708
SHORT COMMUNICATIONS
R. D., ANDM. A. JENKINS.
1988. Pollutants
PORTER,
and eggshellthinningin peregrinesand their prey
P. A. 1982. Functionalresponsesof optimal
ABRAMS,
in the BajaCaliforniaregion,p. 413-422. In T. J.
foragers.Am. Nat. 120:382-390.
Cade,J. H. Enderson,C. G. Thelanderand C. M.
D. W., ANDJ.J. HICKEY.1970. Ecological
ANDERSON,
White [eds.], PeregrineFalcon populations,their
data on egg and breedingcharacteristicsof Brown
managementand recovery.The PeregrineFund,
Pelicans.Wilson Bull. 82(1):14-28.
Inc., Boise, ID.
F. L. 1960. The marine peregrinesof the PORTER, R. D., M. A. JENKINS, M. N. KIRVEN, D. W.
BEEBE,
northwestPacific Coast. Condor62:145-189.
ANDERSON,
ANDJ. O. KEITH.1988. Statusand
BENT, A. C. 1938. Life historiesof North American
ReproductivePerformanceof Marine Peregrines
birds of prey. Part 2. OrdersFalconiformesand
in BajaCaliforniaandthe Gulfof California,MexStrigiformes.Bull. U.S. Nat. Mus. 170.
ico, p. 105-114, In T. J. Cade,J. H. Enderson,C.
A. 1926. Notes on the status of the Peale
BROOKS,
G. Thelanderand C. M. White [eds.], Peregrine
Falcon. Condor28:77-79.
Falconpopulations,theirmanagementand recov1969. Hawks,
J. J., ANDF. C. CRAIGHEAD.
CRAIGHEAD,
ery. The PeregrineFund, Inc., Boise, ID.
owls and wildlife. Dover Pub., New York.
H. R. 1973. On the advantagesof flocking.
PULLIAM,
C. DE B. 1916. Note on the distributionand
GREEN,
J. Theor. Biol. 38:419-422.
nesting habits of Falco peregrinuspaealei, Ridg- RATCLIFFE,
D. 1980. The PeregrineFalcon. Buteo
way. Ibis, Ser. 10, 4:473-476.
Books, SD.
selfish
of
the
The
D.
1971.
W.
geometry
HAMILTON,
E. 1989. Conducta y ecologia de la reVELARDE,
herd.J. Theoret.Biol. 31:295-311.
producci6nde la gaviotaparda(Larusheermanni)
C. S. 1959. The componentsof predation
HOLLINGS,
en Isla Rasa, Baja California.Ph.D.diss. Univeras revealedby a studyof smallmammalpredation
sidad Nacional Auton6ma de Mexico, Mexico.
91:
Can.
Entomol.
of the Europeanpine sawfly.
E. 1992. Predation of Heermann'sGull
VELARDE,
293-320.
(Larusheermanni)chicksby Yellow-footedGulls
J. L., AND P. W. SHERMAN.1976. AdHOOGLAND,
(Laruslivens)in dense and scatterednestingsites.
vantagesand disadvantagesof BankSwallow(RiColon. Waterbirds15:8-13.
46:33paria riparia)coloniality. Ecol. Monogr.
E. MS. Comparativebreedingbiology of
VELARDE,
58.
the Heermann'sGull (Larus heermanni)in Isla
R. E. 1978. Hawksand doves:attacksucKENWARD,
Rasa, Gulf of California,Mexico.
cess and selection in Goshawk flights at Wood- VELARDE,
ANDL.
R. ESQUIVEL,
E., M. S. TORDESILLAS,
47:449-460.
pigeons.J. Anim. Ecol.
VIEYRA.MS. Use of seabirdsas samplingagents
1975. Functional
OATEN,
A., ANDW. W. MURDOCK.
of commerciallyimportantfish populations.
response and stability in predator-preysystems.
Am. Nat. 109:89-298.
LITERATURECITED
The Condor95:708-711
? The Cooper Ornithological Society 1993
DIRECT AND INDIRECT CONSEQUENCES OF MINK PRESENCE IN A
COMMON TERN COLONY'
ANDRALPHD. MORRIS
GARYP. BURNESS2
Departmentof BiologicalSciences,Brock University,St. Catharines,Ontario,L2S 3A1, Canada
by variousmammalsis frequentlycited (e.g.,feralcats,
Felis domesticus,Ashmole 1963; Ermine,Mustelaerminea, Cairns 1985; Racoon, Procyonlotor,Emlenet
Colonialbreedingoccursin 98%of seabirdspecies(e..g, al. 1966; Otter, Lutra lutra, Ewins 1985; Red Fox,
and Montevecchi 1981).
