0053610
JOURNALOF AVIANBIOLOGY33: 358-365, 2002
Seasonal changes in the response of oystercatchersHaematopus
ostralegus to human disturbance
Richard A. Stillman and John D. Goss-Custard
Stillman,R. A. and Goss-Custard,J. D. 2002. Seasonalchangesin the responseof
oystercatchersHaematopusostralegusto human disturbance.- J. Avian. Biol. 33:
358-365.
The responseof foraging animals to human disturbancecan be consideredas a
trade-offbetweenthe increasedperceivedpredationriskof toleratingdisturbanceand
the increasedstarvationrisk of not feedingand avoidingdisturbance.We show how
the responseof overwintering
oystercatchers
Haematopusostralegusto disturbanceis
relatedto theirstarvationrisk of avoidingdisturbance.As winterprogresses,oystercatcher energy requirementsincreaseand their feeding conditionsdeteriorate.To
survivethey spendlongerfeedingand so haveless sparetime in whichto compensate
for disturbance.Laterin winter,birdsapproacha disturbancesourcemore closely
and returnmore quicklyafter a disturbance.Their behaviouralresponseto disturbance is less when they are having more difficulty survivingand hence their
starvationrisk of avoidingdisturbanceis greater.Theseresultshaveimplicationsfor
studieswhichassumethat a largerbehaviouralresponsemeansthat a speciesis more
vulnerableto disturbance.The oppositemay be true. To more fully understandthe
impact of disturbance,studiesshould measureboth behaviouralresponsesand the
ease with which animalsare meetingtheirrequirements.Conservationeffort should
be directedtowards specieswhich need to spend a high proportionof their time
feeding,but still have a large responseto disturbance.
R. A. Stillman (correspondence) and J. D. Goss-Custard, Centre for Ecology and
Hydrology (CEH) Dorset, Winfrith Technology Centre, Winfrith Newburgh,
Dorchester, Dorset DT2 8ZD, UK. E-mail: [email protected]
There is considerable debate into the effects of human
disturbance on animal populations (e.g. Hockin et al.
1992, Davidson and Rothwell 1993, Hill et al. 1997).
The response to disturbance is often measured as the
distance over which animals respond to disturbance or
the time to return after human activity has ceased (e.g.
Smit and Visser 1993). An assumption in the interpretation of many of these studies is that disturbance is more
serious (e.g. causes more animals to die) when the
behavioural response to disturbance is greater (e.g.
animals take longer to return after disturbance has
stopped or are excluded from a larger area by disturbance) (Gill et al. 2001).
The response to disturbance can be considered as a
trade-off between food intake and the perceived predation risk of human presence (Gill et al. 1996, Sutherland 1996). Animals choose either to tolerate human
presence by continuing to feed, but at an increased
C
perceivedpredationrisk, or to avoid it and decreasing
their perceivedrisk, but at the expense of reduced
intakeand henceincreasedstarvationrisk.A prediction
of this frameworkis that the responseto disturbance
will depend on the starvation risk of avoiding the
disturbance;animalsmay respondless when their starvation risk is greater(Gill et al. 2001).
We measuredthe responseto disturbanceof an overwinteringshorebird,the oystercatcherHaematopusostralegus.Shorebirdsmay be particularlyvulnerableto
disturbanceas their feeding areas are frequentlyused
by people,and they havehigh energydemands(Kersten
and Piersma1987),that becomeincreasinglydifficultto
meet as winterprogressesand feedingconditionsdeteriorate (Goss-Custardet al. 1996)and thermoregulatory
energydemandsincrease(Wiersmaand Piersma1994).
To survivethey must spendlongerfeedingand so have
less sparetime in whichto compensatefor disturbance.
JOURNAL OF AVIAN BIOLOGY
358
JOURNAL OF AVIAN BIOLOGY 33:4 (2002)
0053611
We show how the response to disturbancevaries as
energydemandsand feedingconditionschange.
Methods
source of disturbancethroughoutwinter. As soon as
the personleft the bed, the observerrestartedcounting
at 10-20 min intervalsuntil the bed was completely
coveredby the advancingtide, approximately4 h later.
