in Kenya. Thus, it appearsthat this isotope signal is a
quantifiablerecordof crop raiding(Fig. 3). While in the Imenti
Forest,C3vegetationwastheprincipalfoodavailable,andtherefore
1. DeNiro,M. J. & Epstein,S. (1978) Geochim.Cosmochim.
Acta 42, 495-506.
2. DeNiro,M. J. & Epstein,S. (1981) Geochim.Cosmochim.
Acta 45, 341-351.
3. White,C. D. (1993)J. Archaeol.Sci. 20, 657-666.
4. Macko,S. A., Engel,M. H., Lubec,V. G., O'Connell,T. C. & Hedges,R. E. M.
(1999)Philos.Trans.R. Soc. LondonB 354, 65-76.
5. Lee-Thorp,J. & van der Merwe,N. J. (1987)S. Afr.J. Sci. 83, 712-715.
6. van der Merwe,N. J., Lee-Thorp,J. A., Thackeray,J. F., Hall-Martin,A.,
Kruger,F. J., Coetzee,H., Bell, R. H. V. & Lindeque,M. (1990)Nature346,
744-746.
7. Cerling,T. E., Harris,J. M. & Passey,B. H. (2003)J. Mammal.84, 456-471.
8. Bender,M. M. (1971)Phytochemistry
10, 1239-1245.
9. Sage,R. F., Li.,M. & Monson,R. K. (1999)in C4PlantBiology,eds.Sage,R. F.
& Monson,R. K. (Academic,San Diego), pp. 551-584.
10. Ayliffe, L. K., Cerling,T. E., Robinson,T., West, A. G., Sponheimer,M.,
Passey,B. H., Hammer,J., Roeder, B., Dearing,M. D. & Ehleringer,J. R.
(2004) Oecologia139, 11-22.
Cerlinget al.
%C4
0
1 Jun
1 Jul
1 Aug
1 Sept
1 Oct
Date (2001)
Fig.3. Detail of diet for B1013from June 1 to October 1, 2001 using ~1-mm
hair segments. The diet estimate of C4fraction uses C3and C4endmember
mixing lines for both mesic (upper boundary)and xericenvironments(lower
boundary).These have average 613Cvalues of -28%o and -12%ofor mesic
environments and -26%o and -13%o for xeric environments, respectively.
Average intervalof time is 1.8 days (maximum,2.4 days;minimum,0.9 days).
the C4componentof diet was most likelyobtainedfromadjacent
crops,evidentlyat night.Duringthe dryseasonbetweenJuneand
Augustof 2001,our studyindicatesthatB1013wassupplementing
his C3forestdiet with nocturnalcropraidingof C4maize.Fig. 3
shows a detailedstable isotope profilealongwith the estimated
fractionation
C4intakeduringthisunusualC4dietperiodduringthe
long dry seasonof 2001.
Quantificationof longitudinaldiet recordsfrom hair in wild
animalscan offer importantinformationto conservationistsand
wildlifemanagers.This articleprovidesan exampleof one of the
manypossibleuses that stable isotopes can providein resolving
the elephant-human conflict issue. Despite the recordingof
conflict incidences,it is often difficultto understandelephant
decisionsmade at an individuallevel and to quantifythe dietary
importanceof crop raidingby elephants.Combiningstudiesof
elephantmovementpatternsand overalldiet with incidencesof
raidinginjects additionalscientificdata into the highlytopical
discussionof human-elephantconflict alleviation.
andthe StableIsotopeRatioFacilityfor
We thankJ. R. Ehleringer
Environmental
Research(SIRFER)at the Universityof Utah, the
of Kenyafor permissionto workin Kenya,the Kenya
government
WildlifeServiceforfacilitation,
SaveTheElephantsfortechnicaland
logisticalfieldsupport,andthe PackardFoundation.
11. West,A. G., Ayliffe,L. K.,Cerling,T. E., Robinson,T. F., Karren,B., Dearing,
M. D. & Ehleringer,J. R. (2004)Funct.Ecol. 18, 616-624.
12. Cerling,T. E., Passey,B. H.,Ayliffe,L. K.,Cook,C. S.,Ehleringer,J. R., Harris,
J. M., Dhidha, M. B. & Kasiki, S. M. (2004) Palaeogeogr.Palaeoclimatol.
Palaeoecol. 206, 367-376.
13. Cerling,T. E. & Viehl, K. (2004)Afr.J. Ecol. 42, 88-92.
14. Douglas-Hamilton,
I., Krink,T. & Vollrath,F. (2005)Naturwissenschaften
92,
163-168.
15. Goward,S. N. & Prince,S. D. (1995)J. Biogeogr.22, 549-564.
16. Diallo,O.,Diouf,A., Hanan,N. P.,Niaye,A. & Prevost,Y. (1991)Int.J.Remote
Sensing12, 1259-1279.
17. Thouless,C. R. (1994) Oryx28, 119-127.
18. Hoare, R. E. (1995)Pachyderm19, 54-63.
19. Gathaara, G. N. (1999) Aerial Survey of the Destruction of Mt. Kenya, Imenti
and Ngare Ndare Forest Reserves (Kenya Wildlife Service, Nairobi, Kenya)
p. 33
PNAS I January10, 2006 1 vol. 103
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