Changes Attributable to Pesticides in Egg Breakage Frequency and Eggshell Thickness in Some
British Birds
Author(s): D. A. Ratcliffe
Reviewed work(s):
Source: Journal of Applied Ecology, Vol. 7, No. 1 (Apr., 1970), pp. 67-115
Published by: British Ecological Society
Stable URL: http://www.jstor.org/stable/2401613 .
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CHANGES ATTRIBUTABLE TO PESTICIDES IN EGG
BREAKAGE FREQUENCY AND EGGSHELL THICKNESS
IN SOME BRITISH BIRDS
BY D. A. RATCLIFFE
Station,
Monks WoodExperimental
The NatureConservancy,
AbbotsRipton,Huntingdon
INTRODUCTION
Beforethe late 1940s it was a rare eventforbrokeneggs to be foundin the nestsof
and sparrowhawk
peregrine(Falco peregrinus)
(Accipiternisus),butfrom1951 onwards,
of clutchdepletionsin whicheggswereeither
bothspecieshave showna highfrequency
was not
found broken, or disappearedin circumstanceswhere human interference
birds
their
destroyed
indicatedas thecause. In mostinstancesit appearedthattheparent
own eggs,eitherby eatingor by breakingand/orejectingthem(Ratcliffe1958, 1960).
Scottishgolden eagles (Aquila chrysaetos)also showedan unusuallyhighfrequencyof
egg breakage,again attributableto parentaldestruction,during1960-63 (Lockie &
becamefrequentbefore
Ratcliffe1964). Althoughgolden eagle egg breakageevidently
1960 (Ratcliffe1960), lack of earlierobservationsmade accuratedatingof the change
An examinationof the eggshellsof peregrineand sparrowhawkhas recently
difficult.
decreasein weight(thickness)occurredin bothduring
disclosedthata highlysignificant
1946-50, and has been maintainedever since; golden eagle eggshellsshowed a less
decreasein weight(thickness),
datingfromaround1951
markedbutstillhighlysignificant
setsout in greaterdetail
The
to
paper
1966
present
1967a).
(Ratcliffe
and continuing
up
and changein eggshellweight,and discussesthecorrelatheevidenceforeggdestruction
declinein population
to thewell-established
tionbetweenthesephenomena;relationships
three
are
togetherwith the
in
these
examined,
success*
species
status and breeding
has
extendedto other
been
The
study
to
be
responsible.
believed
changes
environmental
of
other
bird
types.
and
a
wider
range
raptors
RECENT FREQUENCY OF EGG BREAKAGE
Beforeabout 1950, Britishperegrineshad a mean clutchsize of 3f5eggs and a mean
one egg
fledgedbrood size of 2 5 young(Ratcliffe1963a, 1967b).On average,therefore,
the main causes of
in everysuccessfulnestingfailed to produce a fledgedyoungster,
or deathof embryos)and nestling
of eggs(throughinfertility
failurebeingnon-hatching
Some failuresinvolvedbreakageor unexplaineddisappearanceof one or two
mortality.
eggsduringincubation(total failures,as throughthe takingof wholeclutches,are disregarded),but Table 1 suggeststhatduringthe firsthalfof thiscentury,partialclutch
cause of thedisparitybetweenclutchand brood size.
depletionwas an infrequent
By contrast,forthepost-1950period,in a total of 208 peregrineeyrieswitheggs,no
involvingbreakage
certainly
lessthaneighty-one
depletedclutcheswereknown(fifty-one
ten-foldincreasein thisphenomenon,from400
of one or moreeggs); an approximately
*
ofa population.
to thetotaloutputofyoung(i.e. productivity)
Breedingsuccessin thispaperrefers
67
68
Pesticidesand egg breakagein birds
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D. A. RATCLIFFE
69
to 3900. Duringtheperiod1961-66,mean brood size in northern
Englandand southern
Scotland(wherethemajorityof depletionshave beenfound)was only1P5and 1P7young
respectively,
comparedwiththeformernationalaverageof 2-5 young.Mean clutchsize
has shownno decrease,in termsofeggsactuallylaid, and thisfallin brood size is largely
an effectof increasedclutchdepletion.Since about 1950,egg breakagehas also been a
common cause of loss of entireperegrineclutches,and thereforeof total breeding
failureof manypairs.
Whiletheperiodafter1950is indicatedas theera offrequent
peregrine
clutchdepletion,
and used as thebasis forcomparisons,thephenomenonmayhave beguna littleearlier.
My firstrecordof egg breakagewas in 1949,and othersingleinstanceswerenotedby
D. Humphreyin Dorset in 1948,and by R. J. Birkettin Cumberlandin 1948 or 1949.
While observationalbias is possible,and breakageor disappearanceof peregrineeggsis
not a completely
newevent,clutchdepletionin thisspecieshas clearlyoccurredwithunprecedentedfrequencyin recentyears. Moreover,the more intensiveobservationsof
Birkett& Parr(Table 1) suggestthatmyown data underestimate
thescale ofthephenomenon,at least since 1961. While I have reportedthe more criticalseriesof records
available to me, thousandsof otherperegrineclutcheswere seen by ornithologists
in
Britainduringtheperiod1900-50,and it is inconceivablethateggbreakageon therecent
scale could have escapednoticeand comment.Such a phenomenonwould not be overlooked by the collectingfraternity,
yet when Nethersole-Thompson
& NethersoleThompson (1942a) wrote on eggshelldisposal, theyknew of only two instancesof
peregrineeggs beingbrokenbeforehatching.It is truethat small shell fragments
can
easily pass unobserved,and disappearanceof eggs withouttraceis even less likelyto
attractattention,yet the testimonyof severalexperiencedobserversleaves no doubt
thatfullclutchesof less than threeeggswereunusualbeforeabout 1950.
Full clutchesof two eggscan be acceptedas a normalthoughinfrequent
occurrence
(c. 50 ) but genuinefullclutchesof one egg wereformerly
rare,and the majorityof
recentincubatedsingleeggsprobablyrepresent
clutchesdepletedotherthanby human
I saw no incubated'singles'in thirty-four
intervention.
eyriesbetween1945and 1950,but
therewerefourteenin 176 eyriesbetween1951 and 1968,eightbeingaccompaniedby
definiteremainsof brokeneggs. Of the othersix 'singles',fivecould not be examined
closelyto look for accompanyingshell fragments;moreover,four of the six were in
territories
wherebreakagehas been provedin otheryears,and the othertwo werein
hauntslittledisturbedby humans.These six 'singles'have therefore
beenincludedin the
Appendixlist of depletedclutches.I have omittedfromthislistany instancesin which
collectingwas suspectedas a cause of eggsdisappearingwithouttrace;in thesesixty-one
depletedclutches,onlysixteeninvolvedsimplytheunaccountabledisappearanceof eggs,
and in ten of theseat least one egg was left.
When thepost-1950data in Table 1 are analysedaccordingto district,
the following
geographicalpictureemerges:
NorthernWales:
4 depletedclutchesout of 9 (440%)
NorthernEngland: 27 depletedclutchesout of 63 (430%)
SouthernScotland:38 depletedclutchesout of 96 (400%)
Highlands:
12 depletedclutchesout of 40 (300%)
Frequencyin the Highlandsas a whole is not significantly
different
(at the 500 level)
fromthatin the otherthreedistrictscombined.However,data on breedingsuccessare
available (mainlyfromD. Weirand A. Watson) fora morelimitedarea of thecentral
70
Pesticidesand egg breakagein birds
givinga total of forty-nine
Highlandsfortheperiod 1961-65; tenpairs bred regularly,
were successful,with an average of 2-5
nestingsobservedand of these, forty-three
youngper successfuleyrie.Althoughmosteyrieswerenot examinedclosely,onlythree
definiteclutchdepletionswereknown,and as mean brood size here equalled the prelowerin thecentral
of egg-losswas probablyconsiderably
1950nationallevel,frequency
Highlandsthanin otherpartsof Britain.
No criticaldata are availableforsouthernEnglandor southernWales,wheretheperegrinebreedingpopulationshave been close to extinctionsince 1961, and information
fromIrelandis also lacking.
sparrowhawknestsseen with
Data on otherraptorsare scantier,but in twenty-four
Englandbetween1943 and 1950,eggbreakagewas found
eggsin Norfolkand northern
Wales and
clutchesseenin northern
onlyonce,in 1947;whereaseightout oftwenty-seven
northern
Englandbetween1951and 1960weredepletedbybreakage(Ratcliffe1960and
unpublished).Moreover,I. Prestt(personalcommunication)has numerousrecordsof
clutchdepletion(ofteninvolvingegg breakage)in sparrowhawknestssince 1960, and
believesthatduringrecentyearsit has been a frequentcause of smallbroodsand failed
nestings.WhileCampbell(1960) reportedan instanceof eggbreakagein a sparrowhawk
nest in 1927, it is apparentthat the phenomenonhas occurredwith unprecedented
in thisspecies,too, sincearound 1950.
frequency
(1964) reportedthefollowingincidenceof eggbreakagein Scottish
Lockie & Ratcliffe
clutches;
goldeneagle eyries:1937-50,one in nineclutches;1951-60,fourin twenty-six
clutches.For an earlierperiod 1936-42, D. Nethersole1961-63,eightin twenty-two
golden
Thompson(unpublished)foundonlyone instanceof egg breakagein twenty-six
eagle eyriesseen witheggs.
Isolated instancesof egg breakagehave been notedin Britishnestsof kestrel(Falco
in
in 1966; D. A. Ratcliffe
in 1931; D. J.Jefferies
tinnunculus)
(D. Nethersole-Thompson
in
1968),merlin(F. columbarius)(D. A. Ratcliffein 1964; E. L. Roberts 1964), hobby
(F. subbuteo)(D. Nethersole-Thompsonin 1932), common buzzard (Buteo buteo)
in 1962; C. Tubbs in 1963-66)and osprey(Pandionhaliaetus)(D. Weirin
(D. A. Ratcliffe
of
to indicatetherecentfrequency
1964).These raptorshave notbeen studiedsufficiently
much
comto
attract
not
been
enough
frequent
thisphenomenon,but it has evidently
mentamongornithologists.
Amongstotherbirdswhichare themselvespredatorsof eggs,brokeneggs are rarely
found,but in the Corvidaetheyhave been reportedoccasionallyforthe raven(Corvus
duringthelast 10 years.The majorityofbirdspecies
corax)(D. Holyoak,D. A. Ratcliffe)
to
their
eggsby predators,so thatthefindingof brokeneggsin
loss and damage
suffer
ofthephenomenon
to
is
be
expected,and anychangein frequency
someof theirnests only
such as lapwing
species
localities,
In
some
in
predation.
an
increase
mightwell reflect
a substantial
lose
annually
and
apricarius)
(Charadrius
goldenplover
(Vanellusvanellus)
or
and thiscan
foxes,
gulls
crows,
first
by
predation
of
their
through
layings
proportion
be regardedas a normalsituation.Moreover,birdswhichare themselvespredatorsof
onlyamongthe
eggsmay have strongdefencesagainsteatingtheirown. It is therefore
raptorsthattherecentspate of eggbreakagestandsout as a strangeand unprecedented
event.
THE NATURE OF EGG BREAKAGE
clutchesknownpersonallyby thewriterare given
Details of sixty-one
depletedperegrine
D. A. RATCLIFFE
71
in the Appendix.These are givenas a sample; lack of space precludesmentionof the
manyotherinstancesreportedby otherobservers.
Breakageofperegrine
eggsis indicatedbypiecesof shell,usuallyin thenest,but sometimeson ledgesor thegroundbelow.Typically,thereare comminuted
angularfragments
to the egg complete
2-10 mm across, but the remainsvaryfromthe tiniestfragments
exceptfora gapinghole; oftenthereare large,crumpledpiecesof shellheldtogetherby
the liningmembranes.The egg contentsare usuallymissing,thoughoccasionallycongealed tracesare found.The majorityof depletedclutchesshow definiteevidenceof
breakage(Table 1 and Appendix),but eggssometimesdisappearwithouttraceand their
fateis thenobscure.Twice,however,afterseeingeyriesin whichno traceof shellor egg
came acrosstheremainsof an eggsomelittledistance
contentswas visible,I accidentally
away, on the open hillside.
Egg loss can occurbeforethefemalehas completedherclutch,or at any pointin the
incubationperiod; and it can involveanynumberof eggsin theclutch.Occasionallythe
butmoreusuallyeggsare lost one
wholeclutchappearsto be destroyedsimultaneously,
by one duringincubation,and Table 1 (footnote)indicatesthata higherproportionof
losses occurs when the incubationperiodis well advanced.Usually,once egg loss has
occurred,it sooneror laterinvolvesthewholeclutch.Onlyfourof mysixty-oneeyries
withdepletedclutchescertainlyproducedflyingyoung,thoughthe singleyoungsterin
anotherdied,and thirteen
eyrieswhichstillheldat leastone,possiblyviable,eggwerenot
re-visited.
In forty-four
depletedclutchesitwas certainthatno youngwerereared,and in
onlytwo of thesewas humanrobberyof remainingeggsknownor suspected.In fiveof
theseforty-four
eyries,the remainingeggs (fourc/l, one c/2) were addled and in two
more,singlefertilesurvivingeggs were deserted.The taking,forchemicalanalysis,of
clutcheswhich
singlefresheggscould have beenan additionalcause offailurein thirteen
producedno young,thoughin tenof theseeyries,all theremaining
eggswerelost-sughad theybeen left.
gestingthatthetesteggswould probablyalso have been destroyed,
incubatedfirstclutchesusuallylay second
Peregrineswhichlose freshor onlyslightly
clutchesafteran intervalof 16-26days(D. Nethersole-Thompson,
personalcommunication; Walpole-Bond1938),butnormallytheyseldom'repeat'whenincubationofthefirst
eggswas faradvanced.In the majorityof clutcheswhichlose all theireggs,loss of the
last egg occurswhenincubationis welladvanced,and thechanceof repeatsbeinglaid is
loweredaccordingly,
althoughin one instance(Appendix,no. 45) a repeatwas laid after
the remainingaddled egg of thefirstclutchhad evidently
been incubateda fullmonth.
While the truefrequencyof repeatclutchesfollowingfailureof firstlayingsthrough
depletion(as distinctfromhumanrobbery)is notknown,itis unlikelyto be high.Loss of
a wholeclutchin themannerdescribedthususuallyspellsnestingfailurefora peregrine
pairfortheyearconcerned;evenwhen'repeat'clutchesare laid, theseare likelyto suffer
the same fateas thefirstlayings.My own recordscontainthreeinstancesof peregrines
replacingclutcheslostbydepletion;in one (no. 25) therepeatalreadycontaineda broken
and theothertwo (nos. 45 and 52) eventually
eggwhenfirstseenbut was not re-visited,
failed.I have, however,heard of severalreliableinstancesin whichyoungwerereared
from'repeats'afterthefirstclutcheswerebroken.
The patternof clutchdepletionis thus extremely
variable,but the net effecton the
peregrinepopulationis a loweringof outputof flying
youngaccordingto thefrequency
of egg loss.
Breakageof goldeneagle eggs is usuallymarkedby the presenceof numerouscomminutedshellfragments
in theeyrie,thesebeinglarger(5-20 mm)thanin theperegrine,
72
Pesticidesand egg breakagein birds
thoughrelativelyof similarsize. Sometimeslarge pieces of shell are found,but the
contentshave usuallygone. In mostinstances,the whole clutch(usuallytwo eggs)was
destroyed,but in one eyriewithtwo addled eggs,theremainsof a thirdegg werefound
some distancefromand below thenest.As thegoldeneagle seldomlays 'repeats'under
any circumstances,
egg breakagein thisspeciesusuallymeanstotalbreedingfailurefor
thepairconcernedin thatyear,and was evidently
an important
factorin thesharpdecline
in breedingsuccessof thisspeciesin thewesternHighlandsduring1961-63.
Brokenremainsofsparrowhawk
eggsare as oftenlyingat thefootofthenesttreeas in
thenest.Usuallytheyare comminuted
fragments
less than10 mmacross,butoftenthere
are largerfragments
and I. Prestthas recordsof eggswithonlyslightdamage,and still
containingmost of the contents,lyingbelow the nest as thoughsimplytipped out.
Eggshellshave occasionallybeen foundat some distancefromnestswhichthemselves
containedno traceof eggs.In thisspecies,egg breakageis onlysometimesthecause of
totalbreedingfailureforthepairsconcerned:out ofnineinstances,sevenofthenestsstill
containedat least one incubatedegg whenlast seen,and I. Prestthas knownyoungto
fledgefromseveraldepletedclutches.Even so, egg breakagewould seem to contribute
strongly
to therecentincreasein nestingfailuresin thisspecies,and certainly
to reduced
total outputof young.
Most of theisolatedinstancesof brokeneggsin otherraptorsinvolvedthefindingof
comminutedshellfragments
in or beneaththenest.The generalsimilarity
of appearance
of the shell remainsin all theseraptors,but especiallyin peregrine,goldeneagle and
sparrowhawk,
suggeststhattheproximatecause ofbreakageis thesameforeach species.