Control counts were made of the numberof birds on
the bed throughoutthe exposureperiod on two undisturbeddays in early and late winter.
The responseto disturbancewas measuredfrom the
numberof birds excludedfrom the bed and the time
taken for them to return afterwards.The number of
birds expected to be on the bed over low tide was
calculatedby modellingthe changes in bird numbers
from 90 min after first exposureto the time of disturbance (Fig. la).
Experimentswere performed between October 1994
and September1996on musselMytilusedulisbed 20 of
the Exe estuary, England (see Goss-Custardet al.
(1982)for a full descriptionof the Exe estuary'smussel
beds). This intertidalbed is near the shoreline,has an
area of 9.4 ha, and is fully exposedon springtides for
about two hours. It is relativelyundisturbedin comparison with other parts of the estuary(Goss-Custard
and Verboven 1993), allowing the controlled disturbancesto be the only majordisturbanceduringexperiments. However,the bed is not completelyundisturbed
and birds encounter human activities (walking, bait
collecting and shellfishing)on a regularbasis; during
(a) Bed-wideexperiment
25% of experimentssome birds on the bed were disturbedas a personeitherpassednearbyor crossedpart C
.
of the bed. Changesin the responseto disturbancewere
.... .. ..
.300
....n..x.
measuredby repeatingexperimentsthroughoutwinter.
In orderto reducethe likelihoodof birdshabituatingto
the disturbance,experiments were conducted infre200
nr
amx
quently,on successivespringtide seriesand so about 14
days apart. The experimentswere also designed to
100
replicatethe types of human activity normallyoccurring on or near the bed. Experimentswere performed -o
E
on spring tides because only part of the bed was
0,t
exposed on neap tides. Results were very similareach
100
0
200
300
year, and so were combinedfor analysis.
We measured the response to disturbanceat two
Timesincefirstexposure(t)(min)
scales. The bed-wide disturbance measured the com-
bined responseof the populationof birds on the bed,
while the local disturbancemeasuredthe response of
birds arounda disturbancesource.
(b) Localexperiment
150
Bed-widedisturbance
An observer,in an elevatedposition on the shoreline,
counted the numberof feeding and non-feedingbirds
on the bed and on an adjacentsand ridge (on which
birds were known to gatherafter disturbances)at 1020 min intervalsfrom first exposureof the bed on the
recedingtide. Counts continuedfor about two hours
until the bed was fully exposed. At low tide a second
person walked across the bed, following a standard
route so that all parts of the bed were approachedto
withinapproximately75 m and all birdstook flight.In
most experimentsthe majorityof birdsleft the bed and
settled on or near the sand ridge, but in late winter
manybirdsreturnedimmediatelyto the bed, landingon
areaspreviouslydisturbed.In thesecasesthe persondid
not alter his route to re-disturbareas of the bed, but
adhered to the standardroute to ensure a constant
JOURNAL OF AVIAN BIOLOGY 33:4 (2002)
C100
tO
1
50
0
0
25
50
75
100
125
Time since start of disturbance (min)
to disturbance.
Fig. 1. The responseof oystercatchers
(a)
Bed-wide experiment- observed and fitted bird numbers
duringa day with disturbance;(b) local experiment- exclusion distance(mean+ standarderror)against time since the
disturbancestarted.In (a), numbersprior to the disturbance
are describedby equation1, numbersafterby equation2 and
the amountof lost feedingtime (min bird- ) measuredfrom
the shadedarea A.