Wittenbergerand Hunt 1985). Colonies are conspic- Vulpes vulpes, Maccarone
uous, however,and as predatorsare likelyattractedto Whilerelativelyfew citationsreportpredationby mink,
largeaggregationsof individuals,predationon seabirds Mustela vison, (e.g., Burger 1974, Olsson 1974, Folkestad 1982, Albericoet al. 1991, Burgerand Gochfeld
1991), mink can be a serious threatto seabirdpopulations. In Norway, for example, breeding of Black
'1Received 20 January 1993. Accepted 23 March Guillemots (Ceppusgrylle) currentlyis restrictedto
areas where mink are absent (Folkestad 1982). While
1993.
attacksby mink on gullsand ternsappearrare(Burger
2 Presentaddress:Departmentof Zoology, University of BritishColumbia,Vancouver,B.C., V6T 1Z4, 1974, Dunstone and Birks 1987, Albericoet al. 1991,
Canada.
Burgerand Gochfeld 1991), the slaughterof tern and
Key words: Common Tern;predation;parental neglect;exposure;Sternahirundo.
SHORT COMMUNICATIONS
709
TABLE1. Fateof chicksfrom studybroodsduringthe nocturnalperiodsof 30 May-7 June 1991as determined
by dawn nest checks. Broods were not checkedon the morningsof 4 and 5 June. The mink was firstseen on 1
June and was removed from the site on 8 June at 01:00 hr.
Date
30/5
31/5
1/6
2/6
3/6
6/6
7/6
8/6
9/6
10/6
Totals
Study
broods
(n)
8
9
12
11
11
8
8
7
8
7
At riskp
PresentAM
MissingAM
Dead AM
Totaldead/
missing
15
22
28
29
15
11
10
7
9
8
154
15(100.0)
22 (100.0)
27 (96.4)
13(44.8)
9 (60.0)
11(100.0)
4 (40.0)
6 (85.7)
8 (88.9)
7 (87.5)
122
0 (0)
0 (0)
1 (3.6)
4(13.8)
3 (20.0)
0 (0)
2 (20.0)
1(14.3)
1 (11.1)
1(12.5)
13
0 (0)
0 (0)
0 (0)
12(41.4)
3 (20.0)
0 (0)
4 (40.0)
0 (0)
0 (0)
0 (0)
19
0 (0)
0 (0)
1 (3.6)
16(55.2)
6 (40.0)
0 (0)
6 (60.0)
1(14.3)
1(11.1)
1(12.5)
32
(n)
n (%)
n (%)
n (%)
n (%)
SThe numberof chickspresentduringthe nightand at riskto possiblenocturnalpredation.
gullchickshasoccasionallyresultedin almostcomplete
breeding failure (Folkestad 1982). We report a case
where nocturnalparentalneglect,as a resultof adults
stayingoff their nests in responseto a mink, resulted
in many indirectchick deaths and consequentfitness
costs to adults.
MATERIALSAND METHODS
The observationswere made at a Common Tern colony on a concretebreakwater,I km offshorein Lake
Erie,nearPortColborne,Ontario(420 52'N, 79 15'W).
Approximately900 pairs of Common Terns nest on
the loose gravel substrateof the breakwaterand presently comprise the largest Common Tern colony on
the Great Lakes (Morriset al. 1992).
An observationblindwas erectedpriorto the arrival
of terns in late April at the edge ofa 15 m x 4 m area
of known high density breeding.Daily or twice daily
nest checkswereconductedbeginningon 29 April 1991.
Seventeen pairs of birds were chosen for a detailed
behavioral study (Burness 1992) and their breeding
success was followed until the last chicks reached20
days of age. Diurnal observation sessions were performedfor six hours/dayfrom 30 May-18 June 1991,
and for three hours/dayalternatingmorningand eveningfrom 19June-28 June 1991. Diurnalobservations
coincided with periods of peak HerringGull (L. argentatus) predation (06:00-09:00 and 17:00-20:45,
Morris 1987). Nocturnal observation sessions were
performedon 5 June(00:30-05:45),and on 6 Juneand
7 June (22:30-03:00), to determine the source of an
unknownnocturnaldisturbance.Daily nest checks of
chicksurvivalwereperformedat dawnand duskwhich
allowed for calculationof diurnaland nocturnalpredation rates.
