The Effects of a Perceived Predation Risk on Chickadee
Body Weight and Foraging
Amy Elizabeth Gordon
Neuroscience Graduate Program
Submitted in partial fultillment of the requirernents
for the degree of iMaster of Science
Faculty of Graduate Studies
The University of Western Ontario
London, Ontario, CANADA
O Amy Elizabeth Gordon 1999
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lncreased fat reserves in passerines protect against starvation, but a b decrease
flight ability, possibly increasing predation risk. Theoretically, a trade-off should exist
between the starvation cïsk and the predation risk of maintaining lowered fat reserves.
Experiment one tested how black-capped chickadees (Purus orricapillus) adjun both
intemal (fat) and extemai (cache) reserves under a predation threat. Birds were exposed to
a taxidermic mount of either a sharpshïnned hawk (Accipiler striafus) or a red-winged
blackbird (Agelaius phoeniceirs). Taxiderm ic mount days altemated with baseline days.
Evening weight and caching were significantly lower on hawk mount days than on the
following baseline days. Behaviour on hawk mount days minimized predation nsk and
die next day minimized starvation risk. Experiment two ex-ned the prolonged effect of
hawk exposure on feeding. No signitïcant di fferences in weight or daily intake were
found, although these results may have been confounded with the deteriorating condition
of the birds.
Kevwords: Chickadee; predation risk: starvation risk; body weight; foraging.
iii
Acknowledgment of Co-Authors hip
Al1 experimental work was c d e d out solely by Amy Gordon. Dr. Sherry
participated in the conception of the experiments presented here and in the writing of the
manuscnpt-
Acknow ledgments
First, I would like to thank my supenrisor, Dr. David Sherry, for his advice and
support throughout this project. I also want to thank my Iab-mate, Mike Boisvert, for
keeping things interesthg around the [ab (and for providing an exarnple of senous results-
oriented dedication). Thank you also to Shelley, Jen, Kathleen and Ioanne for your
support, encouragement and Eendship. Findly, 1 wodd iike to thank m y parents for
thrü incredible support and encouragement over the years.
................................................. 1.4 Predation Risk 9
......................... 1.4.1 Starvation Risk Versus Predation Risk 10
........................ 1.4.2 Predation Risk and Food-Ston'ng Birds 13
................. 1-43 Regulation OP Fat Reserves and Cache Reserves 14
................................................. 1.5CurrentStudy 15
................................................ 1 -6 Reference List 16
Chapter 2
Effect of a perceived predation threat on chickadee body weight and forrging . . - 2 3
2.1Introduction .................................................. 24
2.2Methods ..................................................... 27
................................................. 2.2.1 Subjects 27
................................................. 2.2.2 Design -27
............................................... 2.2.3 Procedure 28
................................................. 2.2.4 Analysis 30
2.3 Results ...................................................... 31
2.3.1 Weight ................................................. - 3 1
.................................................. 2.3.2 Eating 35
................................................. 2.3.3 Caching 35
2.3.4Activity ................................................. 35
2.3.5 Vigilance .....................................-......... - 3 7
................................................... 2.4 Discussion 39
.................................. 2.4.1 Body Weight and Foraging 39
........................................ 2.4.2 Change in Activity 40
2.4.3Vigilmce ................................................ 40
.............................................. 2.4.4 Cohclusions 4t
........................................ 2.4.5 Other Explanations 42
..................................... 2.4.6 Significance OP Results 44
................................................. 2.5 Reference List 47
Chapter 3
............................................ Conclusioas and Perspectives 50
.................................... . 3 L Conclusions and Perspectives 51
....................................... 3.1 -1 Summary of Results 51
.......................... 3.1.2 Alternate Anti-Predator Behaviours -51
............................... 3.1.3 Appiicability for Other Species 52
............................................. 3.1.4 Future Work 52
................................................ 3.2 Reference List 53
List of Figures
Figure 2.1 Mean afternoon body weight over the three experimental blocks in experiment
one .................................................................. 32
. .............. Figure 2.2 Afiemoon weight over the 18 trial days in experiment one ~3
....................... Figure 2 3 Mean weight gain per trial in experirnent one - 3 4
...................... Figure 2.4 Mean caching rate per trial in experiment one - 3 6
............... Figure 2.5 Long head-ups over the 18 trial days in expriment one - 3 8
Chapter 1
General Introduction
1, l The Blac k-camed C hickadee
The b lack-capped c hickadee (Purzrs rrrriccrpiZizcs) is a small common bird found
throughout most of North Amerka. C hickadees generally weigh between IO and 14 g
(Smith 199 1). in the winter. chickadees fotm large flocks. while in the spnng and
sumrner they segregate into temtonal breeding pairs (Smith l991). Chickadees feed
mainly on seeds d u ~ g the faIl and winter. and mainly on insects during the spring and
summer (Smith 199 1).
1 -1.2 Food-S torinp;
Chickadees are a food-storing species. meaning that they cache individual food
items in separate locations and retrieve them at a later the. Most food-storing is done in
the fall. when chickadees can store up to hundreds of food items a day (Odum 1942,
Sherry 1984).