359
0053612
n=
nmaxi
m1 -
r(ti - t) if t < t
if t > t1
nmaxi
(1)
where n = number on bed, t = time since first exposure
(min), nmaxl = maximum numberon bed at low water,
t, =time at which numbers reach a maximum and
r = rate at which numbersincrease.Non-linearregression was used to estimateparametersfor each of the
experimentaldays. This model accuratelydescribedthe
build up of birds on the bed for all replicates(mean
r2 = 97.8%, range = 91.5-99.4%). As the control counts
showedthat the numberof birds on the bed remained
relativelyconstant while it was fully exposed (see below), the predictedvalue of n immediatelyprior to
disturbancewas assumedto be the numberthat would
have occupied the bed during low tide if the disturbance had not occurred. After the disturbance,but
before the tide startedto cover the bed, the returnof
birdswas modelledusing a similarapproach(Fig. la).
nmax2nmax2
g(t2 -
t) if t < t2
if t > t2
(2)
of the nearestcell (as the transectran perpendicularto
the shore and the observer'sinitial position on the
shore was always the same, the route to the transect
and the final location of the observeron the transect
were the same in each replicateexperiment).Once at
the transect,the observercountedthe numberof birds
in each cell every 5 min. Duringthe first winterof the
study, the observerremainedin place (for up to 2 h)
until the advancingtide started to cover the bed. In
subsequentwinters,the observerremainedon the bed
for approximately30 min and then returnedto the
initial locationon the shoreline.Once on the shore,the
numberof birdsin each cell was againcountedevery 5
min until the advancingtide startedto cover the bed.
Control counts were made of the numberof birds in
each cell throughoutlow tide on two undisturbeddays
in early and late winter.
The responseto disturbancewas measuredfrom the
numbersof birds in the transectduring and after the
disturbance.As the observerwalked to the first cell,
birds took flight or walked away so that none were
found within a certain distance. Although this local
exclusiondistancewas only measuredaccuratelywithin
the transect,estimatesof the distancesto nearestbirds
in other directions suggested that this measure was
comparableto that surroundingthe observer. Birds
continuedto move awayfromthe observerfor about 15
min after which the exclusiondistanceremainedrelatively stable,even if the observerremainedin place for
two hours (Fig. lb). The exclusiondistancewas highly
variablebecauseit could changeby 25 m if a singlebird
moved betweentwo cells, and so was not used in the
where nmax2 = maximumnumberof birds on bed after
disturbance,t2 = time at whichnumberof birdson bed
reachesa maximumand g = rate at which birds reoccupy bed. Non-linear regressionwas used to estimate
parametersfor each of the experiments,and the model
accuratelydescribedthe changesin birdnumbers(mean
r2 = 91.4%, range= 44.7-98.9%). The bed-wide return
time was measuredas the amount of lost feedingtime
per bird duringthe 45 min after the disturbance(Fig. analyses. Instead, the local response distance was measured, approximately30 min after the start of disturla).
bance (i.e. when the exclusiondistancehad stabilized),
as the distancefrom the observerto the nearestcell in
which the number of birds was unchangedfrom the
Local disturbance
mean numberpresentbeforethe disturbance.The local
The local disturbanceexperimentswereperformedon a returntimeafterthe observerleft the bed was measured
25 x 150 m, relativelylevel (30 min from first to com- as the time takenfor the numberof birdsin the nearest
plete exposure)part of the mussel bed, located about cell to return to the number observed before the
250 m from, and runningperpendicularto the shore- disturbance.
line. To measurethe locationof birds,this transectwas
divided into six 25 x 25 m cells using white plastic
markers(approximately15 x 15 cm in cross sectionand
Statistical analysis
25 cm high)whichremainedin locationthroughoutthe
study and were visible from the shore. Experiments The followingvariableswere relatedto the three meastarted when the bed was fully exposed and finished sures of responseto disturbance:feedingeffort= mean
when the tide startedto cover the bed, approximately proportionof birdsfeedingon the bed from the time it
two hours later. After the bed was fully exposed and becamefully exposed to the disturbance(mean= 0.82,
before the disturbance,an observer, located on the range = 0.50-0.95); number of birds on bed =mean
shore with a view along the longest length of transect, number of birds on the bed during the same period
counted the number of birds in each cell at 5-min (mean = 313, range = 201-415); stage of season = numintervalsand the numbersof feeding and non-feeding ber of days since 1 August (mean= 120, range= 8birds throughoutthe bed at approximately20-min in- 217); temperature= mean of maximumand minimum
tervals. The observerthen walked on to the bed, di- temperatures(oC) recordedin the 24 hoursbefore 17.00
rectlyto the transect,until he reachedthe nearestedge on the day of the experiment(mean= 10.7, range=
360
JOURNAL OF AVIAN BIOLOGY 33:4 (2002)
0053613
Fig. 2. Numbers(a, c) and feeding
effort (b, d) of oystercatcherson the
whole musselbed (a, b) and in each
transectcell (c, d) duringtwo
undisturbeddays in early (16 Nov
94) and late (30 Jan 95) winter.In
(c, d) the errorbars are maximum
and minimumvalues recordedin
each cell while the bed was fully
exposed.