PARENTAL DESTRUCTION
AS THE PROXIMATE CAUSE OF EGG BREAKAGE
In 1951,whenre-visiting
a Lakeland eyrie(Appendix,no. 2) which3 days beforeheld
threefresheggs,I watchedthefemaleperegrine
eatingone ofherowneggs.Afterflushing
her,I foundthe scrapecontainedlargepieces of shell,wetwiththeremainsof theconofanotheregg,withcongealedtracesofyolkand
tents,and also theground-upfragments
albumen,indicatingthatit had beenbrokenat leasta day.The thirdeggwas undamaged.
In 1952,P. Kimberand J. Robson also watcheda femaleperegrine
eatingherown eggin
a NorthWales eyrie.
For manyyearsafterthis,therewas no directproofthatotherbrokeneggshad been
eaten by theperegrinesthemselves.The shell remainsdiscoveredin manyothereyries
and largercrumpledpiecesfoundin eyrie
closelyresembledthecomminutedfragments
was oftensuggestedbyothercircumstances,
suchas thebreakno. 2. Parentaldestruction
age of eggs one by one, withoutensuingdesertion,and the brooding(by at least three
females)of the brokenremainsof entireclutches.Then, in 1966, in a Galloway eyrie
(Appendix,no. 50), fromwhichthebroodingfemalewas flushed,I foundtwoeggs,large
ofthesamebroken
piecesofshellfroma third,and a castingcontainingsmallerfragments
eggshell.The castingwas certainlya peregrine's,foramongstthefeathermatrixwas a
evidenceof egg-eating
homingpigeonring.I regardthisas further
by parentperegrines.
The twoshatteredeggsfoundawayfromeyries(Appendix,nos. 5 and 23) appearedto
have had theircontentseaten.Eggs whichdisappearwithouttracecould wellbe carried
fromtheeyriebeforebeingeaten,the remainslyingunseenon the adjacenthillside,or
consumed.
theycould be entirely
has beenknownbefore.Nethersole-Thompson
& NethersoleEgg-eatingbyperegrines
D. A. RATCLIFFE
73
Thompson(1942a) recordedthatP. M. Meeson watchedan Irishperegrine
eatingone of
itsown eggsin 1914,butthisegghad beendamagedpreviouslyby a fallingstone.At the
famouseyrieon the Sun Life buildingin Montreal,in 1949,thefemalewas seen eating
of othershad been found,and a secondclutchdisappeared
an egg aftershellfragments
whichsuggestedthattheperegrines
in circumstances
had eatentheeggs(Hall 1955).The
brokeneggfoundby E. Blezardbelowa Lakelandeyriein 1924had probablybeeneaten,
thoughthe femalewas sittingon foureggs in this nest; and in 1927, D. NethersoleThompsonsaw a Sussexeyriewiththreeslightly
incubatedeggsand theshellfragments
of a fourthegg clearlymatchingthe comminutedremainsI have so oftenfound.
Egg-eatinghas not actuallybeen witnessedin the otherraptors,thougha sparrowhawkwas seento hole one ofitseggswithitsbill and thento tipthedamagedeggout of
thenest(M. E. Greenhalgh,personalcommunication
to I. Prestt).In theinstanceofegg
breakagein a Scottishospreynest,a castingof theparentbirdcontainedfragments
of
shellwhichexactlymatchedthelargerpieceslyingat thefootof thenest tree(D. Weir,
unpublished).Otherwildbirdspeciescertainly
eat theirowneggson occasion(e.g. thejay
(Garrulusglandarius)Goodwin 1956), and the phenomenonis well knownin domestic
fowl.A male heron(Ardea cinerea)underclose observationwas seen severaltimesto
incubationbypiercingan egg,tastingthe contentsand thenflicking
interrupt
theremains
out of thenest(Millstein,Prestt& Bell, in press).
Two considerations
arise; first,theremay be otherimportantdirectcauses of clutch
and secondly,parentaleggdestruction
is itselfpresumably
depletionbesidesegg-breaking,
theexpressionof otherindirectcausativefactorswhichstillhave to be identified.
Moreover,a factorwhichcan be a directcause of egg breakagemay also operateindirectly,
is to determinethe relative
throughits effecton behaviour.The problem,therefore,
importanceof parentaldestructionas a cause of clutchdepletion,and to identifythe
factorsresponsibleforthisbehaviour.
underlying
OTHER POSSIBLE CAUSES OF EGG BREAKAGE
Predationcannot be acceptedas a probable frequentdirectcause of egg breakagein
fewauthenticrecordsof non-humanpredatorsraiding
raptornests.Thereare extremely
thenestsof Britishraptors,and thereis no evidenceof a significant
increasein possible
predators,or of a changein behaviourof thesepredators,after1950,in the areas conthateggs of peregrine,sparrowhawkand goldeneagle were
cerned.Recentstatements
destroyedbycrowshaveinvariablyturnedout to be surmisesbased merelyon thefinding
of brokeneggshells.
It has been suggestedthatthe increasein raptoregg breakageis connectedwiththe
In thearea wheremostclutch
post-1945increasein humaninvasionof thecountryside.
depletionswerefound,therehas been collectingof raptoreggsfornearlya century,
but
thispaperdeals explicitly
withinstancesofeggloss whichcannotbe attributed
to
directly
humanintervention.
Collectorsseldomtake onlypartof a clutch,and it is inconceivable
thatpeople could be directlyresponsibleforegg breakageon thescale described.There
fromcasual humandisturbance.
are, however,thepossibilitiesof adverseindirecteffects
From suchanalogiesas theeatingofyoungbytamerabbitsthroughhumandisturbance,
it could be that,whileparentalegg-eating
is indeedtheusual proximatecause of clutch
depletion,it is a stressreactioninducedby the presenceof humansat or neartheeyrie.
Armstrong
(1947) has cataloguedinstancesof both egg and nestdestruction
by parent
reactions'usuallyoccasionedby human,
birds,and regardstheseas typical'displacement
74
Pesticidesand egg breakagein birds
oftheincubate.g. suddenflushing
is thatsuchinterference,
presence.Anotherpossibility
ing bird,could increasethe chancesof accidentaldamage to eggsin the nest.It is also
could eithermake the ownersdeserttheirnests,wherepossiblethathumandisturbance
upon predatorswould destroythe eggs; or simplythatpredatorssuch as crowswould
have a greaterchanceof raidingnestswhenthedisturbedownerswereon thewing.
as an invalid
Thereare twomainreasonsforregarding
thiskindofhumaninterference
explanationof theegg breakagephenomenon.First,thisincreasein humandisturbance
is verylocal, and manyinstancesof clutchdepletionwerein remotecountryor sequesteredplaces wherefewpeople everpenetrate;moreover,manyof theraptornestscontainingbrokeneggsshowedno signsof havingbeen visitedpreviouslyby otherhumans
duringthe same season. Secondly,many raptornestswere subjectedto considerable
humandisturbancebeforethelast war,but withoutegg breakageresulting;thisdisturbance involvedthedeliberateand oftenrepeatedvisitingofnests,or thecasual and excessive disturbanceof nestinghaunts,such as that obtainingon some of the Kent and
before1939.
Sussex cliffsregularlyoccupiedby breedingperegrines
In Cornwall,Treleaven(1961) foundthat after1955 the failureof certainperegrine
eyriesto produceyoungcoincidedwiththe appearanceof extrafemales,whichsometimesfoughtwiththeestablishedfalcons.This antagonismwas usuallythepreludeto the
desertionof the particulareyriesand, althoughthese were not examinedclosely,by
it has been a not
implicationthe eggsweredestroyedor abandoned.In manydistricts,
ofeithersex,to appear
infrequent
event,bothbeforeand after1950,fora thirdperegrine,
whenthe occupyingpair are flyingaround afterbeing disturbedfromtheireyrieby
and occupants,but sometimes
humans.Usuallythereis no antagonismbetweenintruder
(unfightingoccurs. Before 1939, Walpole-Bond (1938) and Nethersole-Thompson
interaction
denseperegrine
population
amongsttheparticularly
published)notedfrequent
of the Sussex coast; theyfound that some intruderswere toleratedand otherswere
attacked,but egg breakageremaineda rare event.In 1936,W. C. Lawrie (see Blezard
1946) photographedtwo femaleperegrinesstandingtogetheron a Lakeland eyriewith
foureggs,one birdbeingin an aggressive
pose, butfouryoungflewfromthiseyrie.I have
betweenthe occupantpair
knownthreeinstances,all in southernScotland,of fighting
and an intruding
peregrine:in thefirst,in 1949,therewas an eyriewithone of theeggs
broken(Appendix,no. 1); whilein the othertwo,in 1960 and 1966,the occupantshad
eitherfailedto lay or losttheireggs.D. Weir(in preparation)also foundthatan instance
in Speysidein 1968was associatedwithpersistent
of nestingfailurebya pair ofperegrines
interference
by an intruderfemale.
The associationof nestingfailurewithintraspecific
interactionthusappears to have
been mainlya featureof recentyears.It is doubtfulwhether'intrusion'at eyrieshas increasedgenerally,and myown observationsdo not suggestthatit is a normaleventat
eyrieswithdepletedclutches;but perhapsbirdswhichhave brokentheirown eggs or
failedto lay mightbe inclinedto visitand disturbneighbouring
pairs. Obviously,any
scuffles
at eyriescould easilydamageeggs,theintruder
mightbreakthem,or stressmight
develop in the owners,causingthemto destroytheirown eggs. However,even if the
oftheabove kind,
ofeggbreakagewereassociatedwithinteractions
recenthighfrequency
been
an
in
theremust necessarilyhave
change populationbalance or
unprecedented
in
has
to
be
turn.
Such
effects
and
this
have not been
intraspecific
explained
behaviour,
with
Potts
found
that
were
correlated
for
other
they
raptors,though
(1968)
suggested
the
in
shag(Phalacrocoraxaristotelis).
egg breakage
interaction
could
In conclusion.whilepredation,humandisturbanceand intraspecific
D. A. RATCLIFFE
75
accountforoccasionalor local egg breakagein raptornests,theyare totallyinadequate
as a generalexplanation,bearingin mindthe scale of thisphenomenon.The following
in theraptorsconcerned,
a prevalentchangein eggshellthickness
section,demonstrating
moreor lesscoincidentin timewiththeonsetofwidespreadeggbreakage,makesparental
destructionan entirelyfeasiblegeneral explanationof this phenomenon,though it
the searchforan ultimatecause.
throwsback stillfurther
DECREASE IN EGGSHELL WEIGHT
An examinationofeggshellstakenfromvariouspartsof Britainduringthelast 100years
been a highly
and goldeneagletherehas recently
sparrowhawk
showedthatin peregrine,
and widespreaddecreasein eggshellweight,withoutanyparallelreductionin
significant
1967a).Measurements
size,and thatthischangehas beenmaintainedeversince(Ratcliffe
eggshells(see Appendix,p. 112) revealedthatthis
of severalperegrine
and sparrowhawk
changehas involveda decreasein shellthickness,but thatthedecreasein weightis not
also be involved.
whollyaccountablein thisway; decreasein shelldensitycould therefore
Both kinds of changeimplydecreasedstructuralstrengthof eggshellsand, hence,increasedchancesofaccidentalmechanicaldamageto eggsin thenest,as wellas metabolic
changein theparentbird.McNally(1965) foundthatin domesticpoultry,thepercentage
as the eggshellweightdecreasedfrom6-0g to
of eggscrackedincreasedlogarithmically
3 5 g and thattherewas an incidenceofcrackingsubstantially
higherthannormalin eggs
withshellsmorethan0-6 g below thecalculatedweightforthesize. Eggshellsweighing
over6-0g wereseldombrokenundergood handlingconditions.
The parameterused to measureeggshellsin thisstudyexpressesrelativeweightand is
knownas 'the eggshellindex'; it is explainedin theAppendix(p. 113).
Peregrine
Eggshellindex in this species shows a sudden and unprecedenteddecreaseduring
1946-48 (Figs. 1 and 2). Values for eggs takenfromvariousparts of Britain(mainly
southernEngland,northernEngland and southernScotland) during1947-69 are, on
Britishand
average,19 1% lessthanthosefora sampletakenduring1900-46.Forty-nine
in
p.
Ootheca
(see
Appendix,
Wolleyana
(1845-65)
continental
Europeanperegrineeggs
from
different
the
1900-46
British
sample;
not
show
mean
index
significantly
a
111)
moreoverthedecreasewas foundwithineach of thetwelvecollectionswhichcontained
pre-1947and post-1946eggshells.The eggshellchangeis thusnotan artifactconnected
of thespecimens.
withage or treatment
Before1947,therewereno significant
geographicalvariationsin mean peregrineeggshellindexwithintheBritishIsles. Since 1947,eggshellsfrominlandareas of thecentral
and easternScottishHighlandshave showna muchsmallerdecrease(4.40 O) in meanindex thanthosefromotherpartsof Britain(Table 2). In fact,theonlypost-1946eggshells
examinedwhichcould be describedas havinga 'normal'indexare eightof the sixteen
specimensfromthispart of Scotland (Fig. 1). All ten of the post-1946eggsfromthe
westernHighlandsare of sub-normalindex.
Sparrowhawk
overalldecrease
The situationin thisspeciesis similar:a suddenand unprecedented
froma fallin weight
in mean eggshellindex(17-2%) during1946-50,resultingentirely
(Figs. 3 and 4). Whileno recentHighlandeggshave been examined,veryfewpost-1947
Pesticidesand eggbreakagein birds
76
eggshellsof'normal'indexhaveyetbeenfound;buteggshellsfromsouth-eastern
England
have showna significantly
greaterdecreasein index(2-9" against13-9y0) thanthose
fromotherdistricts,
althoughno regionalvariationwas apparentbefore1947(Table 3).
Goldeneagle
Fewer data are availableforthisspecies,especiallyduringthe earlypost-warperiod,
and thoughtherehas been a highlysignificant
decreasein meaneggshellindexof 9.900,
The earliestpost-1946specimen
theonsetofthischangecannotbe datedwithconfidence.
2-302-20-
2190
1
1.* t
-CP
E E
*
1.80 -:;.!i,j
E1-70-
.
.
.*
1~
~
8... 0
%IS
*
~
.
3
0
;iy
,
*
.*
.
o
60
1-
;
1-50 -.:
.
140 :-;
130 -.
1-20I 10
1*00
1900
1910
1920
1930
Year
1940
1950
1960
1970
in Britain.0,
index(relativeweight)of theperegrine
FIG. 1. Changein timeof eggshell
fromtheCentralandEast ScottishHighlands;*, eggshellsfromotherdistricts
Eggshells
(see Table 2).
availablefromwesternScotlandwas in 1951and had an indexof 2-83; a clutchfromthe
same territory
in 1952 had a mean indexof 2-82. Eggshellsof sub-normalweightwere
regardedas theonsetof
subsequentlyusual in thisregion,so that 1951is provisionally
change.However,the decreaseapplied to eggsfromwesternScotlandonly,thosefrom
thecentraland easternHighlandsshowingno change(Table 4).
Otherspecies
The studywas extendedto theeggsof otherraptors,and a widerrangeof otherbird
to
and ecologically.
The studywas,however,confined
bothphylogenetically
typesdiffering
c'J
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78
Pesticidesand egg breakagein birds
mediumsized or largebirds,as the delicateeggshellsof smallspeciespose problemsin
measurement.
The resultsare givenin Table 5. No geographicalsub-division
was made
forthesespecies,becauseeithertherewereno indicationsofregionalvariationin eggshell
indices,or the data weretoo fewto testthispossibility.The kestrelshoweda smaller
decreasein mean eggshellindex(4.90 .), beginningin 1946,whilethemerlinand hobby
showeddecreasesof 12-7y.and 5-2y. respectively,
beginningin 1951 and 1952. In all
threespeciesit appearsthattheeggshellsofcertainindividualshave undergonea marked
Table 2. Comparisons
ofperegrineeggshellindicesbetweendifferent
periodsand regions
Regionand
period
Mean
index
+ S.E.
(1) All regionsof
1-866
+ 0-021
Britainand
northern
Europe1847-65
(2) All regionsof
1-836
? 0007
BritishIsles
1901-46
(3) All regionsof
BritishIsles
1901-46
(4) All regionsof
BritishIsles
1901-46
(5) All regionsof
BritishIsles
1901-46
(6) All regionsof
British
Isles
1901-46
(7) All regionsof
British
Isles
1901-46
(8) All regionsof
BritishIsles
1901-46
1P836
? 0007
1-836
+ 0007
1-836
+ 0007
1P836
0 007
1-836
?0 007
1-836
? 0007
No. of
eggs
Regionand
period
49 All regionsof
BritishIsles
1901-46
509 All regionsof
BritishIsles
(excl.Centraland
East Highlands)
1947-69
509 Centraland
East Highlands
1949-69
509 WestHighlands
ofScotland
1956-68
509 Southern
Scotland
1958-69
509 Northern
England
1947-69
509 Wales
1947-54
509 Southern
England
1947-59
00
Mean No. of
Significance
of
index
eggs differ- difference
+ S.E.
ence betweenmeans
(t-test)
1-836 509
-1-6
Not
? 0007
significant
1-485
+ 0011
211
-19 1
<0 001
1-755
? 0 037
16
-4-4
< 0 05
1-414
+ 0-028
10
-23.0
< 0 001
1 432
+ 0-023
29
-22-0
< 0 001
1-473
? 0-020
79
-19-8
<0 001
1-628
13
-11P4
<0 001
1-503
+ 0-014
75
-18-1
<0 001
+0-051
in eggshellindicesfordifferent
Thereare no significant
differences
regionsoftheBritishIsles before
1947,butas someregionalsamplesare small,theoverallBritishmeanindexhas beenusedas thebasis
of comparison
forthisearlierperiod.
decreasein index whereasthose of othersare unchanged.There is not a significant
decreasein thecommonbuzzard,thoughin thisspeciestheeggshellindexseemsto show
an unusuallyhighvariancebothbeforeand after1947.OnlyeightrecentBritisheggshells
are availablefortheosprey,but as theyshow a 21P24%decreasein eggshellindexcompared withan oldersample,thisis clearlya speciesin need of further
study.