Food-storing is generdly believed to be an adaptation which allows individuals to
survive penods of unpredictable or variable food supplies (McNamara et al. 1990).
Problems may aise from fluctuations in the food supply itself, changes in the cost of
foraging, changes in energy requirements or increased cornpetition for resources
(McNarnara et al. 1990). Hoarding more food than can be immediately consumed may
permit the bird survive periods of shortage.
3
Lucas and Walter ( 199 I ) summarize four main theories about the advantages of
food-storing. Fint, if caching a food item is faster than eating it, caching may dlow a
forager to get a disproportionate share of a short-lived resource (Clarkson et al, 2986).
Second, if birds cache most when food is abundant and retrieve most when food is scarce,
caching may reduce the rïsk of starvation. Third. if fat storage is costly, cachîng may act
as an alternative form of reserve (Lima 1 986). Fourth. cactiing may "decouple" the need
for food and the need to forage for it (S heny L 985). This would allow the bud to eat
when it is most profitable to do so, such as when predation risk is low.
t -1.3 Chickadees and Predation Risk
The main predators of chickadees are hawks ofthe genus Accipiter: the sharp-
shimed hawk (A. striarus) and the Cooper's hawk (A. cooperii) (Smith 199 1). Other
common predators include Amencan kestrals (Fuko spurverius), merlins (F.
colirmbarius), northem pygmy owls (Glaucidium gnoma), eastem screech owls (Otus
asio), boreal O wls (Aegolius jicnerr us) and northern shr i kes (Lanius exaibitor) (Bent
1946, Smith 1991). Healthy chickadees are generally agile enough to escape such
predators and usually only birds weakemd by age or disease are captured (Smith 199 1).
Non-avian predators, such as weasels (ibhsrela sp.), climbing snakes and squirrels. are
most likely to capture chickadees at the nest or roost site (Smith 199 1).
The sharp-shinned harvk. however. is probably the most common predator of
4
chickadees (Smith 199 1). Their diet consists primady of small birds and is known to
include chickadees (Bent 193 7)-
1.2 Anti-Predator Behaviours
Predation risk plays an important role in the behaviour of smdl birds. Even
though the predation of adult birds is relatively rare. the rnere presence of predatoa elicits
anti-predator behaviour (Lima 1993. Lima and Di1 1990).
SrnaIl birds exhibit a wide variety ofanti-predator behaviours. One common fom
of predator evasion is flock formation. As flock size increases. the arnount of vigilance
by individual flock members decreases, thus increasing the amount of foraging time
available for each individual (Waite L987). SimiIarlyt the unpredictable movements of
flocks rnay help to prevent hawks from leaming their daily routine (Gaddis 1980).
Staying close to protective cover is another common form of anti-predator
behaviour (Witter and Cuthill 1993). Birds may also alter when they forage, where diey
forage, what food items they eat and how they handle food items (Lima and Di11 1990).
For example. birds may select a less profitable food item if it allows the bird to be more
vigilant while eating it (Le. if the bird can eat the food item with its head up rather than its
head down),
I -2- 1 Escatie Tactics
When faced with an actual predator attack. birds may either freeze in an attempt to
avoid detection, or they may make a quick dash for shetter (Lima 2993). Different
species tend to have different escape tactics. Tactics may also Vary depending on the
surrounding habitat, the availabte shelter. the weather and the type of predator (Lima
1993)-
Chickadees and titrnice oFeastem North Amerka use a woody-cover dependent
tactic common to many passerines (Lima 1993). In other words, they make a quick dash
to cover when under attack. Dense woody cover is likely a fairly safe refuge, although
accipiter hawks have been known to pursue birds into such cover (Smith 199 1).
1 -3 Passerine Bodv Mass
1 -3.1 Variations in Bodv Mass
The body mass of small birds at high latitudes
the more northerly populations of a species tend to be
more southerly populations (Blem 1976. King 1972).
varies seasonally. Individuais in
heavier than individuals in the
In addition, the mass of individual
birds in a northem pcipulation tends to peak during midwinter (Helms and Dniry 1960).
Finally, birds show more pronounced daily fluctuations in body mass in the winter
(Metcalfe and Ure 1995). These daily variations in body mass occur because birds build
up fat reserves during the day and deplete them ovemight (Metcalfe and Ure 1995). In
6
the winter. birds may lose 7-1 5% of their body mass overnight (Huriy 1992)- Fat reserves
have been s h o m to account for most of these variations in mass (Hurly 1992)-
Little is known about the daily pattern of weight gain in small birds. Hurly (1992)
found that weight gain was delayed until the end of the day in ma& tits (Parus
puIzatrr's)). This tactic was maintained when the birds were on both a low variability and
a high variability food suppIy. He suggests that the marsh tits were using stored food to
keep them on a set weight trajectory each day. In other words, the stored food would
even out variability in the food suppIy.