RESULTS
While a largernumberof pairs had broods within our
study area, the observationsand numericaldata that
follow are restrictedto the chicks associatedwith the
17 studypairs.The firstegg laid by a studyfemalewas
found on 6 May 1991, and the first chick hatched28
May. The first study chick was observed missing on
29 May. A mink was first seen on 1 June running
throughan adjacentRinged-billGull (L. delawarensis)
colony, and a dawn nest check on 2 June performed
on 11 remainingstudy nests found that 16 of the 29
(55.2%)chicks that were presentthe night before,and
at risk to predation,were either dead or missing (and
presumeddead;Table 1).Periodicallythereafterduring
the daytime observation sessions the mink swam or
ranbehindthe breakwallfrom its den, towardthe east
end of the colony. The terns exhibited a stereotypical
mobbing behavior,hoveringas a tight groupapproximately 10 m above the water surface.The mink was
never seen enteringthe colony duringthe day.
Duringan overnightobservationsession on 5 June
however, we saw the mink make repeatednocturnal
tripsthroughthe terncolony. First,it swam or raneast
from its den behindthe lengthof the breakwall,out of
sight of the terns, and then appearedfrom over the
back of the breakwalland ran into the east end of the
colony. The mink then ran from east to west through
the colony towardits den, attackingchicks as it went.
During the 47 min of mink activity (00:55-01:42, 5
June),it ranthroughthe colony 16 times. Poor lighting
conditions prevented accurate quantificationof the
numberof chickstaken.However,on each of five trips
madebetween00:55-01:14(5 June),the minkwas seen
to captureand carrya singlechick towardits den. The
chicks varied in size, but the largestappearedabout
6-7 days of age. Although caching by the mink was
not observed on 5 June, on 6 and 7 June, the mink
capturedand cacheda numberof chicks in rocksnear
the blind. Some chickcarcasseswerefoundthe following morning,althoughas they were not banded,their
natal nests could not be determined.The mink was
removed from the colony at approximately01:00 hr
on the morning of 8 June, and chick loss thereafter
droppedto pre-disturbancelevels (Table 1).
When the mink enteredthe colony most adults immediatelyperformed"dreads"(Marplesand Marples
1934) and circled the colony. After the mink passed
througha regionof the colony the birds with nests in
710
SHORT COMMUNICATIONS
that area returnedwhile those in the directvicinity of
the mink hovered about 5 m above their nests. The
frequentruns by the mink through the colony on 5
June left little time for the birds to settle before they
took flightagain.
The numberof chicks recordedas missing or dead
at the dawn check after an overnight period of nocturnalpredationwhen the mink was active (Table 1)
was contrastedwith the numbermissingor deadat the
dusk check. The numberof chicks found dead in their
nests at the beginningof a dawn nest check ranged
from 0-41% of the numberof chickspresentthe night
beforeand consequentlyat riskto nocturnalpredation
(Table 1). Between0 and 20%of chicks went missing
overnight.In contrast,no chicks were found dead in
their nests duringthe day while the numberof chicks
that went missing over the day rangedfrom 0-20%.
Between 30 May and 7 June, 22%(29 of 130) chicks
werefounddeador wererecordedas missingovernight.
This was significantlygreaterthanthe 8%(nineof 108)
recordedas missingor dead duringthe day (G = 6.70,
df = 1, P < 0.05).
Chicks that went missing overnightduringperiods
of mink activity were marginallyolder (4.60 days +
1.58, n = 10) than those that went missing duringthe
day (3.22 days ? 1.56, n = 9; Mann-WhitneyU-test,
U = 22.5, Z = -1.88, P = 0.06). Therewas, however,
no significantdifferencebetweenthe age of deadchicks
(4.22 days 1.22, n = 18)and those that went missing
?_ days + 1.50, n = 10; U = 76.0, Z =
overnight(4.60
-0.69, P = 0.49).
The number of missing chicks is a likely index of
the time spent by the mink in the colony. There was
a significantpositive correlationbetweenthe percentage of chicks that were recordedas missing at dawn
and the percentagethat werefound dead in their nests
(Spearman-rankcorrelation,rs = 0.81, Z = 2.0, P <
0.05). This suggestsa relationshipbetweenthe number
of dead chicks and the length of time that the mink
was in the colony.
A comparisonamong the minimum daily temperaturesrecordedat St. Catharinesairport(Atmospheric
EnvironmentService monthly meterologicalsummary) over 30 May-7 June in 1989, 1990, and 1991 revealed significantdifferencesamong years when data
werelog-transformed(F(2)= 4.41, P = 0.02). The mean
minimumtemperaturein 1991wassignificantlywarmer (13.5 ? 3.880C, n = 9) than 1990 (10.0 ? 4.24?C,
n = 9, ScheffeF-test = 3.85, P < 0.05). Regularnest
checks performedin 1990 in the absenceof the mink
found few dead chicks despite cooler temperatures.