(a) Bed-wide numbers
1.00
400
(b) Bed-widefeeding effort
0
4
e 0 0
00O
00
0o
-
300
.
o
o0 C0
S0.75
.-
o00
0 o
%
- 0.50
oo
oo
z
o
0
-00C
0
0
e Latewinter
o Earlywinter
0.25
0.00
0
100
300
200
10 (c)
100
0
Timesince firstexposure(min)
E
It
o
S200
E
9
Local numbers
200
300
Timesincefirstexposure(min)
(d) Local feeding effort
1.00
I
4-
z
0.25
0"
.
2•a
0.00
0
0
50
100
Distancealongtransect(m)
2.0-23.0); day length = hours of daylight on day of
experiment (mean = 11.6, range = 9.3-16.7). Feeding
effort and the number of birds on the bed were measured from a number of counts, rather than from the
last count before the disturbance, in order to account
for short-term fluctuations after minor disturbances.
Stage of season is related to the general decline in
feeding conditions during winter, while the other variables measure specific aspects of the birds' energy demands
or
feeding conditions:
temperature =
thermoregulatory energy demands; day length = time
available for feeding during the hours of daylight;
number of birds on bed = strength of interference.
In the analyses we separately related stage of season
and feeding effort to each response to disturbance (see
below). By performing two tests, we increased the
chances of obtaining spurious significant results, and so
performed a Bonferroni correction (Zar 1984) to adjust
the significance level in these tests from 0.05 to 0.025.
Results
150
0
50
100
150
Distancealongtransect(m)
all cells of the experimental transect were occupied
continuously by feeding birds while the bed was fully
exposed (Fig. 2c, d). Neither feeding effort (one-way
ANOVA; early winter, F = 2.32, df= 42,5, P = 0.060;
late winter, F = 1.43, df=42,5, P=0.233) nor bird
numbers in late winter (one-way ANOVA; F = 1.49,
df = 42,5, P = 0.215) varied significantly among the different transect cells. In contrast, bird numbers in early
winter did vary among cells (one-way ANOVA; F =
3.73, df= 42,5, P = 0.007), possibly due to local variation in feeding conditions, with bird numbers between
75 and 125 m from the start of the transect being lower
than in the rest of the transect (Fig. 2c). However, the
method of measuring the local response distance accounted for this variation as it compared the numbers
of birds present before and after disturbance. Therefore, we did not consider that this variation would
affect the experimental results. As the control counts
showed that both the entire bed and the transect were
used throughout the low tide exposure period, any
absence of birds during experiments could be attributed
to the disturbances themselves rather than any other
factors.
Behaviourin the absenceof disturbance
The bed-wide control counts showed that, in the absence of disturbance, feeding birds used the bed
throughout the low tide period and their numbers were
relatively stable between the bed being fully exposed by
the receding tide, approximately 100 min after first
exposure, and the advancing tide starting to cover the
bed (Fig. 2a, b). The local control counts showed that
JOURNALOF AVIAN BIOLOGY33:4(2002)
Responseto disturbance
The bed-wide disturbance always caused all birds on
the bed to take flight, and the local disturbance always
excluded birds from an approximately circular area
around the observer. There was considerable variation
361
0053614
in the three measuresof the responseto disturbance: temperature,the numberof birds on the bed and day
the bed-wide return time ranged from 5 to 32 min length.As it was a proportion,a logistictransformation
bird-1 (mean = 18, sd = 10, n = 15), the local response (logit = In(feedingeffort/(1- feeding effort))) was apdistance from 90 to 140 m (mean = 123, sd = 19, n =
plied to the proportion of feeding birds before the
27) and the local returntime from 5 to 60 min (mean=
27, sd = 19, n = 15).