Among the Corvidae,the ravenshows no significant
change,but in both rook and
carrioncrowthereis a smallyetsignificant
decreasein eggshellindexof 5.000 and 4800
and blackThreemoorlandbreedingspecies,thegoldenplover,greenshank
respectively.
D. A. RATCLIFFE
79
180 170 160
0 -
60
;
*~~~~~~~~~~~~~
~~~~I50
*
1 ?
150 _-* E .:
_
.,,,
* .
* XP
.
0
*0
0
J
*Cs
g
~0?
;
120~~~~~~~~~~~~~~~~~~
-
s
*~~~~~~~~~~~~~~~~
O
O
"0 J
10
1*0~~~~~~~~~~~~~~~~~~~~~~~~~0
*s
.
I*30
"
oo
so
0
*
"
*
O
"
oO ?
0E
*+x".
9
as0~~~~~~Ya
_
1a,Eghel
30
pi
(1) Stet
4
C
EnGl02?
(1
(2)
eg EnlnT pi an3).
rmot-astr
id
920
6
England
South-east
+
0
013
?0013
1-418
68
+0-00
1902-46~~~~~~~~~~~~~~~~~C
Ise
(3l Oh regionis
(2 outhEagstel f
()AlRegionsa
British
Isles
1902-46
1942
230
+
0-0
+ 05
No
c
+001
England~~~~~~~~~~~~~~~~C
Briis
0
fromohrdsics(e
eg
d
tigicn
68
1ot-eas
101
England
tri
*, egseO
ine
Ohregos
1902-46
England
South-east
Enln
20
+0010~~~~0n
1-121~co
010
1976
Brts
+
145
0 008
129
+05
No
significant0
0
-0f9
00
4
<01
0
cm01
Ise
i
42
20
her
418 68thestrSouth-asta
423
298n
ofRegions
All
a178
? 0008o gg Britis Isles
0
bw
regions000
121 frm00edsrit(e
-2gsell
129
279n
?r0008fernc
-172
<0%igifca1
1947-67
headed gull,showno significant
change.Of thesea birdsstudied,thekittiwake,
razorbill
and guillemotshowno significant
change,buttheshagshowsa12s3a decreasein eggshell
index.The eggshellchangein rook,carrioncrowand shaghas notbeen datedaccurately,
0
0
(p
0
0
LC)
8
.
*
*
0
0~~~~~~
-
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*
o C0o
*.o
e
*-
*
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% ~~0
0~~~~~~~~~
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0
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9)
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C)
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oO
??0
o
o
~ ~ ~ ~ ~
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3.
;.
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et;
*
6
.
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.
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~~~
rO
N
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00
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0
a 0
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00
0
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9) wo
o
0 a
?ooo8
o. o
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0
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~~~~~~~~~00
~~~~~
0)
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-6)
+
N- a
-
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0
a
p
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10 a
-~~~~~
(b)
Ia 0!eM
--
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a
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93
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aa
a?O
O
Cl)
0
00
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OO
0 0
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_~~~~~~~~~~~~~~~~~~~~~~
~~~t~~~~~t
(0
Ol
9
o8
ooc
0
0
*
*00
?
a
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o
dO
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a
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9
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81
D. A. RATCLIFFE
as thesamplesavailabledo not covereach consecutiveyear,butin all three,changeafter
1947is indicated.
(Ratcliffe1967a) thateggshellsof merlin,hobby
This revisionof a previousstatement
and carrioncrow had shownno changein weightresultsfromexaminationof much
largersamplesforthesespecies.
periodsandregions
ofgoldeneagle eggshellindicesbetweendiferent
Table 4. Comparisons
Regionand
period
(1) WestScotland
1848-1946
Mean
index
+ S.E.
3-146
+ 0035
3.146
(2) WestScotland
+0 035
1848-1946
(3) Centraland east 3-137
Scotland
?0053
1949-67
(4) Centralandeast 3-164
? 0-032
Scotland
1855-1946
No. of Regionand
period
eggs
84 Centraland east
Scotland
1855-1946
84 WestScotland
1951-65
22 WestScotland
1951-65
45 Centraland east
Scotland
1949-67
Significance
No. of
%
eggs differ- ofdifference
means
ence between
(t-test)
Not
+0 6
3K164 45
significant
+
?0032
Mean
index
+ S.E.
2-834
+0054
2-834
+ 0 054
27
-9 9
< 0 001
27
-9 7
< 0001
3-137
22
-0.9
+ 0053
Not
significant
THE CAUSES OF THE EGGSHELL EFFECT
Chemicalanalysisof 30-50 yearold specimensshowedthatoldereggshellspreservedin
collectionsconsist,on average,of about 900o calciumcarbonate,theremainingfraction
beingshellprotein(Tyler& Geake 1953),adherentshellmembranesand residualfilmof
contentsleftafterrinsingwhentheeggswereblown.Comparisonof pre-1947withpostthatthedecreasein shellthickness
eggsanalysedin thiswayconfirmed
1947sparrowhawk
thecalciumcarbonatefraction.Change
or densityhas involvedmainly,ifnotcompletely,
raptorsis thusimplied.
in calciumcarbonatemetabolismof theaffected
Eggshellthicknessin birds is known to be affectedby severalfactorsunder both
conditions,and thineggshellsseemto be a reactivesymptomcomnaturaland artificial
of calcium,
diet,especiallydeficiency
mon to variouskindsof avian adversity.
Imperfect
eggs
but also of manganeseand vitaminD, causes domesticfowl to lay thin-shelled
(Sturkie1965). Shortageof food in a wildbirdspeciescould lead to productionof thinshelledeggs,butthereis no evidencefora declinein availablefoodsupplyfortheaffected
raptorsat thetimeand overthetotalarea concerned.
Sturkie(1965) mentionsthat age and geneticconstitutionaffecteggshellthickness;
be thatin thesewild species,the eggshellchange reflectsa general
could it therefore
ageing,or geneticshiftin thepopulation?Clutchestakenannuallyfromthesamefemale
peregrinein Devonshirefrom1924to 1929 showedthefollowingmean eggshellindices:
1924-179, 1925-185, 1926-178, 1927-199, 1928-193, 1929-199. This suggeststhat
diminishing
eggshellindex does not normallyoccur withinthe averagelife span of a
breedingperegrine,whichcan be put at less than the 6 years above (Ratcliffe1962).
Increasingaverageage of thepopulationis thusnotlikelyto be thecause of theeggshell
A substantialdecreasein shellindexwas, moreover,knownto occurin eggsof the
effect.
same individualoccupantsof threedifferent
peregrineeyriesduringthe criticalperiod,
of the
therebyrulingout thepossibilityof it beingdue to changinggeneticconstitution
population(Table 6).
82
Pesticidesand egg breakagein birds
~~~~~~~~~~~~~~~~~~~~~~~~~~~~o
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D. A. RATCLIFFE
83
Thereis some evidencethatstresscan cause decreasein eggshellthickness,but stress
is itselfa responseto other,externalfactors,themostrelevantofwhichhavealreadybeen
discountedas an adequateexplanationoftherecentprevalenceofeggbreakagein raptors
(p. 74).
My colleague,I. Prestt,is currently
thequestionofdiseasein wildraptors;
investigating
thisstudyhas involvedconsultationwithspecialistsin avian diseasesand post-mortem
examinationof severalhundredraptors.Disease is wellknownas a cause of thin-shelled
eggs,and theappearancein Britainoftwo suchdiseases,infectious
bronchitis
and Newcastlediseasein 1947does,in fact,givea fairlyexacttimecorrelation
withtheonsetofthe
eggshellchangein wild birdshere.Infectiousbronchitishas not been reportedin wild
birds,butNewcastlediseasewas knownto occurin a numberofwildBritishspecies.While
theeggshellsofinfected
wildbirdsmayhaveshowna decreasein thickness,
thewidespread
and persistent
eggshellchangereportedforseveralBritishraptorscan hardlybe attributed
to Newcastledisease,as thishas not been isolatedin anybirdof prey.Moreover,some
poultryinfectedby thisdiseasewerefoundto recoverfullhealth(and to lay normaleggs
Table 6. Changein eggshellindexin threefemaleperegrines
Year
EyrieA, Lancashire
EyrieB, Lancashire
EyrieC, Yorkshire
Clutchsize Mean index Clutchsize Mean index Clutchsize Mean index
1943
1944
3
4
2-03
1-97
3
3
1.90
1-86
-
1946
1947
3
1-36
2
-
1-49
3
3
1945
1948
1949
3
3
4
1-92
1-35
1-29
3
1-79
-
-
-
2-18
1-78
-
again),whereastheeggshelleffect
has continuedin someraptorsat an undiminished
level
from1947 up to the presentday. Finally,thereis no reason whygolden eagles and
peregrinesin the easternHighlandsshould have been exemptfromsuch an epidemic
disease while those in the westernHighlandswere infected-a necessarypostulateto
accountforthe differences
in eggshelleffectby the disease hypothesis.Thereis no evidence thatany otherdisease could have affectedBritishraptorson a widespreadscale
from1947 onwards.
All thefactorsmentionedabove completely
failto providean adequateexplanationof
theeggshellchange,bearingin mindits extremely
widespreadyetunprecedented
nature,
the patternof geographicalvariation,the synchrony
and otherremarkableparallelism
in severaldifferent
specieswithwidelyvaryingecology,and thewayin whichit has been
maintainedwithapparentlyunabatedstrength
sinceitsfirstappearance.Onlysome profound,widelypervasive,simultaneousand unprecedented
environmental
changeseems
adequate to account for this effect.Attentionnaturallyfocuses on the large-scale
environmental
pollutioncaused byman,showingrapidaccelerationduringthepost-1945
period.First,thereis therapidincreasein fall-outofradioactivematterfromatomicand
thermo-nuclear
explosions,beginningin 1945. Fall-out did not become a matterof
concernuntilthermo-nuclear
deviceswereexplodedin 1954,and itsgeographicalpattern
does notmatchthatofeggshellchange.In Britain,fall-outis highestin theheavyrainfall
areas of the northand westof Britain.This factorseemstherefore
unlikelyto be the
cause of decreasingeggshellindex.
84
Pesticidesand egg breakagein birds
The othermain increasein environmental
pollutionhas been the accumulationof
persistent
residuesof synthetic
organicchemicalsmanufactured
in largequantitiesand
used widely.Tyler(1950) has shownthatcertainorganicdrugs,suchas sulphanilamide,
caused a markeddecreasein eggshellthicknesswhenadministered
to domesticfowl,and
it is conceivablethata varietyof accidentalchemicalpollutantsmighthave thiseffect.
Althoughpollutionby inorganicsubstances,such as atmosphericsulphurdioxide,is
increasing(Mellanby1967)thisis nota newphenomenonand is notlikelyto be involved.
Environmental
contamination
by lead frommotorfuelsis now causingconcernin some
countries,
thoughthisis mainlya problemofurbanareas,and is unlikelyto haveshowna
sudden,spectacularincreasearound 1947. However,a notablefeatureof the post-war
world,includingBritain,has been the greatincreasein productionof complexorganic
chemicalsforindustry,
agriculture
and domesticuse.
and thecontribution
oftheseto riverpolluThe post-warincreasein use of detergents
tionis well known,but thesesubstancesgiveno groundsforsuspicionas the agentsof
eggshellchangein raptors.On theotherhand,attentionhas onlyrecently
been drawnto
the potentiallyharmfuleffectsof the persistent
poly-chlorinated
biphenyls,whichhave
beenfoundin tissuesoffish,eaglesand humansin Sweden,and werefirstdetectedin an
eagle(Jensen1966).Thesesynthetic
compounds,whicharewidelyusedin themanufacture
ofplastics,lubricantsand insulatingmaterialand are releasedunalteredintotheenvironmentin a numberof ways,have recentlybeen shownto accumulatewidelyin thetissues
ofwildbirds,includingraptors,in Britain.It is suggestedthatPCBs aretoxicresiduesand
constitutea potential
that,beingpersistent
organochlorine
compounds,theytherefore
hazardto wildlife(Holmes,Simmons& Tatton1967).WhilePCBs wereused industrially
before1939, theyhave showna substantial,thoughprobablygradual,increasein use
duringthepost-warperiod.Reynolds(1969),in discussingtheuses ofPCBs, suggeststhat
theymay have been used in pesticideformulationsto extendthe active life of these
caused by thepresenceof
chemicals.This authoralso discussestheanalyticaldifficulties
thatthepeaksobtainedbygas-liquidchromatography,
PCBs and considersthepossibility
and identified
as PCBs, could be condensationproductsof the metabolitesof organochlorineinsecticides.
of persistent
residuesof agriThe widespreadoccurrencein the Britishenvironment
culturaland otherinsecticidesand fungicidesis well known(Moore 1965a). Particular
noticehas beentakenin Britainof theorganochlorine
compounds,DDT, yBHC,dieldrin,
aldrinand heptachlor.In Swedentherehas been moreconcernabout contamination
by
residuesof organomercury
persistent
compounds,whichincreasedrapidlyin the 1940s,
a trendreflected
by levelsin raptortissues(Berget al. 1966). Similarincreasesin use of
and organosulphur
non-persistent
organophosphorus
compoundsalso occurredat this
that
certainof thewidelyused dithiotime,and amongthelattergroupthereis evidence
carbamatescan affecteggshellthicknessin poultry(Johnson,Waibel & Pomeroy1955;
Picco 1962).
The relevanceof non-persistent
pesticidesto raptorsis unknownand attentioninevittoxic
residuesknownto accumulatein thetissuesof raptors,
ablyfocuseson persistent
them
in
some of
relatively
largeand potentiallyharmfulamounts,e.g. pp' DDT (commercialDDT also containsop' DDT), and itsmetabolitespp'DDE, TDE; yBHC andother
isomersofBHC; HEOD (dieldrin);heptachlorepoxide; organomercury
compoundsand
between1963 and
PCBs. In Britain,tissuesand eggs of peregrinesand sparrowhawks
in detectableresidues,of DDE, whereasin
1968have showna consistent
preponderance,
the golden eagle, during1963-65, DDE and dieldrinwere usuallypresentin similar
D. A. RATCLIFFE
85
amounts.No eggor tissueofanyofthesethreeraptorswhichhas beenanalysedso farhas
been withoutone or otherof theseresidues,and themajorityhave containedboth. Of
799 liversor eggsof all Britishraptorsexaminedduring1963-67,9900 containedresidues
of DDE (Prestt1967). Though organochlorineresiduelevels are oftenless in other
species,Table 7 shows thatcontaminationby thesesubstancesaffectsa wide range of
of Britishbirdpopulationsby organoon contamination
Britishbirdtypes.Information
eggsexaminedin 1966showed0 3 ppmand
mercury
residuesis scanty,buttwoperegrine
pictureofcontamination,
nilresidues.Data on PCBs are too fewto givea comprehensive
eggsexamined(13% nil),2-15
butlevelsduring1967-69average1 80 ppmin 30 peregrine
sparrowhawkeggs (3500 nil). For the golden eagle, nineteeneggs
ppm in forty-eight
frominlandeyriesall showednilPCBs, butan eagletfounddead belowa westcoast eyrie
contained1700 ppm in its liver.
The organochlorine
pesticideresiduesand PCBs have preciselythatmaintainedperchangeresponsiblefordecreasein eggshell
vasivenesspostulatedfortheenvironmental
weightin certainBritishraptors.DDT and yBHC weredevelopedas insecticidesduring
to maintainhygieneamongstmilitarypersonnel,
the 1939-45war and used extensively
especiallythoseon activeservice.Whenthewarended,thewideruses ofDDT and yBHC
soon resultedin extensiveuse,forcontrol
wereexploredand exploited;theireffectiveness
and agriof insectpests of households,gardens,pets,farmlivestockand horticultural
culturalcrops.In 1945 and 1946,followingreleaseof DDT on thecommercialmarket,
numeroussuccessfulfieldtrialswere reportedin its applicationagainstinsectpests of
cropsand animals,and it is clearthatin 1946therewas alreadyconsiderablelocal use of
DDT as a sprayin orchards(Shaw 1946a, b; Massee 1945, 1946; G. H. L. Dicker,
In Shaw (1946a), J.G. Mitchell,reviewingsheepdip trialsof
personalcommunication).
DDT against blowflyand tick,reportedthat 'the success achieved has stimulateda
vigorousdemandamongfarmersforpreparationsforfielduse'.