DISCUSSION
This study indicates that the presenceof a mink had
severeincidentaleffectson the annualbreedingsuccess
of Common Ternsat this location.More strikingthan
the numbersof missingchickswerethe numbersfound
dead in their nests, and these only duringdawn nest
checks.Thereareat leastthreepossiblecausesof death:
(1) chick starvation;(2) direct predationby the mink;
(3) exposure due to parentalneglect during mink incursion.First,it is unlikelythat such largenumbersof
chickswould have simultaneouslysuccumbedto starvation and there was no indicationof body mass loss
fromthe sternumregiontypicalof starvingbirds(Blokpoel et al. 1984). Second, as dead chicks showed no
obvious signs of injury,criticalwounds by the mink
seem unlikely.
We suggest, therefore,that the chicks died due to
exposure.Parentalneglectin responseto an avianpredator has been suggestedpreviouslyin Common Terns
(Nisbet 1975, Hunter and Morris 1976, Nisbet and
Welton 1984, Shealerand Kress 1991). While Common Tern chicks are capable at three days of age of
maintaininga nearly stable body temperatureindependent of ambient, they likely have sub-adultbody
temperaturesfor some period of time (LeCroyand
Collins 1972). The averageage of the dead chicks was
four days and rangedfrom 2-6 days so the degreeof
temperatureregulation varied between chicks. Furthermore,the chickdeathswerenotedon the mornings
of 2, 3, and 7 June followingcool overnightminimum
temperaturesof 13.2 and 13.1 and 9.4?C,respectively.
On the night of 5 June, the mink kept adults off their
nests for 47 consecutive minutes (15%of the observation period) preventingbrooding by parents. The
positive correlationbetween the number of missing
chicks (a likely index of time spent in the colony by
the mink) and dead chicks (a likely index of degreeof
parentalneglect)supportsthis conjecture.
Duringthe mink attacksadultternsdid not abandon
the colony. Theirresponsesweredistinctfromthe synchronous nocturnaldesertion or "selective abandonment" reported in response to Great Homrned
Owls,
Bubovirginianus(Nisbet1975,NisbetandWelton1984)
and Black-crownedNight-Herons,Nycticoraxnycticorax(Hunterand Morris1976,ShealerandKress1991)
wherethe colonies remainedessentiallydeserteduntil
dawn. Our observationsmore closely resembledthe
"upflights"performedby Common Ternsin response
to a disturbancelocalized to one part of the colony
(Morrisand Wiggins 1986).
Chickswent missing from study broods duringthe
day in the same frequencyas overnight. Some were
likelypredatedby gullswhileotherscouldhave strayed
into neighbors'nests and been adopted (cf. Morriset
al. 1991). Chicks that disappeared overnight were
slightlyolder than those that went missing duringthe
day. This could have been because the mink could
more easily see the older, largerchicks, or they were
more prone to runningduringa nocturnalattack.
A diurnalnest check of the entirecolony performed
on 2 June showed that the occurrenceof dead chicks
was restrictedto the west end of the colony. As egg
layingstartedearlierat the east end, chicksat the east
end wereprobablyold enoughto surviveanycold nights
without being brooded. If so, we conclude that there
appearsto be a narrowwindowduringwhichternchicks
are subject to potential exposure due to parentalneglect.
The behaviorof adult ternsin responseto the mink
resultedin a heavy seasonalbreedingcost for individuals (some lost entirebroods).In long-livedorganisms
such as terns, selection is likely for self preservation.
Adultsthat lost chicksduringthe peakmay have relaid
later in the season (e.g., Palmer 1941 for Common
Tern; Massey and Atwood 1981 for CaliforniaLeast
Tern, Sterna antillarum).Consequentlyin 1991, the
SHORT COMMUNICATIONS
711
seasonal breedingsuccess of individuals,althoughre- LECROY, M., ANDC. T. COLLINS.1972. Growth and
survival of Roseate and Common Tern chicks.
duced by the mink, was not necessarilyzero.
Auk 89:595-611.
We thank M. Killoran for helping with behavioral
A. D., ANDW. A. MONTEVECCHI.
1981.
observationsof the mink, and J. P. Brucefor help in MACCARONE,
Predationand cachingof seabirdsby Red Foxes
much of the other field work. P. Ewins,J. Spendelow
(Vulpes vulpes)on Baccalieu Island, Newfoundand an anonymous reviewermade useful suggestions
land.