(a) Bed-widereturntime
40 Seasonal changes in response to disturbance
Variationin the responseto disturbancewas relatedto
the stage of the season (Fig. 3). Later in winter,birds
returnedmore rapidly after the bed-widedisturbance
(bed-wide return time = 29.4 - 0.0934 stage of season;
P = 0.005, r2 = 46.0%), approached the local distur-
bance more closely (local response distance= 1380.130 stage of season; P=0.018, r2= 20.4%) and
returnedmore rapidlyafter the local disturbance(local
return time = 48.7 - 0.195 stage of season; P = 0.004,
r2= 48.7%).All resultswere significantat the threshold
P value of 0.025 derived from the Bonferroni
correction.
30 -
E 20
*
0
-
.)
10 -
0
0
50
0
100
150
200
Dayssince 1stAugust
(b) Local response distance
150 -
Seasonalchangesin feedingeffort
125 -
100 The study aim was to determinewhetherthe response
to disturbancewas relatedto changesin feedingconditions, and hence the difficulty birds were having in r 75
meeting their requirements.The explanatoryvariables
50 each measuredseparateaspects of the birds' feeding
25
conditions (see above), and so we investigated,using
step-wise multiple regression,whether any combina0
tions of stage of the season, temperature,day length
150
100
50
0
and number of birds on the bed were related to the
to
no
variable
disturbance.
1st
since
However,
response
single
August
Days
consistentlyexplaineda higherproportionof the variance in the responseto disturbancethan stage of the
(c) Local returntime
season,and no combinationsof variableswere selected.
The final model for bed-widereturntime only included
60
stage of the season, that for local response distance
only the numberof birdson the bed, and that for local
returntime only temperature(P < 0.01 in all cases).An
0
E 40explanationfor the lack of significantcombinedrelationshipsis that each variablewas correlatedwith stage
E
of the season (Pearson correlation coefficients with
20 =
of season;
0.852, P < 0.001; day
temperature
stage
length= -0.675, P <0.001; number on bed = 0.353,
P = 0.019).
To overcomethis problem,we used the proportionof
birds feeding on the bed prior to the disturbanceas a
single explanatoryvariable, expected to provide an
index of the difficulty oystercatcherswere having in
meetingtheir requirements.As a test of this, the proportion of birds feeding was comparedin a stepwise
multipleregression(using data collectedduringexperimental and control days) with stage of the season,
362
*
200
*
*
O0
0
50
100
150
200
Dayssince 1stAugust
betweenstageof the seasonand the
Fig. 3. Relationships
responses of oystercatchersto disturbance:(a) return time
after bed-widedisturbance;(b) responsedistanceduringlocal
disturbance;and (c) returntime after local disturbance.The
lines show relationshipsfittedusing linearregression(see text
for coefficients).
JOURNAL OF AVIAN BIOLOGY 33:4 (2002)
0053615
feeding effort; P = 0.002, r2= 53.1%).All resultswere
significantat the threshold P value of 0.025 derived
from the Bonferroni correction. Oystercatchersreturnedmore quicklyafter disturbanceswhen they were
having more difficultymeeting their energy demands,
1.0
0
c"
(
O0
0.8
o
S
*
o
o
o
o
a0
0
0
0.6
0.
oo
0 .4
0
(a) Bed-widereturntime
40
* Temperaturelowerthanexpected
o Temperaturehigherthanexpected
I
50
I
100
,
150
30-
I
E
200
Days since 1 August
Fig. 4. Relationshipbetweenoystercatcherfeedingeffort and
stage of the season and temperature.The open circlesshow
days on whichtemperaturewas higherthan expectedand the
closed circles days on which temperaturewas lower than
werecalculatedby regressing
expected.Expectedtemperatures
= 18.7temperatureagainststage of the season (temperature
0.067 stage of season;P < 0.001, r2= 72.5%).
analysis. The regression selected stage of the season and
temperature as explanatory variables, showing that the
proportion feeding increased later in the season, but
was particularly high on unusually cold days (logit =
1.76 + 0.00596 stage of season (P = 0.001) - 0.0691
temperature (P = 0.002); r2 = 80.2%; n = 45; Fig. 4). An
explanation of why feeding effort was related to a
combination of variables, despite the correlation between them, is that, by combining data from all experiments and controls, a larger sample size (n = 45) was
possible than for tests on the separate responses to
disturbance (n = 15, 27 and 15 for bed-wide return
time, local response distance and local return time
respectively).