The Cook Report(1964; p. 57) says 'DDT was firstavailable in theU.K. forexperibut
on fruitthereafter
mentaluse againstcroppestsin 1944-45.It was used commercially
treatment
an
economic
made
until
price
reductions
its use on fieldcrops was limited
propositionabout threeyearslater'.The same sourceindicatesthatyBHC had a similar
earlyhistoryto DDT; 'BHC was developedas an insecticidein Englandin 1942. Field
trialswerein progressin 1945-46.Because of thelow cost of thismateriallittletimewas
lost in applyingtheresultson a commercialscale; crudeBHC wirewormand fleabeetle
dusts were freelyavailable by 1947'. The scale of use of DDT and yBHC continuedto
and a growing
increaseas theyfoundapplicationto a wideningrangeofcropprotection,
use as sheepdips. After1955,themoretoxiccyclodienecompoundsdieldrin,aldrinand
as seed
use, particularly
heptachlorwereintroducedand foundwidespreadagricultural
these
last
to
In
of
wild
birds
attributable
deaths
1962,
following
catastrophic
dressings.
began to reducethe amountsbeingreleasedinto the
substances,voluntaryrestrictions
theseand furtherrethe Cook Report (1964) in formally
recommending
environment;
in reducingtheuse ofcyclodienes(Moore 1965b).
strictions,
probablyhad stillmoreeffect
Dieldrinwas widelyused as a sheepdip, sometimeafter1955,untilthisuse was banned
in 1966.
voluntarily
In reconstructing
of raptors,it is imporcontamination
thepictureof organochlorine
firstreacheda
tantto knowwhentheamountof chemicalreleasedintotheenvironment
quantityto
level highenoughto enterthesebirdsin the areas concernedin sufficient
is
of causal relationship
cause physiologicaldisturbance.
A correlative
patternsuggestive
not simplya matterof timingof residueintroduction,
but mustincludeamount,distri-
86
Pesticidesand egg breakagein birds
butionand circulation.Figuresforthemanufacture
and use of thefirstorganochlorine
insecticides
have notbeenfoundforGreatBritain,butin theUnitedStates,productionof
DDT was 15 000 tonsin 1945,risingto 32 000 tonsin 1950(Quaife,Winbush& Fitzhugh
extensiveapplicationsof DDT againstinsectpests,
1967). Foreseeingthe forthcoming
Wigglesworth
(1945) discussedthe implicationsand possible dangersof this for 'the
balance of nature'withintheinsectworld.Only3 yearslater,theaccuracyoftheprediction about use is confirmed
by the statementof Vogt (1948, p. 30) that'. . . biologists
throughoutthe world are alarmed by the widespreadand unselectiveuse of DDT'.
It is evidentthattheaggregateuse of DDT and yBHC in Britainwas considerablein
1946and thattheamountused increasedin each successiveyearup to at least 1950.The
adventand increaseof theseinsecticidesin theenvironment
thuscoincidedcloselywith
the onset of eggshellchange and its evidentlyrapid spread throughcertainraptor
populations.It is notat firstobvioushow thisenvironmental
changecould haveimpinged
upon wildraptors,forthelinkbetweenthetwoseemstenuousuntilDDT cameintomore
use in 1948.Whentheearlyuses of DDT and yBHC are examinedin
generalagricultural
detail,however,some probablelinksat once emerge.
An earlyapplicationof theseinsecticides
whichfoundenthusiastic
use was thedusting
of domesticanimalsand birdsagainstexternalparasites.The Veterinary
Record for26
October 1946 containsthe followingeditorialcomment,underthe heading'DDT and
gammexanein small animal practice':'A greatdeal of publicityhas resultedfromthe
DDT-and it is not surprising
developmentof thesepowerfulinsecticides-particularly
thattheend ofthewarhas seenthemarketing
ofverynumerousinsecticidalpreparations.
Many of theseare producedby reliablefirmsand the amountof the activeprincipleis
are now availableofvaryingcontentand
clearlydefined:on theotherhand,preparations
issued by "mushroom"firms.... We find,in fact,almosteverychemist,cornstrength
chandler,or generalstorestockedup withDDT preparations,easilypurchasableand
used upon animals,numbersof whichare unfortunately
indiscriminately
findingtheir
In the same issue,Kirk (1946) said 'It is to be regretted
way to veterinary
infirmaries.'
thatthegeneralreleaseof DDT has been extendedto thelaity,as we findalmostevery
little"general"shop or pet shop is sellingthesubstanceindiscriminately,
thepurchasing
cumulativeand cats are especipublicbelievingthatit is harmless.The drugis extremely
ally susceptibleto its cumulativeaction.'
This earlyveterinary
use ofDDT evidently
appliedto homingpigeons,althoughitwas
discontinued
later;Whitney(1961) listsDDT dustsand spraysas one ofthemosteffective
meansofcontrolling
ectoparasitesofhomingpigeons.Preparationsofan anti-feather-rot
creamcontainingyBHC are still(1969) availableto fanciers.From 1946 onwards,there
could thushave been a remarkablydirectlink betweenthesenew insecticidesand the
whichtakes(and took at thattime)the domesticpigeonas its principalprey
peregrine,
in
all
districts
southof theHighlands(Ratcliffe1963a). The writerfoundhoming
species
in
Lakeland
and Gallowayperegrine
pigeonrings every
eyriecontainingyoungwhichhe
examinedduring1945-48.This use of DDT could have been appliedto militarycarrier
pigeonsevenbefore1946,but it is not likelyto have becomewidespreaduntilafterthis
insecticidewas firstreleasedto thepublic,at theend of 1945.Agricultural
and horticulturaluses of DDT probablysooneror laterbecame a chiefsourceof DDE residuesin
theperegrine.
In the peregrine,thefirstsignsof decreasein eggshellweightmayhave been in 1946
(Fig. 1 and Table 6) but onlyone clutch(c/2),in Lakeland,was involved.In 1947,six out
of elevenclutches(eightLakeland,two Brecon,one Sussex) werewellbelowpreviously
D. A. RATCLIFFE
87
normalweight.All fourclutches(two Dorset,two Lakeland) examinedfor1948wereof
sub-normalweight;in 1949,offourclutches,three(twoLakeland,one Sussex)werelight,
but theother(Cairngorms)was of normalweight(Fig. 1). The availablesamplesforthis
to givean accurateidea of the
criticalperiodare thustoo smalland unevenlydistributed
incidenceand geographicalspreadof eggshellweightdecreasein thewholeBritishpereis necessary,
as Fig. 1 could be misleadingin itsimpligrinepopulation;thisqualification
cation of rapid eggshellchangethroughthewholepopulation.
The sparrowhawkdoes not normallytake homingpigeons,but preysmainlyon small
passerines,manyof whichfrequenthabitats,suchas gardensand orchards,whereDDT
foundwidespreadearlyuse. In thisspecies,one clutchout of eightin 1946was evidently
an area with
lighterthan normal(Fig. 3); it came fromthe outskirtsof Bournemouth,
Of sixclutchesin 1947,fourfromtheIpswicharea were
numerousgardensand nurseries.
werenormal.In 1948,ofnine
all light,buttheothers,fromDorsetand Nottinghamshire,
clutches,threewerelight(Surrey,Hampshire,Suffolk),two borderline(Surrey,HampSutherland).In 1949,ofeightclutches,five
shire)and fournormal(Dorset(two),Suffolk,
werelight(Dorset, Surrey,Hampshire,Suffolk(two)), and threewerenormal(Dorset
(two), Hampshire).Only by 1950 were all clutches(three)lighterthan normal.While
in theabove southerncountiesin
contaminationof some sparrowhawks
organochlorine
of
1946and 1947,fromsuburbanand horticultural
uses,is veryprobable,contamination
the whole southernEnglandpopulationis likelyto have been variableand incomplete
use of DDT and yBHC becamereallywidespreadand intensive.
untiltheagricultural
Althoughmore sparrowhawkeggs were available for the criticalperiod,compared
withthe peregrine,the datingof the eggshellchangein both speciesdependson small
samplesdrawnfromveryfewpartsofBritain.Untilmorematerialis foundand examined,
it is impossibleto tell how far thisevidencehas nationalor merelylocal significance.
whenthe data for both speciesare takentogether,theysuggesta wideNevertheless,
spreadand moreor less synchronous
phenomenon,at leastin England,coincidingin its
of these
insecticides
intotheenvironment
onsetwiththeintroduction
of organochlorine
birds.
but in the
Kestreleggshellsof sub-normalweightfirstappearedin 1946(in Wiltshire),
merlinno signofdecreasewas detecteduntil1951,and in thehobbynoneuntil1952.This
situationcorrelateswiththeenvironmental
forsomekestrelsin southernEngland
pattern,
frequenturbanand suburbanareas,whereasthishabitatis unusualformerlinand hobby
areas. It is thus
which,moreover,each spend at least halfthe yearin non-agricultural
likelythatpopulationsof thelast two specieswereless exposedto earlyorganochlorine
contamination
thanthoseof peregrine,
sparrowhawkand kestrel.
The widespreaduse ofDDT and yBHC in sheepdipsprobablygave an earlysourceof
forbirdswhichhabituallyfeedon sheepcarrion,notablythegoldeneagle
contamination
(in westernScotland),buzzard and raven.The last two specieshave shownno eggshell
change,and whilethegoldeneagle has undergonea markeddecrease,thelack of specimens for the period 1946-55 makes dating of the eggshellchange uncertainin this
species.Most of the recentgolden eagle eggshellsexaminedhave been post-1955,and
those analysedfrom1963-66 containedapproximatelysimilaramountsof DDE and
dieldrin(Lockie, Ratcliffe
and Balharry1969). Dating of eggshellchangein shag,rook
and carrioncrowis also uncertain.
However,for all speciesshowinga decreasein eggshellweight,it is certainthatthe
change occurredafterand not beforethe widespreadintroductionof organochlorine
insecticidesinto the environment.
It is possiblethattherewas interspecific
variationin
88
Pesticidesand egg breakagein birds
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90
Pesticidesand egg breakagein birds
in exposureand in sensitivity
to the
onsetofeggshellchangeaccordingto bothdifferences
earlierand laterinsecticides.
If therewereno morethana timecorrelationbetweenorganochlorine
insecticideuse
There
and eggshellchange,it would hardlybe justifiableto claim a causal relationship.
are, however,otherrelevantlinesof evidence.
First,thereis theevidenceof geographicalparallelism.The greaterdecreasein weight
of sparrowhawk
eggshellsfromsouth-eastEngland,comparedwiththosefromCumberland, Hampshireand Dorset,matchesthemoreintensiveuse of agriculturaland hortiin differences
in contaminationof the
culturalpesticidesin thefirstregion,as reflected
species(Table 7). In thecentraland easternScottishHighlands,eggshellchangeis slight
thatorganowiththefinding
(or nil) in peregrines
and nilin goldeneagles,corresponding
chlorinepesticidecontaminationof the peregrinethereis onlyabout a quarterof that
foundin otherregionsof Britain(Table 7); whileforthegoldeneagle,thelevelis onlya
tenthof thatfoundin thewesternHighlands(Table 7).
The case of the golden eagle is especiallyilluminating.In westernScotland this
residuesofsheepdips,
specieshabituallyfeedson sheepcarrionand so takesup persistent
thougheagles livingnear or on thewestcoast are also likelyto accumulateresiduesby
theirhabitoffeedingon sea birdsas well(Wormell1965).In centraland easternScotland,
wherethe supplyof wildpreyis good, eagles eat littleor no sheepcarrion,and in some
areas sheepare fewor absentanyway(Brown& Watson 1964).Whilecoastal eaglescan
takeup notonlyorganochlorine
pesticideresiduesfromsea birds(Moore & Tatton1965),
but also PCBs (Presttet al. 1970), those in inland districtsof the Highlandslive the
whichwould be virtuallypesticidefree,but forthe local
yearroundin an environment
use ofsheepdips.The inlanddistricts
ofthewesternHighlands,whereeggshellchangehas
occurred,forma vast wildernesscountry,remotefromurban and industrialcentres.
to imagine
Having discounteddecreasein food supply(Lockie et al. 1969),it is difficult
whatotherrecentenvironmental
changecould conceivablyhave occurredhere,exceptthe
of organochlorine
sheepdips.
verydirectone of introduction
Thereis growingexperimental
biochemicalevidencethatDDT, DDE and dieldrincan
cause decreasein eggshellweight.Calciummetabolism,
and therefore
eggshellformation,
in birdsis controlledby oestrogenand boththyroidand parathyroidhormones(Sturkie
1965). There is a considerablebody of evidence(Kupfer 1967) that in vertebrates
insecticidesin generalstimulatethe productionof liverenzymeswhich
organochlorine
degradethesteroidhormones,and thusdisturbmetabolismof oestrogen.Peakall (1967)
has shownthiseffectin domesticpigeons,withboth DDT and dieldrin,and concludes
thattheeffects
of thetwo chemicalsare additive.A possiblebiochemicalpathwayfrom
eggsis thus demoncontamination
by DDT and dieldrinto productionof thin-shelled
strated.
Jefferies
(1967, 1969) has showna delay in ovulation,decreasedegg weightand an
increaseinrelativeshellweightinBengalesefinches(Lonchurastriata)fedpp' DDT. These
resultsdemonstrate
a disturbanceof eggformationand suggestthatthefinalexpression
of physiologicalchangeinducedby DDT mayvaryaccordingto species.Jefferies
interbalance,producingapparent
pretshisfindings
as an effect
ofDDT on theTSH-thyroxine
in the bird. Jefferies
& French(1969) have shown that feedingsubhyperthyroidism
lethalamountsofpp' DDT to domesticpigeonscaused an increasein thyroidweightand
a reductionin colloid contentof thefollicles.These conditionsmay reflecta hyper-or
hypo-functioning
gland, and could connect with the eggshellchange in wild birds.
of
are knownin thisrespect,as theadministration
Interspecific
physiologicaldifferences
91
D. A. RATCLIFFE
on theoestrogen-induced
has beenfoundto have oppositeeffects
risein plasma
thyroxine
calciumin layingducksand hens(Hohn 1961).
Fig. 5 suggeststhat in the peregrinethereis a correlationbetweenincreasingtotal
organochlorine
pesticideresiduecontentof eggsand decreasingeggshellindex,up to the
residuelevel of about 10 ppm, above whichthereappears to be no markedeggshell
as it connectswiththe observation
change.The formof thisrelationshipis important,
withtimeshowthatthedecreasein eggshellweightin thisspecies(and thesparrowhawk)
i.e. no furtherdecrease afterthe firstfew years (Figs. 1 and 3)
ed a 'plateau-effect',
despite a continuingrise in organochlorinepesticideuse after1950. This lack of a
simplelinearrelationship,shownalso by Fig. 5, suggeststhatabove a certainlevel of
some otherphysiologicalmechanismmay beginto operate.It
residuecontamination,
is also possiblethateggswithshellsbelow a certainlevel of thickness,are brokenand
2 00 _
1.90 _
E
E
E I180.
^1
70
160
*
0
1-150 _
S
1-40 -
0
*~~
*
*
0
S
1 30 1 20 5
10
15
20
25
30
35
Total organochlorine pesticide residues (ppm )
betweenorganochlorine
pesticideresiduecontentand shellindexfor
5. Relationship
fromtheCentralandEastScottish
Highlands;
1963-69.*, Eggshells
eggsoftheperegrine,
fromotherregionsofBritain.
*, eggshells
FIG.
eatenso quicklythattheyareneverfound.The thinnest
and sparrowpost-1946peregrine
hawkeggshellsexaminedwouldcertainly
appearto be highlyproneto accidentaldamage.
It is also possiblethatparentbirdscontainingmorethan a certainresiduelevel do not
lay eggs.McNally(1965) foundthatdomestichen eggswithshellsweighingless than3-5
g werelostin thepoultryhouse.
resulted
It is, however,probablethattheincreasinguse of organochlorine
insecticides
in an increasingproportionof raptorpopulationsbeingaffectedand showingthe eggshellchange.
If thedata in Fig. 5 are analysedin two geographicalgroups,theperegrineeggshells
fromthe centraland easternHighlandshave a highermean index (1.75 against 1.46)
and lowermean residuecontent(2.78 ppm against 13-56ppm) than thosefromother
43
at P <0001 (t = 6-22and 5-22respectively,
beingsignificant
regions,bothdifferences
df). Fig. 5 also impliesratherwide variabilityin individualresponseat any level of
contamination.
92
Pesticidesand egg breakagein birds
Fig. 6 shows that thereis some correlationbetweentotal organochlorinepesticide
contentof different
speciesand percentagedecreasein eggshellindex.This graphcould
also reflectdifferential
environmental
exposureto contaminationor interspecific
differences in retentivecapacityfor residues,as well as a certaininterspecific
variabilityof
responseto these substances.The last possibilitycasts doubt upon any quantitative
inferenceswhich mightbe drawn fromexperimentalspecies about the physiological
effects
ofresiduelevelsin wildspecies.Moreover,thevariableenzyme-inducing
powerof
different
chemicalssuggeststhatthe simplearithmetic
sum of residueshas onlylimited
meaningas an indexof contamination.