CanadianField-Naturalist95:352-353.
for improvementof the text. Fundingforthis and other
MARPLES,
G., ANDA. MARPLES.1934. Sea Terns or
researchwas provided through the Natural Sciences
Sea Swallows. Country Life Press, London, Enand Research Council of Canada (grant A6298 to
gland.
RDM).
MASSEY,B. W., AND J. L. ATWOOD. 1981. Second
wave nesting of the California Least Tern: age
LITERATURECITED
composition and breedingsuccess. Auk 98:596J. A. R., J. M. REED,ANDL. W. ORING.
ALBERICO,
605.
1991. Nesting near a Common Tern colony in- MORRIS,
R. D. 1987. Time-partitioningof clutchand
creasesand decreasesSpottedSandpipernest prebrood care activities in HerringGulls:a measure
dation. Auk 108:904-910.
of parentalquality?Studies in Avian Biology 10:
N. P. 1963. The biologyof the Wideawake
ASHMOLE,
68-74.
or Sooty TernSternafuscataon AscensionIsland. MORRIS,
R. D., ANDD. A. WIGGINS.1986. Ruddy
Ibis 103b:297-364.
Turnstones,GreatHornedOwls,andeggloss from
R.
D.
G.
D.
TESSIER.
H.,
BLOKPOEL,
MORRIS,
AND
CommonTernclutches.WilsonBull.98:101-109.
1984. Field investigationsof the biologyof Com- MORRIS,R. D., M. WOULFE,ANDG. WICHERT.1991.
mon Terns winteringin Trinidad.J. Field. OmrniHatchingasynchrony,chick care,and adoptionin
thol. 55:424-434.
the CommonTern:can disadvantagedchickswin?
1974.
J.
of
Franklin's
BURGER,
Breedingadaptations
Can. J. Zool. 69:661-668.
Gull (Laruspipixcan) to a marsh habitat.Anim. MORRIS,R. D., H. BLOKPOEL,
AND G. D. TESSIER.
Behav. 22:521-567.
1992. Managementefforts for the conservation
BURGER,
J., ANDM. GOCHFELD.
1991. The Common
of CommonTerncolonies:two case histories.Biol.
Tern:its breedingbiologyand socialbehavior.CoConserv.60:7-14.
lumbia Univ. Press, New York.
NISBET,I. C. T. 1975. Selective effects of predation
G. P. 1992. Foragingecology and parental
BURNESS,
in a tern colony. Condor 77:221-226.
behaviourin the Common Tern(Sternahirundo). NISBET,I. C. T., ANDM. J. WELTON. 1984. Seasonal
Brock
M.Sc.thesis,
University,St. Catharines,Ont.
variationin breedingsuccess of Common Terns:
Canada.
consequencesof predation.Condor 86:53-60.
D. K. 1985. Erminevisitationto BlackGuilCAIRNS,
V. 1974. Forandringarinom en population
OLSSON,
lemot colonies in northeasternHudson Bay. Conav tordmulAlcatordaoch tobisgrisslaCephusgrylle
dor 87:144-145.
i Ostergotlandsskargtrd 1954-1973. Vtr FtgelDUNSTONE,
N., ANDJ. D. S. BIRKS.1987. The feeding
vard 33:3-14.
ecologyof the mink (Mustelavison)in coastalhab- PALMER,R. S. 1941. 'White-faced' terns. Auk 58:
itat. J. Zool. (Lond) 212:69-83.
164-178.
R. M. EVANS,
J. T., D. E. MILLER,
EMLEN,
ANDD. H. SHEALER,
D. A., ANDS. W. KRESS. 1991. Nocturnal
THOMPSON.
1966. Predator-induced
parentalneabandonmentresponse to Black-crownedNightglect in a Ring-billed Gull colony. Auk 83:677Heron disturbancein a Common Tern colony.
679.
Colon. Waterbirds14:51-56.
P.
1985.
Otter
J.
on
predation Black Guille- WITTENBERGER,
EwlNS,
J. F., ANDG. L. HUNT,JR. 1985. The
mots. Br. Birds. 78:663-664.
adaptivesignificanceofcoloniality in birds.In D.
A. 0. 1982. The effect of mink predation
FOLKESTAD,
S. Farner, J. F. King, and K. C. Parkes [eds.],
on some seabirdspecies. Viltrapport21:42-49.
Avian biology, Vol VIII. Academic Press,OrlanR.
AND
R.
D.
HUNTER, A.,
MORRIS. 1976. Nocturnal
do.
predationby a Black-crownedNight-Heronat a
Common Tern colony. Auk 93:629-633.