Therefore, the proportion of birds feeding did
provide an index of the difficulty birds were having
meeting their energy demands, and thus the potential
starvation risk of avoiding disturbances.
10
0
0.5
JOURNAL OF AVIAN BIOLOGY 33:4 (2002)
0.6
0.7
0.8
0.9
1.0
Proportion
feeding beforedisturbance
(b) Localresponse distance
150
125
a
100
a)
75
c
50
?
25
0
0.5
0.6
0.7
0.8
0.9
1.0
Proportion
feeding before disturbance
(c) Localreturntime
60 -
Feedingeffort and responseto disturbance
In order to test whether variation in the response to
disturbance was related to the difficulty birds were
having meeting their requirements, bed-wide return
time, local response distance and local return time were
regressed against the proportion of birds feeding on the
bed prior to the disturbance (Fig. 5). When they were
spending more time feeding, birds returned more
rapidly after the bed-wide (bed-wide return time =
61.7 - 54.0 feeding effort; P = 0.002, r2 = 53.0%), approached the local disturbance more closely (local
response distance = 183 - 72.6 feeding effort; P =
0.020, r2 = 19.9%) and returned more rapidly after the
local disturbance (local return time = 140.3 - 133.5
20
E 40a)
E
20
0
0.5
0.6
0.7
0.8
0.9
I
1.0
Proportion
feeding beforedisturbance
Fig. 5. Relationshipsbetweenoystercatcherfeedingeffortand
their response to human disturbance:(a) return time after
bed-widedisturbance;(b) responsedistanceduringlocal disturbance;and (c) returntime afterlocal disturbance.The lines
show relationshipsfitted using linear regression(see text for
coefficients).
363
0053616
and hence the starvationrisk of avoiding the distur- sponsesto disturbancewill be lower on neap tides than
bance was greater.
those on springtides.
The experimentswere conductedon a musselbed on
which the backgroundlevel of disturbancewas relatively low, so that the controlleddisturbancewas usuthe only major source of disturbanceduring the
ally
Discussion
low tide period. Different magnitudes of response
Oystercatchersrespondedless to disturbanceslater in would have been recordedhad the experimentsbeen
winter when they needed to spend longer feeding to conductedat anothersite which had a differentbackmeet theirrequirements.Theymay have respondedless ground level of disturbance.For example,Urfi et al.
either because the starvationrisk of avoiding distur- (1996) showed that oystercatchersflushed at greater
bance was greateror becausetheir perceivedpredation distancesin parts of the Exe estuaryin which people
riskof the disturbancewas lower.The starvationriskof were encounteredless frequently,and Smit and Visser
lost feeding time and increasedenergy cost of flying (1993) showed similareffects for a range of wadersin
away from a disturbancedid increaseduring winter. the WaddenSea. Such a relationshipshouldnot always
Later in winter, birds'energyrequirementsincreaseas be expected,however;if contact with humansis detrithe temperaturefalls, and the feeding conditions be- mental, birds may show stronger responsesin areas
come poorer as food quality declinesand interference were they contact humansmore often (Smit and Visser
competitionintensifies(Stillman et al. 1996). Oyster- 1993).
catcher mortality due to starvationoccurs mostly in
After being disturbedmost birds flew to and settled
late winter (Goss-Custardet al. 1996, Stillmanet al. on the sand ridgenear the bed, whichinvolveda flight
2000). As they need to spendlongerfeedingto survive, of less than about 500 m. Given the small amount of
oystercatchershave less sparetime in whichto compen- variationin flight distance, and the probablylow ensate for disturbancelate in winter.The perceivedrisk of ergeticcost of such short flights,changesin the starvathe disturbancescould have changed if the type of tion risk of disturbanceprobablyarosemainlyfrom the
disturbancechanged or if birds became habituatedto amount of lost feeding time. The risk of this depends
the disturbances.Disturbanceswere the same in all on the ability of birds to compensateafterwardsby
replicates,eliminatingthe first possibility.Habituation eitherfeedingfor longer or increasingtheirintakerate.