21
20 19 -
* Peregrine(excludingEast and
Central Highlands)
18
17
* Sparrowhawk
16 15 -
V
14 -
-13
* Shag
,C
12-
c
10
g
9
* Merlin
* Golden eagle
(West Highlands)
8_
7 6_
5
* Rook * Carrion crow
* Kestrel
4 3 2* Kittiwake
I _
-I -2
-3
0
Buzzard
Raven
a *Raven
~~~~~~~Guillemotl
* Razorbill
Black-headed GulI
0-5
10
1i5
2 0
25
30
log ( Mean total organochlorine residues xlO
6. Relationship
betweenmeanorganochlorine
pesticideresiduecontentof eggsand
meanpercentage
changein eggshell
indexforfourteen
speciesofBritishbirds.A statistical
examination
of thedata has notbeenmadeas thetwoparameters
do notalwaysreferto
thesamesamples.
FIG.
The possibleindividualcontribution
of different
organochlorine
pesticideresiduesto
raptoreggshellchangecannotyetbe gauged.Initialeffects
wereevidentlya responseto
DDT and perhapsyBHC but it seemslikelythataldrin,dieldrinand heptachlorcontributedlater,fortheavailable evidenceindicatesa generalsimilarity
in thephysiological
activityof thesechemicals.In the goldeneagle,the timingof the reductionin breeding
successsuggeststhatin generaldieldrinhad more seriouseffects
than DDT (Lockie &
Ratcliffe1964),but as adequateeggshelldata are lackingforthepre-dieldrin
period,one
cannotbe surethatthiswould be truefortheeggshellchangespecifically.
The case forbelievingthatorganochlorine
insecticidesare themajorcause of theeggshell changeis stronglysupportedby evidencefromNorthAmerica,whereHickey &
Anderson(1968) havefoundthata paralleland unprecedented
decreasein eggshellweight
in the peregrine(18.8% in California),ospreyand bald eagle (Haliaetus leucocephalus)
D. A. RATCLIFFE
93
in 1947 also.
of DDT in thatcontinent,
coincidedin onsetwiththegeneralintroduction
correlationbetweenincreasingmean DDE
Moreover,theseauthorsshoweda significant
gulls(Larus argentatus)
contentofeggsand decreasingmeaneggshellthickness
in herring
betweenthe Britishand North American
fromfivedifferent
colonies. The similarity
change
situationsis remarkableand demandsan explanationin termsof environmental
scale. Finally,Porter& Wiemeyer(1969) have shownexperion an extra-continental
mentallythat in a captivebreedingpopulationof the Americansparrowhawk(Falco
sparverius),
dosage witha combinationof DDT and dieldrincaused increasedegg disapby parentbirdsand reducedeggshellthickness.The
pearance,increasedegg destruction
advancedabove and developedfromcorrelative
evidenceis thusconvincingly
hypothesis
supportedby controlledexperiment.
Thereis evidencethatPCBs could be causallyinvolvedin productionof raptoreggshellsof sub-normalweight.Riseboroughet al. (1968) have shownthatin pigeons,PCBs
have fourtimesthe enzyme-inducing
activityof technicalDDT and six timesthat of
DDE. Littleinformation
is available about thetimingand scale of the appearanceand
oftheenvironment.
Thischemicalcomplexhas manyuses
increaseofPCB contamination
in industry,
and it has evidentlyshowna greatpost-warincreaseas an environmental
pollutant.Compared withDDT and yBHC, however,the increasein use of PCBs is
later,and it is likelyto have showna steady
likelyto have beenmoregradualand slightly
increaseup to the presentday. Even in 1967-68,contaminationof Britishraptorsby
pesticideresidues(no analyticaldata forPCBs
PCBs-isfarlowerthanby organochlorine
are available for earlieryears).Neitherthe biological pathwaysnor the geographical
contaminationby PCBs are yet known accurately.While
patternof environmental
theiruse is likelyto be heaviestin urbanand industrialpartsof Britain,PCB residues
&
(Prestt,Jefferies
appear to be heaviestin birdswhichfeedin an aquatic environment
Moore 1970).
To sum up, it would seem obtuseto denythatthereis a strongprimafacie case for
pesticidalresiduesto be causally
suspecting,
firstand foremost,knownorganochlorine
This hypothesisrestsnot on a
theeggshelleffect.
involvedin initiating
and maintaining
makean extremely
lines,whichtogether
singlelineofevidencebut on severalconvergent
and
compellingcase. Thereare some groundsforsuspectingPCBs to be a contributory
additivecausal agent.It is possible that the total cause of the eggshellchange was a
combinationof severalchemicalpollutantswhichincreasedas a wholeduring1947-68,
of one causal
in timeand location.The identification
thoughwithvaryingcontribution
The factthatPCBs
does notexcludeotherpossibilities.
agentin sucha situationcertainly
pollutantsuntil1966mustnaturally
escapedsuspicionas possiblyharmfulenvironmental
cause the non-chemist
to wonderif therecould be otherpotentiallyhazardous waste
productsof the chemicalindustryto whichattentionhas not yetbeen-drawn.This is a
thattheknown
lineofthoughtwhichwouldgainvalidityifitcouldbe shownconvincingly
of
the
environmental
eggshellchange.
pollutantsare not thecause
THE CONNECTION BETWEEN ENVIRONMENTAL POLLUTION, DECREASE
IN EGGSHELL WEIGHT, EGG BREAKING, BREEDING FAILURE AND
POPULATION CHANGE
This sectionexaminesthe degreeof correlationbetweenthesefour phenomena,and
considersto whatextenttheyare causallyconnected,whethertheycould all be successive
could connectstagesin a differstagesin a singlecausal chain,or whether'short-circuits'
94
Pesticidesand egg breakagein birds
are expresseddiagramaticpossibilitiesof relationship
entorder.The varioustheoretical
allyin Fig. 7.
The firstimplicationis thatthesechemicalpollutantsaffecteggshellweightby altering
the internalregulationof calciumcarbonatemetabolism,so thatCaCO3 supplyto the
period becomesreducedalthoughthe bird's intakeof
oviductduringthe egg-forming
calcium remainsunchanged.There is anotherpossibility:that thesechemicalsimpair
so thatfoodintakeis reduced,or thecatchingofpreymakes
thebird'shuntingefficiency,
moredemandsupon thebird,althoughthereis no decreasein the abundanceof prey.
Organochlorinepesticideshave a neuropathologicaleffectand so mightcause subtle
especially,takingof preydependson
interference
withmotorresponses.In theperegrine
loss of harmonyin
an acutelysensitivecontrolof visionand flight,and the slightest
impairthebird'sabilityto 'lock
mightsignificantly
nervousand muscularco-ordination
on' to its rapidlymovingand manoeuvrabletarget.Revzin (1966) claimedthatendrin
of healthand/or
had an adverseeffecton visual acuityin the pigeon.Anyimpairment
in theproductionof thinnershelledeggs.
huntingactivitymightbe reflected
peregrineswhichdestroytheireggs are not obviouslyunhealthy.One
Nevertheless,
pair (DumfriesE) broke theireggs in 1962, rearedfouryoungkestrelsafterbreaking
theirown eggsin 1963(Ratcliffe1963b),broketheireggsagain in 1964,and rearedtwo
thesamebird(she
youngin 1965.Duringthisperiod,thefemaleofthepairwas certainly
had distinctive
eggsand behaviourpattern)and appearedto be in finecondition;both
the youngkestrelsand the youngperegrinesrearedby thispair werefed on a copious
supplyof theusual prey.
Yet anotherpossibilityis thatthinnershellsresultfromprematureextrusionof eggs,
knownto occurin domesticfowlunderadverseconditions(C. Tyler,personalcommunication). Such an effectmightoccur withoutnecessarilyinvolvingchange in CaCO3
fewof therichlymarkedand marbled
metabolism.Since 1947therehave been relatively
typesof peregrineeggs so prizedby collectors,and a highproportionofeggshave been
appears to
pigmentation
of the 'washy' or 'streaky'type,in whichthe richsuperficial
happeneither
havebeenmostlyrubbedoffwhentheeggwas laid. This could presumably
was completeor 'fast',but
pigmentation
by theeggbeingextrudedbeforethesuperficial
suchas imperfect
maturation
oftheshell,
it could also resultfromothereffects,
structural
extruded
of the oviductor cloaca. Prematurely
inadequatepigmentsupply,or tightness
and thinshelledeggsof lapwingand goldenplover(Charadriusapricarius)are sometimes
ground
foundnaturally,mainlyduringhard weather,and have a completelydifferent
colour and type of surfacemarkingscomparedwithnormaleggs. Egg pigmentation
ofanyoneinterested
to measure,butmightbe worththeconsideration
patternis difficult
in thephysiologicalstudyof thesephenomena.
While the work on hepaticenzymeinductionand steroidmetabolismsuggeststhat
residuesmay affecteggshellthicknessby disturbinghormonebalance,
organochlorine
otherbiochemicalmechanismsincludingthose of the nervoussystemitselfcould be
causationwill onlybe unravelledby
involved.The detailednatureof thisfundamental
carefulphysiologicaland biochemicalstudies.
There is an obvious possibilityof causal relationshipbetweendecreasein eggshell
thicknessand increasein eggbreakage.In the sampleof peregrineeggscollectedduring
1963-69,mean shellindexwas 1 42 in thosefromclutchesdepletedby breakage,comsignificant
paredwith1-67foreggsfromnestswhereno breakagewas found,a difference
at P<0O001 (t = 5 4864, df = 42).
The hypothesisof a causal connectionis not damaged by the lack of an exact time
D. A.
RATCLIFFE
95
correlationbetweenonsetof eggshellchangeand increasedfrequencyof egg breakage.
Onlyin the peregrineare the available recordsnumerousenoughto allow one to place
any weighton thedatingof thebeginningof increasein egg breakage;and evenin this
nests)thatit is
species,therecordsforthecriticalyears1947-50are so few(twenty-nine
quitepossiblethattheearliestinstancesofbreakageweremissedmerelybychance.All of
thesetwenty-nine
nestswerevisitedonlyonce,whentheeggswerefreshor onlyslightly
incubated.The eggshellchangehas evidentlyaffectedthe whole peregrinepopulation
outsidetheHighlands,but by no meansall thesefalconshave brokentheireggs,so that
the onset of the second phenomenonis quite likelyto be less clearlydateable. Three
instancesof eggbreakagewererecordedduring1948-49 (p. 69), but as two of theseare
fromeyriesamples of unknownsize, theyare not claimed to be proof of increasein
frequency.
However,evenifit could be shownthatthetwophenomenadid not coincide
exactlyin time,the hypothesiswould not be demolished;reasons are givenbelow for
thinkingthategg breakingcould be a habit whichtakes a whileto develop.The direct
causes of egg breakagemaybe simpleor complex.
Eggs withthinshellsare moreproneto accidentalmechanicaldamagein thenestthan
those withnormalshells.During incubationthereare normalhazards whichtestthe
structuralstrengthof eggshells:the broodingparentmay accidentallycrush an egg,
knockor pressone eggagainstanotheror againsta rockfragment,
projectionor stickin
thenest,or cause damagewithitsbillwhileturningan egg.Since 1947,I have fourtimes
seen dentedperegrineeggswhichcould have been damagedin such ways,and F. Parr
foundone peregrineclutchapparentlyclaw-holedby the sittingbird.The only one of
thesedentedeggs actuallymeasuredhad an unusuallythinshell(index 1.25) and it is
highlyprobablethatthe thinnestshelledeggs of peregrineand sparrowhawkwould be
especiallysusceptibleto dentingbycontactwitheach otherin thenest.In birds,tremoring
is a characteristic
symptomof acute poisoningby DDT and dieldrin.It is not clear
whetherlow levels of contaminationcan cause such obvious muscularresponses,but
during
sudden,convulsivemovementof the legs,feetor body,or evenmereclumsiness,
incubationcould directly
damageeggs(e.g. bydentingor claw-holing)whichwouldthen
be eaten.The thinnertheeggshellthegreaterthe riskof such accidentaldamage.
Howevercaused, damage to eggsin thenestusuallyelicitsa changein psychological
responsein parentbirds,whichthendestroy(usuallyby eating)or removethe affected
1942a). In wildbirds,
& Nethersole-Thompson
eggs(Kirkman,in Nethersole-Thompson
thisis normallya responseto damaged eggs only,but domesticfowlwhichhave once
eaten theirown eggs oftendevelop a habit of doing so subsequently.In the wild, the
recentprevalenceof egg destructionin certainraptorsprobablystemsfromincreased
frequencyof damage to thinnershelledeggs; once practised,thisbehaviourcould conofeggdamageon subsequent
ceivablybecomea habitwithoutneedingthespecifictrigger
occasions.
In thisview,parentalegg destruction
would merelybe an incidentaland subsequent
effectto the fundamental
metabolicdisturbanceproducingthe thinnereggshells.However,in that the eggshellchangeimpliesinternalizedreductionin CaCO3 supply,the
metabolicchangemightalso be expressedas behaviourtendingto increaseCaCO3 intake,
i.e. a lime 'hunger'whichgives the bird an appetiteforits own eggshells,regardless
ofwhethertheyare damagedor not.Certainhumandisturbances
ofappetite,collectively
knownas 'pica', are apparentlymetabolicallydeterminedand may sometimeshave a
In someinstances,however,theeggcontentsare eaten
functional
nutritional
significance.
and mostof theshellleft,and sparrowhawks
have beenfoundto tipeggsout ofthenest,
D
APP.E.
Pesticidesand egg breakagein birds
96
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D. A.
RATCLIFFE
97
withouteatinganypartof them(I. Prestt,unpublished).It is therefore
possiblethategg
breakingis simplya behaviouralresponseto thechangedinternalstateof thebird,with
no nutritional
significance,
and may occurwithoutpreviousdamage to eggs.
Sincethehormonesofreproduction
are affected
byDDT and dieldrin,itis conceivable
that total reproductiveactivitymight become abated, so that incompleteeggshell
formation,egg breakingand otherabnormalbehaviourwould thenbe simplydifferent
aspects of this tendency.Otherfeaturesof the recentperegrinedeclinehave been the
apparentfailureof manyfemalesto lay eggs,and thefrequently
irregularappearanceof
one or bothbirdsofa pairat thenestingcliffs,
whenno eggshavebeenlaid. This suggests
thata further
symptom
ofdeterioration
to maintainnon-breeding
is a tendency
behaviour
throughthe nestingseason, and it is possiblethathigherlevelsof contaminationcould
suppressovulationand reducethestrength
of thepair-bond.Therehas been an apparent
increasein frequencyof desertionof incubatedeggs by peregrinesand golden eagles
sincearound 1960,and, duringthe same period,goldeneagles and sparrowhawks
have
shown an unprecedently
frequenthabit of buildingnestsbut failingto completethem.
Peregrines,whichdo not build nests,have oftenscrapedand thenbrooded on empty
scrapesfor some time.All thesesymptomspointingto apparentsterility
could result
fromchange in hormonalcondition,whichmightitselfbe temporaryor permanent,
dependingon laterchangesin contamination
level.In thiscontext,egg breakingmight
represent
of breeding,as a reactionappropriateto thehormonalstateof the
termination
parent.
Thereis yetanotherpossibility:thatorganochlorine
residueshave a directneurotoxic
effect,inducingbehaviourwhichis completelypathologicaland aberrant.Kitselman
(1953) foundthatat highdosage dieldrinproducedbrainlesionsin dogs but,whileit is
generallybelievedthattheorganochlorine
insecticides
attackthecentralnervoussystem,
theevidencegiveslittleindicationof effects
on behaviour.Warner,Peterson& Borgman
of
(1965) have,however,convincingly
shownthatexposureto sub-lethalconcentrations
toxapheneproducedchanges-inbehaviouralresponsein goldfish.For theperegrine
it is
knownthatdieldrinand DDE can reachhighlevelsin thebraintissue(Jefferies
& Prestt
1966).Moreover,Jefferies'
(1969) evidencefortheeffects
of DDT on thyroidmetabolism
has clearimplicationsfora changein behaviour.
In someperegrines,
eggbreakingis notnoticeablyaccompaniedby otherabatementof
breedingbehaviour,as in themanyinstanceswheretheemptyscrapesor brokeneggshells
werebroodedforsome time; and moreparticularly
in the two different
pairs whichin
1961 and 1963 appropriatedkestrelclutchesaftertheyhad apparentlybrokentheirown
eggs.In thesecondinstance,theyoungkestrelswerehatchedand rearedbytheperegrines
as thoughtheyweretherealoffspring.
In 1968,thefemaleofthesecondpair(DumfriesE)
was watchedperforming
scrapingmotionsin the eyrie,whichwas foundto containa
singleintactegg,whileon a ledge below was another,evidentlykickedout and freshly
crackedopen,butnoteaten;therewerepreviously
foureggs(G. Carse). Scrapingbehaviourbelongsnormallyto thepre-laying
to thetimesequenceof
period,so thatdisturbance
involved.Subsequentlythispair again dispossesseda
breedingbehaviourwas evidently
pair ofkestrelsoftheireggs,butfailedto hatchthem(J.Young). Thesecuriouseventsall
suggestthatan unusualconflict
ofurgeswas involved,withdisturbance
butnotcessation
of breedingactivities.
These different
hypothesesto accountforthepossiblepathwayswhichmightconnect
pollutantactionwithparentalresponseare not necessarilymutuallyexclusive,and the
causal relationships
mayproveto be multidimensional.
At a biochemicallevelone deals
98
Pesticidesand egg breakagein birds
to determinea
witha complexof interconnected
systemsin whichit may be difficult
sequenceof causation.
