Reviving the calcium-from-lemmings hypothesis
L. G. Underhill
Underhill,L.G. 1994. Revivingthe calcium-from-lemmings
hypothesis.WaderStudyGroup
Bull. 75: 35-36.
L.G. Underhill,
AvianDemography
Unit,Departmentof Statistical
Sciences,University
of Cape
Town, Rondebosch, 7700 South Africa.
The well-knownRoselaar-Summers
hypothesis,states
that there is a relationshipbetween lemmingabundancein
the arctictundraandthe breedingproductivity
of waders
and geese (Roselaar 1979; Summers 1986; Underhill et
rate in layinghens[Simkiss1975]), it wouldtake fourdays
to ingestsufficientcalciumfromtipulidlarvaeto produce
one egg! To putthe problemintoperspective,a clutchof
foursandpipereggscontainsabouttwice as much
calciumas the femalewhichlaysthem. Clearly,an
additionalsourceof calciumis requiredfor egg
production,
and MacLean(1974) hypothesised
thatthis
aL 1993). The birdsbreedmoresuccessfully
in peak
lemmingyears becausepredatorseat abundantlemmings
which may reduceredationon nestingbirds. However
predatorseat eggs and youngof birdsin years duringand
after a decrease in lemmingpopulationsize.
came from lemmings.
Obviously,sandpipersdo not attack lemmingsto eat their
skeletons!But when lemmingsare abundant,their bones
and teeth are readilyavailableon the tundrain the pellets
of avian predatorsof lemmingssuch as skuasand Snowy
Owls Nycteascandiaca(MacLean 1974), and in the scats
of ArcticFoxesAlopexlagopus.MacLeannotedthat
lemmingbones had even been found in the stomachsof
layingfemale LaplandBuntingsCa/car/uslappon/cus.
The Roselaar-Summers
hypothesis
was pre-datedby the
"MacLeanhypothesis"
whichalsospeculated"uponthe
possibledependenceof sandpiperson lemmings...for
reproduction",
althoughMacLean(1974) did not have
prey-switchingin mind!. He suggestedlemmingswere a
calciumsourcenecessaryfor egg productionand growth
Ofjuveniles. He foundthat, in June,32 outof 84 (38%)
stomachsof female sandpipersof four speciescontained
lemmingteeth and bones. Of these 84 females, 61 had
an ovarianfollicleexceeding4 mm in diameter, 29 of the
61 (48%) had skeletalremainsin the stomachs;this
percentageincreaseto 100% (n = 10) for femaleswith
folliclesgreater than 15 mm or an egg in the oviduct. In
The impactof calciumdeficiencyon reducingbreeding
productivityhas been demonstratedfor Great Tits Parus
major(Gravelandet al. 1994). One of the consequences
of acidrainis a leachingof calciumfromsoils- on poor
soilsthe effectis so pronounced
that snails,whichalso
contrast,he foundteeth and bonesin 3 out of 162 (2%) of
stomachsof males in June. In July,the valueswere 1.6%
for females (n = 61) and 0% for males(n = 79). In July
requirelarge amountsof calciumfor growthand
reproduction,
are greatlyreducedin number. Duringthe
criticalegg-layingperiod,the tits normallyconsumesnails
to providecalciumfor egg production.Lackof snails
resultsin eggswith shellsthat are so porousand thinthat
the eggs desiccateor are brokenduringincubation,
leadingto nest failure.
12% of the stomachs of chicks contained teeth and bones
(n -- 131) but only 1.3% in August(n - 76). June for adult
femalesand Julyfor juvenilesare periodswhenthe
demandfor calciumis at a peak.
MacLean(1974) notedthat DunlinsCalidrisalpinaon the
Finnishcoast have a mean inter-layingintervalof 36
hourscomparedwith24 in northernAlaska. He
suggestedthat generalfood availabilityduringthe egglayingperiodwas betteron the Finnishcoastalmudflats
comparedto Alaskanuplandtundraand the shorter
Alaskan layingintervalwas attributableto abundant
lemmingskeletalremainsthere. Thus layinginterval
mightnotbe regulatedby overallenergyavailability,but
An analogousexampleof calciumdeficiencyduringthe
nestlingperiodhasbeendescribedfor CapeGriffon
VulturesGypscoprotheresin southernAfrica(Houston
1978; Richardsonet aL 1986). Here, SpottedHyaenas
Hyaenahyaenaassumethe rolefor vulturesthat lemming
predatorsplayfor sandpiperson the tundra,the provision
of bone fragmentsof manageablesize. In the absence of
bone-crushing
hyaenas,there are no bonefragmentsat
carcassesfor parentsto feed to juvenilevultures. As a
result,these sufferdebilitatingbone deformitiesdue to
lackof calcium.Furtherevidencethatcalciumis required
by developingyoungare providedin studiesby
Douthwaite(1976) of youngPied KingfishersCerylerudis
whichdigestedfishboneswhereasadultsregurgitated
them in pellets,and by Seastedt& MacLean(1977) of
youngLaplandBuntings,whichwere fed lemmingbones
and teeth and egg shell.