to the disturbanceitself is unlikely to have been the Although oystercatchersfeeding on cockles Cerastomajor cause because experimentswere conducted so derma edule may increasetheir intake rate when the
infrequently,once about every 14 days, and experi- time available for feeding is reduced substantially
ments were designed to mimic the types of human (Swennenet al. 1989),mussel-feedingoystercatcherson
behaviourthat birds would experienceanyway. Fur- the Exe have not been shown to increasetheir intake
thermore,individualoystercatchersreturnwinter after rate after disturbance(Urfi et al. 1996). Furthermore,
winter to the Exe estuary (Durell et al. 2000) which they do not increasetheir rate of mussel consumption
probablyallows them to habituatein the long-termto to compensatefor an overwinterdecline in the flesh
disturbancefrompeople.However,we cannoteliminate content of individual mussels of almost 50%, even
the possibility that part of the seasonal trend in the though the decline in prey quality contributesimporresponse to disturbancewas due to habituation to tantly to the starvationof birds (Goss-Custardet al.
generalhuman activitieson the estuary.Whateverthe 2001). It is likely, therefore,that compensationon the
precisecause, the experimentsstill showedthat oyster- Exe occurs by feeding for longer, and so the birds'
catchers responded less when they were most abilityto do so dependson theiramountof sparetime.
vulnerable.
The experimentsmeasuredthe short-termdisplaceExperimentswere only conducted on spring tides ment of birds caused by disturbance,but in common
because the mussel bed did not fully expose on neap with virtually all other disturbancestudies, did not
tides. Oystercatchers
have more difficultymeetingtheir measure the survival consequences.To do this, the
energy requirementson neap tides because a smaller results need to be incorporatedinto a model which
area of mussel bed is exposed and the upper-shore predictsthe consequencesof displacementfor the indimusselswhich are exposed are of a lower qualitythan vidualsconcernedand those feedingin areas to which
the lower-shoremusselsexposedon springtides (Goss- displacedbirds move. The importantfactors are the
Custardet al. 1993).This meansthat interferencecom- amountof time lost and extra energyexpendedduring
petitionis strongerand that birdsmust consumemore the disturbance,the amount of spare time availablein
musselsto meet their daily requirements.We are confi- which to compensate,and the increasedstrength of
dent that a seasonal trend in the responseto distur- interferenceand depletioncausedby the increasedbird
bance will also occur during neap tides. However, as densityin non-disturbedareas.The influenceof disturbirds have more difficultymeeting their requirements bance on mortalityin this systemhas been investigated
during neap tides, it is possible that behaviouralre- using these experimentalresultsand a behaviour-based
364
JOURNAL OF AVIAN BIOLOGY 33:4 (2002)
0053617
model (Goss-Custardet al. 2000, Stillmanet al. 2001,
land, W. J. (eds).Behaviourand Conservation.Cambridge
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J. D., West,A. D. and Durell,S. E. A. le V. dit
An assumptionoften made in disturbancestudies is Goss-Custard,
1993. The availabilityand quality of the mussel prey
that disturbanceis more serious(e.g. causes more ani(Mytilus edulis) of oystercatchers (Haematopus ostralegus).
mals to die) when the behavioural response to disturbance is greater (Gill et al. 2001). Our results show that
the opposite may be true. Oystercatchers responded
more to disturbance at times when they were more able
to compensate for the lost feeding time associated with
this response. We suggest that in order to overcome this
problem, studies should measure both the behavioural
response to disturbance and the difficulty animals are
having meeting their requirements (e.g. the proportion
of time spent feeding). Conservation effort should be
directed towards species which show a large behavioural response to disturbances, even though they
are already having difficulty meeting their requirements.
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