Whateverits real meaning,thereseems littledoubt that the relationshipbetween
close,and thatthe
decreasein eggshellthickness
and increasein eggbreakageis extremely
factorresponsibleforthefirstphenomenonis ultimately
thecause ofthesecond.Thereis
equallylittledoubt thatthe increasein egg breakinghas been associatedwith,and resuccessin theraptorsconcerned.In
sponsiblefor,a considerabledecreasein reproductive
thesampleofperegrine
eggscollectedduring1963-69,meanshellindexwas 1P60in those
fromclutcheswhichlaterproducedfledgedyoung,comparedwith1 46 foreggsfromnests
is significant
at P <0-001 (t = 6 541,
whichfailedto produceany young;the difference
df = 42). In peregrine,sparrowhawkand golden eagle, the breakingor unexplained
disappearanceof eggshas probablybeen a commoncause of breedingfailuresince1950,
and has led to a substantialreductionin numberof youngrearedin Britain.This alone
to accountforthepopulationdeclinein thefirsttwo species.Decrease in
is not sufficient
was widespreadfrom1947onwards,but no declinein breedperegrine
eggshellthickness
ing populationbecame apparentuntilafter1955. In fact,the eggshellchange became
establishedat a timewhentheperegrine
populationwas recovering
rapidlyin areas
firmly
depletedbywar-time'control'.This is provedby data fromDorset,wherethepopulation
increasedfromone pair in 1946to eightpairsin 1956and did not declineuntil1957 (D.
Humphrey,unpublished),yet everyeggshellavailable after1946 was of sub-normal
weight,and egg breakingwas foundin at leastthreeeyries.In Lakeland,whereeggshell
changewas well establishedin 1947,therewas no clear evidenceof populationdecline
until1961.
In areas suchas Dorset and Lakeland,it is apparentthateggbreakagedid not greatly
affectbreedingsuccessof thepopulation,as thiswas alreadylow because of egg collecting; thefirstmajorcause of eggloss merelytendedto replacetheother.However,when
remoterareas, especiallyin Scotlandand Ireland,whereegg
egg breakagelateraffected
itresultedin effective
reductionin breedingsuccess
collectingwas previously
insignificant,
there.If breedingsuccessof the whole BritishIsles peregrinepopulationgraduallyfell
ofthepopulationand,
belowa criticallevel,therecouldhavebeenchangein age structure
However,the 'crash' in
finally,a failureto replacethelosses caused by adult mortality.
breedingpopulation,beginningafter1955 and spreadingin a wave-likemannerfrom
was almostcertainly
southto north,was so abruptthata greatincreasein adultmortality
a
of
there
was
sudden
prevalence
non-breeding
and,in thepopulaundoubtedly
involved;
thanbefore1955.
tionthatremained,hatchingfailureoccurredat evenhigherfrequency
This populationcollapse coincidedwith the widespreadintroductionand rapidlyincontributions
creasinguse of the highlytoxiccyclodieneseed dressings.The respective
and breedingfailureto theperegrinepopulationdeclinewillperhaps
of adult mortality
neverbe known,thoughYoung (1969) has discussedtheoreticalpossibilities.Once the
populationwas thus depleted,the continuedhighrate of breedingfailureamong the
remainderwould tendto preventrecoveryin numbers.In thisway,a merelysub-lethal
effectof persistent
residuescould contributeto the presentlow state of the peregrine
population.
Similarconsiderationsapply to the sparrowhawk,which also showed a post-1955
population 'crash', with an associated reductionin breedingsuccess and increasein
non-breeding
(Prestt-1965). In thisspecies,egg breakagecould possiblyhave caused a
decreasein breedingsuccessbefore1955, and has certainlydone so subsesignificant
quently.As sparrowhawkbreedingpopulationswere previouslycharacterizedby sta-
D. A. RATCLIFFE
99
the'crash'is likelytohave
fromgame-keeping,
resulting
despitea heavymortality
bility,
of numbers
recovery
though,as in theperegrine,
involvedincreasedadultmortality,
population.
in theremaining
failure
bythehighrateofbreeding
wouldbe retarded
and
ofdeterioration,
outputofyoungis theonlysymptom
In thegoldeneagle,reduced
to datetheonsetofthis
It is difficult
population.
Scottish
is shownonlybythewestern
werestudying
fieldworkers
changein thisspecies.Despitethefactthatseveralenergetic
in eggbreakage
no obviousincrease
goldeneaglesfrom1950onwards,
Scottish
western
by1956(e.g.Brown& Watson1964),
successhadbeenreported
inbreeding
ordecrease
1964).
later(Lockie& Ratcliffe
untilsomewhat
andthesechangesdidnotdrawattention
in thelate 1940sandthenweregradually
DDT wereintroduced
Sheepdipscontaining
In thisspeciestheavailableevionwards.
dipsfromthemid-1950s
replacedbydieldrin
mostcloselywithappearwerethuscorrelated
changes
thatthebiological
dencesuggests
itis possiblethatifdecreasein breeding
However,
in theenvironment.
anceofdieldrin
In goldeneagles,
by 1950itwouldhavepassedunnoticed.
successhad alreadyoccurred
but,following
1963-65,
during
failure
causeofbreeding
wasthecommonest
eggbreakage
decrease
dipsin 1966,theperiod1966-68showeda significant
ofdieldrin
thewithdrawal
population
Scottish
successin thewestern
in eggbreakageand increasein breeding
in shellindexin a 1968-69
(Lockie et al. 1969),and therewas a partialrecovery
high
sampleof eggs(see noteaddedin proof,p. 106).Therewas also an unusually
after1960.Thesechangestogether
in thiseaglepopulation
ofnon-breeding
frequency
in a low outputofyoungand it is probablethatby 1965thebalancebetween
resulted
thenthe
forpopulation
critical
maintenance;
was becoming
and recruitment
mortality
rose.
andproductivity
beganto takeeffect
sheep-dip
ban on dieldrin
datingoftheonsetof
in eggshell
weight,
Withspecieswhichshowsmallerdecreases
appearin 1951,inthekestrel
first
clearindications
inthemerlin,
changeis moredifficult;
decline
population
has shownsubstantial
in 1946,andinthehobbyin 1952.Thekestrel
dataon breeding
1965),buttherearefewrecent
England(Prestt
in southern
andeastern
of kestrel
eggbreakage(p. 70) were
instances
Bothof therecent
successforthisregion.
nestsseenwitheggsafter
in lowlandnests,and I foundno eggbreakagein forty-three
the
of speciesis low(Ratcliffe
contamination
whereorganochlorine
1946in hillcountry,
locally,butdataforthisspeciesaretoo fewto
havedeclined
1965).Merlinpopulations
andbreeding
ineggbreakage
increase
ornottherehasbeena significant
whether
indicate
thatthe
informed
am
successofhobbiesbut
ofthebreeding
I haveno experience
failure.
received
the
well,despitehaving
reasonably
itsnumbers
populationmaintains
British
no
show
signof
Buzzards
foroverhalfa century.
of eggcollectors
specialattentions
northern
in
buttheyhavelocally(e.g.
changeandonlyoccasionaleggbreakage,
eggshell
since1960(i.e.after
inpopulation
anddecrease
innon-breeding
England)shownincrease
1965).
(Ratcliffe
had madeitsimpacton thebuzzardpopulation)
myxomatosis
foundthata
FarneIslandshagpopulation
Potts(1968)in a studyoftheincreasing
ofpolygamy
incidence
with
correlation
highrateofeggbreakageshoweda significant
causedby
was
1968
in
atnests.A 'crash'intheeastcoastshagpopulation
anddisturbance
a Dinoflagellate
bloom(Coulsonet al. 1968).
crow,kittiwake
theraven,carrion
wereexamined,
Oftheotherspecieswhoseeggshells
1940.
The rook
since
or
increase
gullhave showna local general
and black-headed
therecontinued
trend
this
whether
uncertain
atleastlocallyupto 1960butitis
increased
in
the
south,
especially
decline,
a
general
shown
have
andrazorbill
The guillemot
after.
a slowdeclineeviThegoldenploverhasundergone
as a resultofoil pollution.
mainly
and
onwards;
from
1955
stable
fairly
been
probably
has
1940,but
before
beginning
dently
100
Pesticidesand egg breakagein birds
the greenshanksummerpopulationhas evidentlymaintaineda generalstabilityduring
recentyears.(Data for the last nine species are mainlyfromParslow 1967.) There is
insufficient
information
to allow one to stateconclusively
whet-her
thelast nine species
have or have not experienced
anymarkedchangesin breedingsuccesssince1940,butno
indicationsof changein eitherdirectionhave been apparent.
For thegroupof speciesexamined,correlationbetweenscale of pesticidalcontamination,eggshellchange,eggbreaking,breedingfailureand populationchangeis notconsistentthroughout.
Partoftheproblemhereis thattheavailabledata on residues,eggshells
and populationstatusfora speciesmayall referto different
districts,
and thereis a need
for more criticalinformation
such as that available for peregrine,sparrowhawkand
goldeneagle.
THE SIGNIFICANCE OF EGG BREAKING IN A 'NATURAL' SITUATION
I wish finallyto examinethe possiblefunctionalsignificance
of parentaleatingor disposal of damagedeggs.Accidentaldamageto eggs,whetherassociatedwithdecreasein
shellthicknessor not,is likelyto resultin hatchingfailure,and egg eatingcan thenhave
the effectof preventing
thecontinuationof probablyfutileincubation,and thusofconservingboth theenergyof theparentsand valuablefood material.Decrease in eggshell
unfavourablecondithicknessmay be a generalizedreactionto internally
or externally
tionsaroundlayingtime.Some suchfactors,e.g.ill-health
(includingdisease),stress,food
shortageand severeweather,wouldmilitateagainstsuccessful
rearingofyoungiftheeggs
hatched,while decrease in eggshellthicknessitselfreducesthe chances of successful
theegg morefragileand proneto accidentaldamage.Egg eating
hatching,by rendering
would thenresultalso in avoidance of hatchingunderconditionsunfavourableto the
survivalof chicks,and underextremeconditionsit mightalso increasethe chances of
survivalof theparents.
breeding
Egg eatingmaythushaveevolvedas an adaptivemechanismwhichterminates
undera widerangeof conditionswhicharisejust beforeor duringthelaying/incubation
periodand are unfavourableto successfulnesting.The abilityof manyraptors(but not
golden eagle and buzzard) to lay 'repeat'clutchesis relevanthere.Predationof raptor
recentphenomenon,so thatthisabilityto
eggsis largelyby humansand is a relatively
more
is
to
be
an
to
more
ancientcauses of eggloss or damage,
'repeat'
likely
adaptation
such as fallingrocks,landslides,wind-blowof trees,ice or snowand severecold. Many
Alaskan peregrinesnest on erodingrivercutbankswheregravitationalinstabilitycan
easilyresultin damageto eggs(Cade 1960).If suchdamageoccurs,parentaleggdestructionthenpromotesa secondattemptat nestinglaterin thesame season and underpossiblyimprovedconditions.
The winterof 1937, in Februaryand March was unusuallyseverein the Scottish
well below average;
Highlands,with exceptionalsnowfalland monthlytemperatures
eighteggslaid byfivepairsof goldeneaglesduringthisspringhad a meanshellindexof
2-83. The followingwinter,1938, had only average snowfall,and January-March
were higherthan average; nine eggs laid by fivepairs of golden eagles
temperatures
duringthisspringhad a meanshellindexof 3-10,i.e. 'normal'(Table 5). January-March
1941 was anotherwinterperiodof greaterthanaveragecold and snowfallin the Highlands,and a ravenclutchlaid in March had a lowermean eggshellindex(1 07) thanthe
(in
repeat(1.22) laid a monthlaterunderimprovedconditions.Nethersole-Thompson
Bannermann1961) also reportsfrequently
blue or bluish-white
eggs
findingthin-shelled
D. A.
RATCLIFFE
101
oflapwinglyingabandonedon fieldsin theCairngormfoothillsafterseveresnowstorms.
The implicationis thatthinnereggshellswerea responseto severecold, eitherdirectly
or
throughincreaseddifficulty
in obtainingfood,in a typicallysomewhatcalcium-deficient
environment.
Althoughegg eatingwas not involvedin theseexamples,theysuggesta
naturalsituationin whichit could be evoked; threedifferent
lapwingswereknownto eat
theirdamagedeggs(Nethersole-Thompson
& Nethersole-Thompson
1942b).
Decrease in eggshellthicknesswould onlyfollowwhenunfavourableconditionsarose
beforelayingtime,but egg eatingwould also be associatedwithadversechangeafter
laying.If hormonalchangeis thebiochemicalmechanismproducingdecreasein eggshell
thicknessin responseto adversity,
thenit is also a predisposingfactorin any parental
egg destruction
whichfollowsaccidentaldamage to eggs. Can egg breakingbehaviour
also be directly
inducedby suchhormonalchange,occurringwithoutthespecifictrigger
of eggdamage,as a parallelresponseto eggshellchange,and as partofa totalabatement
ofbreedingactivityunderunfavourable
conditions? Thisis a theoretical
possibility
which
could be testedby carefulfieldobservation.
to supporthis
Wynne-Edwards
(1962) used theevidenceforegg eatingby peregrines
theoryof a homeostaticpopulationregulationdevice,wherebyindividualsreactinstinctivelyfromtheirassessmentof thefood situation,and limittheirfamilysize so thatthe
populationdoes notreachthe'ceiling'ofitsresources.Egg eatingwouldthuscomplement
the regulatorydevice of asynchronoushatchingwhichin many corvidsand raptors
variationsin availablefoodsupply(cf.Lack 1954;Lockie
adjustsbrood-sizeto short-term
1955a); it would operateduringthelayingand incubationstagesof thebreedingcycle,
whereasasynchronous
hatchingcan onlyoperateat thenestlingstage.
ofCaCO3 metabolismcould be a directdensity-depenOn theotherhand,disturbance
dent effectof available food shortage,and egg eatingwould thenbe a compensatory
orindirectly
reaction,eitheras an innateresponseto calciumdeficiency,
throughthemore
frequentdamage to the thinner-shelled
eggs. The frequenteatingof hatchedeggshells
suggeststhatmanyspecieshave a need to conservecalcium.
The findingof manybrokeneggsin nestsof short-eared
owls (Asioflammeus)during
thefirstyearof a vole plague 'crash' (Lockie 1955b)is suggestive.
Increasedhuntingby
the owls doubtlessgave greaterchancesforpredationofnests,buttheshortageoffood
and increasedcompetition
mighthave producedphysiological
changesin theowls.Stress
is certainlyindicatedas a cause of parentalegg breakageamong some bird speciesin
captivity.
of eggdestrucNeitherthehomeostaticnordensity-dependent
viewofthesignificance
tion,as a responseto food shortage,appear to be relevantto the recentcontextof increasedegg destruction
among Britishraptors.In the peregrineand sparrowhawk,
egg
rateforseveralyearsafter
breakinghas continuedto occurat a highand undiminished
the populationsof both reachedtheirlowestknownlevels.The lack of a tendencyto
asynchronoushatchingin the Britishperegrinealso impliesthat this species is not
normallysubjectto variationsin foodsupplyin thiscountryduringnestingtime.Shortage
of food is moreconceivablein theclimatically
marginalregions,botharidand arctic,of
theperegrine's
worldrange,and itis herethateggeatingcouldbe an associatedregulatory
or compensatory
mechanism.It is interesting
thatLewis (1938) foundtwo instancesof
smashedand disappearingeggsand two smallclutches(one and two eggs)in a seriesof
eighteyriesof Iceland falcon (Falco rusticolusislandicus),a species normallylaying
in
clutchesoffoureggsand knownto be moreaffected
thantheperegrine
byfluctuations
food supply(Cade 1960). Some otherBritishraptorsmorecertainly
showasynchronous
102
Pesticidesand egg breakagein birds
hatching,especiallythegoldeneagle and buzzard,withtheimplications
forvariablefood
supplyduringthenestingseason.
Sometimeseggdestruction
involvesremovaloftheintacteggsinsteadof eggeating.Is
therea possibleconnectionbetweenthese activitiesand the normal,stronglyadaptive
behaviourof eggshelldisposal afterhatching?Especiallyin those birdswhicheat the
hatchedeggshells,such behaviourpointsto a delicatebalance betweentwo conflicting
urgesin theparent;thecompulsionto protecttheegg and to removeit once theshellis
opened (Nethersole-Thompson
& Nethersole-Thompson
1942a).The actionsof a male
heronwhichrepeatedlydestroyedits own eggswerereminiscent
of eggshelldisposal or
nest cleaningbehaviour(I. Prestt,personalcommunication).
Many mammalshabitually
eat theirplacentasand it is onlyone stepfurther
forthemto eat theirsmallyoung.It is
well knownthatrabbits,rats and pigs in captivitysometimeseat theirown young,especiallyafterbeingdisturbed.Armstrong
(1947) regardsparentaleggdestruction
bywild
birdsas a displacementreaction,but thisbehaviourcould perhapsbe adaptivewhena
predatorhas discoveredthenest.Lorenz(1966) believesthatin manyvertebrates
onlythe
developmentof special inhibitionspreventsthe expressionof aggressionby parents
towardstheiryoung,and pointsoutthatvariouscircumstances
these
mayeasilyover-ride
farm
inhibitions;he mentionsa case wherean aeroplaneflyinglow over a silver-fox
caused all themothervixensto eat theiryoung.Richards(1966,1967)has investigated
this
conflicting
behaviourin thegoldenhamster(Mesocrietusauratus);itis onlywhenfemales
are in thehormonalconditionappropriateto theperinatalperiodthatyoungare cared
for; at all othertimestheyare killedand eaten.