rather by abundance of a limitingnutrientwhich, in the
case of egg production,
couldbe calcium.
The dailyfood intakeof layingfemale Dunlinwas
estimatedby Norton(1973)to be 16.5 g. The average
calciumconcentration
of tipulidlarvae,the mainpreyof
Dunlinat thistime,is 0.35%, suggesting
a dailycalcium
intakeper day of 0.06 g. A Dunlinegg contains0.24 g of
calcium. Assuming100% efficiencyof calcium
assimilation
(notingthat 70% is the approximateretention
35
MacLean'scalcium-from-lemmings
hypothesishas
apparentlynot been followedup. Giventhe renewed
interest in calcium deficiencies
in vultures and tits
(Richardson et aL 1986; Graveland et aL 1994), it is
certainlyworth pursuingin relationto sandpipers. One
weaknessof the hypothesisis how sandpipersfind
sufficientcalciumto breed successfullyin years when
there are few lemmingsand fewer lemmingpredators,as
occurredover muchof the Taimyr Peninsulain 1990
(Yurlov1993). Do the pelletsand scatsfromprevious
years stillpersistto providebonefragmentsand teeth?
Likewise, it would be useful to determine the calcium
budgetsof female arctic-breeding
geese and passerines.
REFERENCES
Douthwaite,R.J. 1976. Fishingtechniquesand the foodsof Pied
Kingfishers
on Lake Victoriain Uganda. Ostrich47: 153-160.
Graveland,J., van der Wal, R., van Balen,J.H. & van Noordwijk,
A.J.
1994. Poorreproductionin forestpasserinesfromdeclineof
snail abundance
on acidified soils. Nature 368: 446-448.
Houston,D.C. 1978. The effectof foodqualityon breedingstrategy
in griffonvultures(Gyps spp.). J. ZooL, Lond.186: 175-184.
MacLean,S.F. 1974. Lemmingbones as a sourceof calciumfor
arcticsandpipers(Calidrisspp.). Ibis 116: 552-557.
Norton,D.W. 1973. Ecologicalenergeticso! calidridinesandpipers
breedingin arc•cAlaska. Unpubl.PhD. thesis,Univ.of
Alaska.
Richardson,P.R.K., Mundy,P.J. & Plug, I. 1986. Bonecrushing
carnivoresand theirsignificanceto osteodystrophy
in Griffon
Vulture chicks. J. ZooL, Lond. 200: 23-43.
Roselaar,C.S. 1979. Fluctuatiesi aantallenKrombekstrandlopers
Calidrisferruginea. Watervogels4:202-210.
Seastedt,T.R. & MacLean,S.F. 1977. Calciumsupplementsin the
dietof nestlingLaplandLongspurCalcar•uslapponicusnear
Barrow, Alaska. Ibis 119: 531-533•
Simkiss,K. 1975. Calciumand avianreproduction.Symp.Zool.
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Summers,R.W. 1986. Breedingproductionof Dark-belliedBrent
GeeseBrantabemiclaberniclain relationto lemmingcycles.
BirdStudy33:105-108.
Underhill,L.G., Prys-Jones,R.P., Syroechkovski,
E.E.jr., Groen,
N.M., Karpov,V., Lappo,H.G., van Roomen,M.W.J.,Rybkin,
A., Schekkerman,H., Spiekman, H. & Summers,R.W. 1993.
Breedingof waders(Charadrii)and BrentGeese Branta
berniclaberniclaat PronchishchevaLake, northeastern
Taimyr,Russia,in a peakand a decreasinglemmingyear. Ibis
135: 277-292.
Yurlov,A.K. (ed.) 1993. Breedingconditionsforwadersin the
tundrasof the USSR in 1990. WaderStudyGroupBull.67:
57-62.
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