It thusappearsthata numberofvertebrates
to destroytheirown
havea latenttendency
progeny,and thatsuchmanifestbehaviourcan be adaptivein severaldifferent
contexts,
thoughit could at timesbe regardedas simplyaberrant(i.e. non-adaptiveand pathological).This latentbehaviourcan evidently
be activatedby internalbiochemicalchange
fromperceptionof,or directbodilyresponseto,externalchangein conditions).
(resulting
is therefore
thatcertainorganochlorine
residuesmay,bychance,
My tentative
suggestion
impingeon thebiochemicalprocesseswhichgovernnormalbehaviourpatternsin sucha
latentbehaviouris expressed.In thissituation,thelatentbehaviour
waythatalternative,
(egg breaking)maystillbe expressedadaptively,in thatotherinternalchanges(decrease
in eggshellthickness)are likelyto reducethe chances of successfulbreeding;but this
behaviourcould also be regardedas aberrantin a generalsense,and its outcomeas
to the species.
detrimental
ACKNOWLEDGMENTS
I am gratefulto thefollowing,who have suppliedme withrelevantinformation,
mostly
unpublished:E. K. Allin,C. Best, R. J. Birkett,E. Blezard,D. Brown,S. S. Chesser,
G. Douglas, W. J.Eggeling,I. E. Hills,G. Horne,D. Humphrey,
P. Kimber,R. Laidler,
J. Mitchell,W. Murdoch,D. Nethersole-Thompson,
R. Newman,F. Parr,I. Prestt,A.
Rendall, E. L. Roberts,J. Robson, R. Stokoe,A. Watson,D. Watson,D. Weir,J. E.
Wightman,M. Woodford.For access to egg collectionsin theircare, I have to thank
C. J. 0. Harrison,I. Lyster,R. Wagstaffe,
D. Wilsonand C. W. Benson; and I received
generoushelp fromth-efourteenownersof privateegg collectionswho wishto remain
anonymous.It is a pleasureto acknowledgethehelp and companionshipof E. Blezard
and C. Durellin thefield.ThroughthekindnessofD. Lack, I consultedthejournalsofthe
late E. B. Dunlop, and R. E. Booth of the MeteorologicalOfficecontributeddata on
D. A. RATCLIFFE
103
weather.I. Presttand A. Tynansuppliedeggshellsforchemicalanalysis,and C. Tyler
and
in peregrine
thedecreasein eggshellthickness
byexactmeasurement
kindlyconfirmed
residueswereperanalysesof organochlorine
Gas-liquid chromatography
sparrowhawk.
formedby the AgriculturalScientificServicesof the Departmentof Agricultureand
Fisheriesfor Scotland,Edinburgh,and the Laboratoryof the GovernmentChemist,
Toxic Chemicals
oftheNatureConservancy's
London,as partoftheresearchprogramme
and WildlifeDivision,and I thankN. W. Moore forallowingme to use theseresults
freely.
I appreciategreatlytheviewsand ideas receivedin discussionwithmanyof theabove
J.D. Lockie,N.
named,and J. P. Dempster,M. C. French,J.J. Hickey,D. J.Jefferies,
J.L. F. Parslow,M. P. M. Richards,J.G. Skellam,Mrs L. Stickel,
W. Moore,F. Moriarty,
For theirhelp withstatisticalanalysis
W. Stickel,C. Tylerand V. C. Wynne-Edwards.
to K. Lakhaniand M. D. Mountford.Manyotherswhohaveat
of the data,I am grateful
to thepresentpaper,
have thuscontributed
sometimehelpedme withraptorinformation
of theirhelp.
and I regretit is not possibleto giveherean individualacknowledgment
Finally,mygratitudeis due to Miss S. Batchelorand Mrs M. Haas, who have helped
enormouslyin thepreparationof thispaper,especiallyin processingthe eggshelldata.
SUMMARY
in the nests
frequency
(1) Since 1950,egg breakagehas occurredwithunprecedented
and goldeneagles.The majorityof theseeggbreakof Britishperegrines,
sparrowhawks
ages are believedto have been caused by the parentbirdsthemselves,usuallyby the
eatingof both shelland contents.
(2) One proximatecause of thisphenomenonappearsto have been a widespreadand
substantialdecrease in relativeweight(largelythickness)of eggshellsof peregrines,
In the firsttwo
sparrowhawksand golden eagles (19.1, 17-2and 9.90o respectively).
species,this eggshellchange began in 1946-47,reached a climaxin 1948-50, and has
persistedup to 1969. In the goldeneagle it probablybegan not laterthan 1951. Other
species showingdecreasein relativeweightof eggshellsare kestrel(4.900, from1946),
merlin(12.700, from1951), hobby (5.2%, from1952),shag (12.3o%, from1951),rook
changewas found
(5O00o from1958)and carrioncrow(4.80 from1958).No significant
black-headedgull,
razorbill,kittiwake,
in eggshellsofcommonbuzzard,raven,guillemot,
goldenploverand greenshank.
change which parallels the eggshellchange in
(3) The only known environmental
has
a likelyphysiologicalconnection,is thewideand
timingand geographicalpattern,
of
the
organicchemecosystemby residuesof synthetic
spreadpost-1945contamination
comIn
in
icals used as pesticidesand industry. particular,persistentorganochlorine
been
shown
and
have
to
of
wild
tissues
experimentally
in
raptors,
poundsaccumulate the
The
in
birds.
introduction
of
calcium
mechanisms
general
affecting
disturbphysiological
horticultural
and
and
then
into
into
first
use,
DDT and yBHC,
domestic,veterinary
during1946-48,coincidedexactlywiththeonsetof theeggshellchange,and
agriculture,
thesechemicalsare suspectas initiatorsof thischange.The post-1955use of dieldrincontaminationand probably
typeinsecticidescontributedadditivelyto organochlorine
showeda
theinitialeggshellchange;theindustrialpollutantPCBs evidently
reinforced
and
could
also
have
contrienvironmental
as
an
increase
contaminant,
post-war
gradual
butedto theeggshellchange.
(4) WithinBritain,thereis a strongcorrelationbetweengeographicalvariationsin
104
Pesticidesand egg breakagein birds
leveloforganochlorine
contamination,
degreeofchangein eggshellweight,and frequency
of egg breakage,in peregrine,
sparrowhawk
and goldeneagle.
(5) Organochlorine
contaminationevidentlytriggers
a causal chain in some raptors;
decreasein eggshellthickness(producingreducedmechanicalstrength)leads to more
frequentaccidentaldamageto eggs,and henceto morefrequent
parentaleggdestruction
(sincebirdshave an innatetendencyto destroytheirdamagedeggs).Adverseeffects
on
breedingbehaviourmay also occur. The outcomeis a reductionin breedingsuccess.
While the well-knownpopulation'crashes' of peregrineand sparrowhawkafter1955
thedeclinesin breedingsuccessmay
evidently
involvedunusuallyheavyadultmortality,
have contributed,
and would certainlyhelp to preventrecovery.
(6) Interspecific
differences
in eggshellchange probably reflecta combinationof
in exposureto persistent
differences
residuecontamination,
differential
uptakeand variationsin biochemicalresponseto a particularlevel of a residue.
(7) Parentegg-breaking
may be a normal,adaptiveresponseto variousadverseconand militateagainstsuccessfulbreedditionswhicharisebetweenovulationand hatching,
ing. Contaminationby chemicalresidues,whenresultingin eggshellchange,takes the
place of a 'natural'adversefactor,but theoutcomeis moredetrimental
to thespeciesif
reducedbreedingsuccessis maintained.
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L. F. (1961).KeepyourPigeonsFlying.London.
Whitney,
V. B. (1945).DDT and thebalanceofnature. Atlant.Mon. 176,107-13.
Wigglesworth,
and goldeneagles. Br.
and othersea-birds
as preyofperegrines
P. (1965).Manxshearwaters
Wormell,
Birds,58, 149.
and London.
inrelation
toSocialBehaviour.
V. C. (1962).AnimalDispersion
Edinburgh
Wynne-Edwards,
Their
on peregrine
FalconPopulations:
Peregrine
populationdynamics.
Young,H. F. (1969).Hypotheses
Biologyand Decline(Ed. byJ.J.Hickey),pp. 513-9.Madison,Milwaukeeand London.
(Received20 May 1969)
Note added inproof
have produced
otherinvestigations
Sincethispaperwas acceptedforpublication,
change.
of
on thecause eggshell
itsmainconclusions
supporting
evidencestrongly
demonstrated
studies
have
three
other
on
sparrowhawks,
American
Besidesthework
in
thickness
producedecreasein eggshell
thatorganochlorine
pesticides
experimentally
produced
DDT
and
fed
pp'
op'
birds.Bitmanet al. (1969)foundthatJapanesequail
than
ofshellweight)
(as a percentage
shellsand lowercalciumcontent
eggswiththinner
of
include
inhibition
they
involved
mechanisms
biochemical
usual. Amongpossible
avian
in
the
activity
anhydrase
of
carbonic
and
inhibition
bone formation
medullary
decreasesin
gland.Heath,Spann& Kreitzer(1969)obtainedsignificant
shell-forming
(Anasplatyof
in
mallard
eggshells
in
cracking
and
increases
(1300)
thickness
eggshell
mallard
that
found
feeding
&
Egbert
(1969)
Lehner
and
DDE.
DDT
fedpp'
rhynchos)
that
and
in
eggshell
thickness,
a
decrease
caused
significant
dieldrin
with1 6 ppm
deThese
studies
obtained
further
effect.
this
level
had
little
above
increaseddosage
those
to
levels
comparable
dose
sub-lethal
at
thickness
experimental
in
eggshell
creases
in thefield.
foundwiththesepesticides
golden
western
Scottish
isthata sampleofseventeen
evidence
observational
Additional
indexof 3-066whichis sigeagleeggsobtainedduring1968-69showa meaneggshell
fromthe meanindexof 2-834forthe 1951-65samplefromthis
different
nificantly
thatas wellas thedecreasein egg
region(P < 0.01,t = 2-754,df42). This suggests
by Lockieet al. (1969),there
successreported
in breeding
breakageand therecovery
sheep
in thisspeciessincethedieldrin
ineggshell
thickness
has beena partialrecovery
in 1966.
dip ban wasimplemented
D. A.
RATCLIFFE
107
REFERENCES
Bitman,J.,Cecil,H. C., Harris,S. J. & Fries,G. F. (1969).DDT inducesa decreasein eggshell
calcium.
Nature,Lond.224,44-6.
ofMallardreproduction
J. F. (1969). MarkedDDE impairment
Heath,R. G., Spann,J. W. & Kreitzer,
in controlled
studies. Nature,Lond.224,47-8.
Lehner,
P. N. & Egbert,
A. (1969).Dieldrinandeggshell
thickness
inducks. Nature,
Lond.224,1218-9.
108
Pesticidesand egg breakagein birds
APPENDIX
depletedclutchesknowninperegrineeyries
Recordsofsixty-one
examinedby D. A. Ratcliffe1949-68
eyrieA. 18 April 1949. c/2 and one egg, emptyand withlarge
(1) Kirkcudbright,
hole, in crevice12 ftbelow eyrie.Brokenegg was pure whitewhereasothertwo were
typicalred. Two femalesabout and one seen in skirmishwithmale. Clutchfreshand
perhapsincomplete.
21 June1949. Eyrienot reached,but obviouslyhad no young.
(2) Cumberland,eyrieA. 10 April 1951.c/3,freshand perhapsincompleteclutch.
shell
12 April 1951. Two eggsbroken;femalewatchedeatingone, stale comminuted
of the other.Thirdegg undamaged.Not re-visited.
fragments
eyrieB. 18 April 1951. c/2,and comminutedshellof at least one
(3) Kirkcudbright,
moreegg in the scrape.Eggs incubatedprobablya fewdays. Not re-visited.
(4) Caernarvon,eyrieA. 29 April 1951.c/2,incubatedprobablya week.
3 May 1951.Comminutedshellofone eggin thescrape;theotherintact.Not re-visited.
brokeneggshellon hillside,
(5) Dumfries,eyrieA. 1 June,1951.Largepiece ofrecently
within2-300 yd of eyrieledges.Both peregrinesabout, but evidentlywithno occupied
eyrie.
shellofat leastone more
eyrieC. 4 June1951.c/2and comminuted
(6) Kirkcudbright,
egg in the scrape. Eggs a few days incubated.A repeatclutchafterprobable human
nest.Not re-visited.
robberyof firstlayingin a different
eyrieD. 8 April 1952.c/3and comminutedshellof anothereggin
(7) Kirkcudbright,
thescrape.Eggs freshand breakagemayhave occurredbeforefourthegg was laid. One
younglaterreportedhatched,but finallyfounddead (G. Trafford).
(8) Caernarvon.11 May 1952.c/I and comminutedshellsof othereggsin the scrape.
Incubationwell advanced.
30 May 1952.Brokenshelland congealedcontentsfromlasteggin thescrape.Female
stillsittingon theeyrie(P. Kimber).
(9) Dumfries,eyrieA. 6 April 1953. c/3 and fourthegg empty,withlarge hole, on
notthelastlaid. Not
ground20 ftbeloweyrie.Clutchfresh,and brokeneggwas evidently
re-visited.
shellof at leastone more
(10) Merioneth,eyrieA. 25 April1953.c/2and comminuted
in
Incubation
well
advanced.
the
scrape.
egg
(11) Cumberland,eyrieB. 8 April 1955. c/4fresh.Reportedlaterwithonlytwo eggs
and thesedisappearedone by one (F. Parr).
eyrieC. 17 April 1955.c/2,apparentlyincubatedat least a week.
(12) Kirkcudbright,
of othereggs. Reportedlaterwithonly one egg, but thisprovedto be
No fragments
addled and was finallydeserted(W. Murdoch).
of
(13) Dumfries,eyri!B. 19April1955.c/i,advancedin incubation,butno fragments
othereggs.Not re-visited.
(14) Dumfries,eyrieA. 19 April 1955. c/I advancedin incubation;nestviewedfrom
15 ftaway,and no remainsof othereggsvisibleat thisdistance.Not re-visited.
of
(15) Peebles,eyrieA. 20 April 1955.c/2advancedin incubation,but no fragments
othereggs.
25 May 1955.Brokenremainsof one egg and the otherdeserted,but bothperegrines
about near theeyrie(W. J. Eggeling).
D. A. RATCLIFFE
109
(16) Caernarvon,eyrieC. 18 April1956.c/l,advancedin incubation,and comminuted
shell of othereggsin theeyrie.Eyrielaterreportedempty(E. K. Allin).
(17) Dumfries,eyrieC. 20 April,1959.c/l, advancedin incubation,and comminuted
shell of othereggsin the scrape.Not re-visited.
(18) Dumfries,eyrieB. 26 April 1959.c/i, advancedin incubation.Nest viewedfrom
30 ftaway,and no remainsof othereggsvisibleat thisdistance.Not re-visited.
eyrieA. 9 April 1960.c/3fresh.Later reportedbroken(F. Parr).
(19) Westmoreland,
(20) Cumberland,eyrieC. 13 April 1960. c/3,fresh.Later reportedto have disappeared; robberyunlikely(R. J. Birkett).
(21) Dumfries,eyrieB. 16 April 1960. Half the shellof an egg,veryrecentlybroken,
lying30 ftbelow eyrie,on a ledge. Female present.No repeatfound.
(22) Dumfries,eyrieA. 16April1960.Brokenremainsofthreeeggsin thescrape.Eggs
completelysmashedand empty,but shellsleftin big pieces. Female present.
eyrieE. 23 April1960.Eyrieempty,butemptyeggwithlargehole
(23) Kirkcudbright,
lyingon thehillsideabout 30 yd away. Female present.
(24) Cumberland,eyrieD. 30 April 1960. c/3,evidentlyadvancedin incubation.
24 May 1960. Eyrieempty,but not reached.Robberynot suspected.
shellof
(25) Dumfries,
eyrieA. 11 May 1960.Repeat layingof22. c/2and comminuted
at least one moreegg in the scrape.Eggs fresh.Not re-visited.
(26) Tiree. 12 June1960.c/l,probablyfaradvancedin incubation.Nest viewedfrom
10 ftaway and no remainsof othereggsvisibleat thisdistance.Not re-visited.
(27) Peebles,eyrieB. 23 April 1961. c/2,and comminutedshellof at least one more
incubated.
egg in the scrape.Eggs probablyslightly
6 June1961. One young,whichwas reared.
(28) Inverness.11 May 1961.c/I hatching.The eyriecould not be examinedforshell
remains,owingto awkwardnessof situation.One youngreportedto reared(M. Woodford).
(29) Inverness,eyrieB. 13 May 1961. Comminutedshellof recentlydestroyedegg in
the eyrie.Female was incubatinga c/6 of kestrelon anotherledge,havingevidently
dispossessedthe owners.Not re-visited.
(30) Ross-shire,
eyrieA. 16 May 1961.Brokenremainsoftwoor threeeggsin theeyrie.
been eaten,not merelycrushed.
One or two stonesin theeyrie,but eggshad evidently
(31) Perthshire,
eyrieA. 30 June1961.c/2,and comminutedshellof at leastone more
egg in the scrape.Both eggsaddled but femalestillincubating.
(32) Dumfries,eyrieD. 7 April 1962.c/3,and comminutedshellof at least one more
egg in theeyrie.One eggwas quitefresh,indicatingbreakagehad occurredbeforeclutch
completed.Nest laterreportedto have failed(W. J. Eggeling).
(33) Peebles,eyrieB. 8 April 1962.c/l, fresh.
26 May 1962. Eyrieempty,but forcomminutedeggshell.
(34) Dumfries,eyrieE. 7 July1962.Comminutedshellofprobablymorethanone egg
in thescrape.Both peregrinesstillabout.
(35) Dumfries,eyrieE. II April 1963. c/4,fresh.One egg takenforanalysis.
leftfromthisclutch,but peregrine
14 May 1963. Only a few small shellfragments
incubatingc/4 of kestrellaid in same eyrie.The kestreleggshatchedlaterand all four
youngwererearedto theflyingstageby theperegrines.
(36) Inverness.14 April 1963.c/I fresh.
23 June1963. Nest empty,exceptforcomminutedshellfragments.
(37) Peebles,eyrieB. 18 April 1963. c/3,fresh,one egg takenforanalysis.
110
Pesticidesand egg breakagein birds
11 May 1963.c/2.One egg obviouslyaddled,the otherfertile.
20 May 1963. Addled egg vanished withouttraceand fertileegg deserted,but the
embryohad been dead fora week.
(38) Kirkcudbright,
eyrieF. 19 April 1963. c/3and comminutedshellof at least one
moreegg in thescrape.One eggtakenforanalysis.The othertwoeggsdisappearedlater
(E. L. Roberts).
(39) Kirkcudbright,
eyrieE. 19 April 1963. c/3and comminutedshellof at least one
more egg in thescrape.One egg takenforanalysis.The othertwoeggsdisappearedlater
(D. Watson).
(40) Perthshire,
eyrieB. 21 April 1963.c/3and largepieces of shellof anotheregg in
the scrape.Not re-visited.
(41) Inverness.eyrieD. 22 April 1963,c/4,somewhatincubated.Nest laterreported
empty(F. Parr),but no reasonto suspecthumanrobbery.
(42) Dumfries,eyrieE. 14 April 1964. c/4,fresh,one takenforanalysis.
31 May 1964.One desertedaddled egg,and thecomminutedshellsoftheothertwoin
the scrape.
(43) Peebles,eyrieB. 14 April 1964. c/4,fresh,one takenforanalysis.
31 May 1964. One deserted,addled egg,and the comminutedshellsof theothertwo
in the scrape.
incubated.
(44) Peebles,eyrieA. 1 May 1964. c/4,slightly
June1964. Female sittingcloselyon largebrokenpieces of shellof all foureggs.
incubated.Repeat layingof 42. In
(45) Dumfries,eyrieE. 31 May 1964.c/2,slightly
Novemberthefemalewas sittingon theeyrie,buttherewas no traceoftheseeggs,and no
younghad been reared.
(46) Kirkcudbright,
eyrieD. 8 April1965.c/4,fresh.One eggtakenforanalysis.Eyrie
found1 June1966.
laterreportedempty(E. L. Roberts)and shellfragments
(47) Kirkcudbright,
eyrieB. 11 April 1965. c/3,fresh.Eyrie later reportedempty
found8 April 1966.
(E. L. Roberts)and shellfragments
11
incubated(J. Mitchell).
1965.
(48) Stirlingshire. May
c/4,slightly
near
but
no
trace
of fourthegg.Threeyounglaterreared
5 June1965.c/3,
hatching,
(J. Mitchell).
(49) Perthshire,
eyrieC. 9 May 1965.c/4,incubated(J. Mitchell).
in the scrape.
6 June1965. Onlycomminutedshellfragments
8
D.
1966.
and
(50) Kirkcudbright,
eyrie
April
c/2
largefreshly
brokenfragments
of at
leastone moreeggin thescrape,whichalso helda peregrine
castingcontainingshellfrom
thisegg. One of the othertwo eggshad two dents;thisegg was takenforanalysis.
1 June1966. Eyrieempty,but repeatclutchfound(52).
brokenfragments
(51) Kirkcudbright,
eyrieC. 8 April1966.c/2and crumpled,freshly
of at least one moreegg in the scrape.One egg takenforanalysis.
1 June1966. Eyrieempty.
(52) Kirkcudbright,
eyrieD. 1 June1966.Repeatof50. c/2and comminuted
shellofat
leastone moreeggin thescrape.One eggwas 'chipping',buttheotherwas deeplydented,
and its well-developed
embryohad died. The dentedegg was takenforanalysis.
(53) Kirkcudbright,
eyrieD. 8 April 1967.c/4,fresh.Eyrielaterfoundemptyexceptfor
brokenshells(G. Horme).The femalewas thesame as thatoccupyingthiseyriein 1965
(46) and 1966 (50, 52).
(54) Peebles,eyrieB. 11 April1967.c/2,fresh.Eyrielaterfoundempty(G. Carse),but
no reasonto suspectrobbery.
D. A. RATCLIFFE
1I1
(55) Kirkcudbright,
eyrieC. 9 April 1968. c/3,slightlyincubated;one egg takenfor
analysis.A singleegg laterstillbeingincubated(R. Roxburgh).
(56) Dumfries,eyrieE. 9 April 1968. c/4,fresh,one egg witha hole in its side and
completelyempty,as thoughsucked.Not re-visited.
(57) Dumfries,eyrieA. 10 April 1968. c/2,fresh.
15 May 1968. Brokenshellsin theeyrie(G. Horne).
(58) Peebles,eyrieB. 10 April 1968.c/3,fresh;one egg takenforanalysis.Eyrielater
foundempty(G. Carse) but no reasonto suspectrobbery.
(59) Perthshire,
eyrieD. 11 April 1968. c/4,fresh;one egg takenforanalysis.Eyrie
laterfounddeserted,but youngrearedfromrepeatclutch(J. Mitchell).
- (60) Cumberland,eyrieD. 17 April1968.c/3and comminuted
shellof a fourtheggin
the scrape.Remainingeggsseen intactjust beforehatchingbut onlyone youngreared
(R. J. Birkett).
6 June1968.Comminutedshellof at leasttwoeggsin thescrape.
(61) Aberdeenshire.
/
EGG DATA
(1) Sourcesof materials
Measurementsof eggshellswereobtainedfromthefollowingegg collections:
E. P. Chance collectionin theBritishMuseum(NaturalHistory),London.
Generaland Sir Maurice Denny collectionsin the Royal ScottishMuseum,Edinburgh.
V. Hewittcollections(mainlyF. C. R. Jourdainand J. M. Goodall) in Rothschild
Museum,Tring.
Ootheca Wolleyana(J. Wolley collection)in Departmentof Zoology, University
of Cambridge.
Generalcollectionin the Cityof LiverpoolMuseums.
Fourteendifferent
collectionsin privateownership.
Mostly singleeggs,taken underlicenceduringthe period 1963-68,for chemical
oftheToxic Chemicalsand WildlifeDivision,
analysisas partoftheresearchprogramme
Monks Wood Experimental
Station.
Fennoscandianperegrine
Exceptfor twenty-two
eggsin OothecaWolleyana,all eggs
examinedhad been takenin theBritishIsles.
(2) Methodsof examination
All the eggshellsexaminedhad beencleanlyblownthrougha hole notexceeding7 mm
in diameter.Eggs withlargerblow holes wererejectedbecause:
(a) The weightof shelllost in drillingthe hole is no longeran insignificant
proportion of thetotalweight.
ofsignificant
(b) Largerholesare an indicationofadvancedincubationand therefore
withdrawalof calciumand decreasein shellweight.
The lengthand breadthof the eggshells(i.e. externaldiametersof the long and short
axes) were measuredto 0-01mm by verniercalipers.The air dryweightwas takento
0-01g on a Sauter-Toppananalyticalscale S.113 portableelectricalbalance.
With such instruments
these measurementscan be rapidlymade. More accurate
measurements
of size,i.e. volumeor surfacearea, are eitherimpracticalor slow to make
Pesticidesand egg breakagein birds
112
fora numberof
fora largenumberof eggs.Estimatesof surfacearea weredetermined
sparrowhawkeggs by use of the formulaS = 2rBP/2(Romanoff& Romanoff1949);
withtheseestimatesof surface
values of L x B forthesameeggsgave a linearcorrelation
judged valid to use L x B as a linearand simplyobtainedproduct
area. It was therefore
thepresentpaper.
forcomparingeggshellareas throughout
of eggshells
(3) Characteristics
ofeggshellindex(relativeweight)foreach ofthespeciesstudied
The normalvariability
maybe gaugedfromthestandarderrorsgivenin Table 5. It is usual to finda moderate
in size, weightand eggshellindexwithinthesame clutch.However,
degreeof variability
the combinationof mean size, mean weight,mean eggshellindexand eggshellshape is
eggshells
ofperegrineand sparrowhawk
Table 8. Measurements
Shell
thickness
(p)
Length
(cm)
Breadth
(cm)
Shell
weight
(g)
4-48
5.37
5-18
5-35
5-36
4.99
5-12
3.90
4K16
4-20
4-14
4-20
4-17
4.13
3.60*
4.79
4-56
3-96
4-45
3-86
4-20
241t
313
310
272
294
274
284
Recentshells
1
2
3
Mean
5-21
5-12
5-26
5-20
4-02
4.03
3.95
4 00
3 40t
2-74
3-04
3-06
265t
220
241
242
Sparrowhawk
Old shells
1
2
Mean
3-81
3 95
3-88
3-19
3-28
3-24
1.70*
1-88
1-79
208t
244
226
Recentshells
1
2
3
4
Mean
4-64
4-06
3-86
4 03
4-15
3 40
3-22
3-10
3-20
3-23
1-32t
1-29
1-17
1-61
1-35
144t
161
165
213
171
Peregrine
Old shells
1
2
3
4
5
6
Mean
* Withshellmembranes.
shellmembranes.
t Without
oftenremarkablyconstantforthe same femalein successiveyears,and mayeven be a
and colour.
ofa particularbirdthantheeggshellmarkings
morereliableguideto identity
ofindivithismeansofrecognition
reinforce
and colournevertheless
markings
Distinctive
duals.
Limitedobservationsin relationto orderof layingsuggestthatin wild birdsthereis
not necessarilya decreasein eggshellweightor size betweensuccessiveeggsof a clutch;
D. A. RATCLIFFE
113
thelargest
orheaviest
eggshell
maybe anywhere
between
thefirst
andlastegglaid.Nor
was thereanyhintthatwildbirdslivelong,enough
foradvancing
age significantly
to
affect
eggshell
weightor size.Before1947,theoccasionallight(thin-shelled)
or undersizedeggwasliableto be produced
byanyspecies.
In anyspecies,
themeasured
eggshell
weight
islargely
a function
ofeggshell
areax thickness.Therehas beenno changein eggsizesince1946in anyofthespeciesexamined,
so
thattheobserved
changesin eggshell
areevidently
due to changesin thickness.
weight
Theonlyotherpossibleexplanation
wouldbethateggshell
andnotthickness
density
has
or thatbothhavebeeninvolved.
changed,
ofa sampleofperegrine
Measurements
and
madebyProfessor
sparrowhawk
C. Tyler(seeTable8) haveestablished
eggshells
thatthe
decreasein weighthas certainly
involveda substantial
decreasein thickness.
Relative
can therefore
be expressed
eggshell
weight
ofindividual
independently
variations
in eggsizebythe
index'=
'Eggshell
Eggshell
weight
(mg)
Length(mm)x breadth
(mm)
andthisparameter
ofeggshell
mayalsobe a measure
thickness.
TEST OF CHANGE IN EGG-SHELL INDEX
BY M. D. MOUNTFORD
The sequenceof observations
of egg-shell
indexis dividedintotwoperiods,earlyand
late.The earlyperiodextends
fromyear1 to yeark, and thelaterperiodfromk+ 1 to
whichgivesthemaximum
yeark+ 1.Yeark is takento be thatyear,from1946onwards,
between
difference
themeanegg-shell
index,XE oftheearlyperiodandthemeanXL ofthe
lateperiod.
As k is selectedto maximizethedifference
betweentheearlyand lateperiods,an
ofthestraightforward
t-test
ofdifference
meansisinvalid.
application
between
Theprobof themaximum
abilitydistribution
difference
mustbe used as thebasis of thetest
themeansofthetwoperiods.As k rangesoveritspossiblevalues,from1946
between
letbl, b2 ... b, be thecorresponding
onwards,
valuesof
XE-XL
s[+
N-Nj
whereS2 equalsthetotalsumofsquaresabouttheoverallmean,Nk thenumber
ofeggs
in theearlyperiod,andN- Nk thenumber
inthelaterperiod.Let,Bbe themaximum
of
theb,.Thenifh is anyvalue
Pr(fl>h) = ZPr(bj>h)-ZPr(b1>h,
i= 1
16i<j<1
bj>h)+ZPr(bi>h,
1<i<j<
k<1,
bj>h, bk>h)-etc.
(1)
Mountford
that
(1969)demonstrates
Pr(b'>h) =
-(
dN-2
hB(I
N22)
i
(2)
Pesticidesand egg breakagein birds
114
and forlargeN, whichis thecase fortheegg-shelldata,
Pr(bi> h,bj> h) = 2N-(l
i)
exp)
I
(IN 42)(b2I-2Abibj+bj}
(3)
whereA is thecorrelation
betweenbi and bj. Ifbi correspondsto an earlyperiodextending
fromyear I to yeari, and bj to an earlyperiodextendingfromyear I to yearj (i<j),
thenit is easilyseen that
A
(4
{(N- N)Nj
Usingthisrelation,and theprobability
functions
(2) and (3), thefirstand secondsummationsin (1) can be evaluated,forgivenvalues of h, by numericalintegration.
The thirdand highersummationsof (1) could be similarlyevaluated.However,the
numericalintegration
of thesemultipleintegralsis no easytask.In manyapplicationsof
the relation(1), thethirdand highersummationsare of negligiblemagnitude.However,
fortheegg-shellindexdata thevaluesof A are so nearto unitythattheseriesof summationsof (1) is onlyslowlyconvergent;thehighersummationscannotbe ignored.
The difficulty
ofevaluatingthemultipleintegralscan be bypassedby usinga simplified
test; thistestis conservative
in the sense thatit under-estimates
the significance
of the
observeddifference
in means.Let A*be theminimumofthevariousvaluesofA.It willbe
seenfrom(4) thatifyearp is thelast yearbefore1947in whichobservationsweremade,
and ifyearq is thefinalyearin whichobservationsweremade, then
A* =
1(-N_ 1)l/
I
t(N-Np)Nqg
Let cl, c2 ... c, be normal variates,each with variance 1/(N-4) and with equal
correlationsA*.It has been shownby Slepian (1962) that
Pr(fiJ>h)= 1-Pr(b, <h, b2<h, . . . b1<h)<1-Pr(cj<h, c2<h,... c,<h)
(5)
The value of Pr(cl <h, c2<h, . . . cl<h) is obtainedby followingan argumentsimilar
to thatof Kendall & Stuart(1958,p. 353).
N- 4
Letk2
,k*,2= 1
thenPr(c, < h,C2<h,... cl<h)
00
-
-00
j'
'1
ex2
[Xof
ie-2dtjdx,
whereii=kh+(1
I_)x
(6)
-00
This integralis easilycalculatednumerically
forgivenvalues ofh and A*.The inequality
(5) ensuresthe conservative
natureof the test,i.e. if h (0.05) is thatvalue of h forwhich
(6) equals 0 95, then
Pr(f,>h(O005))<?0 05
The numericalworkingofthemethodis demonstrated
by applyingit to theshagdata.
In all thereare sixty-oneobservationsof whichthirty-eight
weremade before1947 and
elevenin 1967,thelastyearin whichrecordsare available.Hence N = 61, Nk = 38 and
forthedifferent
partitions
Np1 = 50. The minimumvalue of thecorrelationcoefficient
after1946is therefore
= 0608
38 0I60289
\23x 50/
D. A. RATCLIFFE
115
Observations
weremadeinfiveoftheyearssucceeding1946;henceI
value of /3,themaximumof theb's, is
p =E
From (5) and (6)
L
tNk
5. The observed
063499
N- Nk)
00
e-x22F
Pr(/>>0-63499)< 1-
where,u= khx+
1/2 =
=
00
e?-t2
5
dt dx
-00
X = 760764+1P23215x.
The integral,evaluatedby Simpson'srule,is equal to 0-999996.Hence
Pr(f > 0 63499)< 0 000004
The difference
is therefore
veryhighlysignificant.
REFERENCES
Kendall,M. G. & Stuart,A. (1958).TheAdvanced
Theory
ofStatistics.
London.
Mountford,
M. D. (1969).A testofdifference
betweenclusters. Int.Symp.statist.Ecol.,Yale.
Slepian,D. (1962).The one-sidedbarrierproblemforGaussiannoise. Bell Syst.tech.J. 41, 463-502.