1 - 3 2 Cause of Variations in Fat Reserves
A number of factors may influence how much fat reserves a bird carries. These
factors inchde (but are not limited to) temperature (Rogers 1995), photoperîod (Witter et
ai. 1995), corticosterone leveb (Witter et al. 1995), sociai status (Ekrnan and Lilliendahl
1993), the predictability of the food supply (Blem 1990. Ekman and Hake 1990,
Pravosudov and Gmbb 1997. Witter et al. 1995) and differences in energy expenditure .
It appears that changes in body mass are not sirnply a passive refîection of food
availability or energetic expenditure and that birds actively regulate the size of their
energy reserve according to their needs (Lima 1986, Witter and Cuthill 1993, Witter et al.
1995)-
1 -3 -3 Function of lricreased Fat Reserves
Excess fat reserves may provide body insulatioa mechanical suppoh protection,
buoyancy and both sexuai and social signals ( Witter and CuthiIl 1 993). More
imponantly, however. it is generally assumed that the more fat reserves an animal cm-es,
the lower the rïsk of starvation that animal faces. Fat reserves are the major energy
reserve of most birds (Grïminger 1986. Witter and Cuthill 1993). McNamara and
Houston (1990) suggested that starvation risk decreases almost exponentially as fat
reserves increase. These fat reserves proiect against cold temperatures, long winter nights
when birds are unable to forage. and unpredictable food supplies (Blem 1990, King
1972).
In theory, therefore. under conditions of limited food availability, birds should
always carry the maximum fat reserves that they are able to. in order to reduce the risk of
starvation. However, this almost never occurs in nature (Witter and Cuthill 1993). This
suggests that there are costs associated with carrying fat.
1 -3 -4 Costs of Carrving Fat Reserves
Carrying extra fat resen-es may require increased muscuIature. which rnay
increase metabolic costs, even during inactivity (Le. because of higher oxygen
consumption and increased energy demand) (Witter and Cuthill 1993). More heat may be
required to warm a larger body and excess fat may decrease thermal conductivity (Scott et
al. 1996). Flying with the extra mass also requires more energy (Scott et al. 1996)- On
the other hand, incfeased fat reserves could have insulatory benefits which would
8
decrease metabolic rate at low temperatures (Witter and Cuthill 1993). An indatory
benefit of fat has not, however. been demonstrated in birds (Scott et al. 1996).
More importantly. Blem (1975) suggested that carrying excess fat may impair
flight ability. Specifically. he suggested that excess fat may affect wing loading and lead
to inefficient flight energetics. An increase in m w without an accompanying change in
wing shape (Le. an increase in wing loading) is predicted to decrease take off angle.
manoeuverability, linear accelerat ion, and the maximum rate of ascent (Alemam and
Lindstrom 1990, Hedenstrom 1992. Marden 198% Norberg 1990). In fact, there is
considerable evidence that fat levels have a negative eKect on flight performance.
Wiîter et al. (1994) added weights to European Starlings (Sturnm vulgaris) and
found that birds with a higher "body" mass were less manoeuverable and had a Iower rate
of ascent than control birds. Adding weights to birds may not, however, mimic n a d
fat reserves. The weights may. for example. shift the bird's center of gravity (Metcalfe
and Ure 1995).
Metcalfe and Ure ( 1995) studied the take offs of captive zebra finches
(Taeniopygia guttata). They compared flight performance at dawn, when the birds were
lighter. to performance at dusk. when the birds were heavier. Individuds were
significantly slower, showed less manoeuverability and took longer to reach a particular
vertical height when they were heavy compared to when they were light. The birds were
only 7% heavier at dusk than at dawn and yet were over 30% slower at dusk- The birds in
this study showed Iess daily variation in body m a s than wild birds, suggesting that the
impact of body mass on flight pertbrmance may be even more pronounced in the wild.
They predicted that the daily mass gain of small birds would produce a 20 - 50% increase
in the time required to Ay a fixed vertical distance-
1-4 Predation Rkk
Lima (1986), however. pointed out that if fat reserves are required for swival.
then they should be maintained regardless of the eEect on flight eficiency. h other
words, if fat reserves are required for survival. then birds have no choice but to pay the
cost of decreased flight effkiency. There must be some other factor, then, that influences
how much fat a smali bird carries.
It has been suggested that one reason birds do not maintain maximum fat reserves
is that this would increase predation risk (Grubb and Pravosudov 1994, Lima 1986.
McNamara 1990, McNamara and Houston 1990). As discussed by Lima (1 986), this
could happen in two ways. Fint of ail. maintaining increased fat reserves requires the
bird to spend more time foraging. which increases the likelihood of encomtering a
predator. Secondly, the decrease in Ilight ability may increase the chances of k ing
caught by a predator. A small bird threatened by a hawk must be able to take off rapidly
because most avian predaton rely on surprise attacks and have a greater chance of
10
success before the prey is fully airbome (Metcalfe and Lice 1995). The bird must also be
manoeuverable in the air in order to avoid any subsequent attacks. As discussed earlier.
excess fat reserves will decrease take off angle. linear acceleration, clirnb rate and
manoeuverability and so even minor variations in the speed and agility of small birds rnay
have a major impact on their risk of predation.
Kullberg et al. (1996) studied the take offs of blackcaps (Sylvia africapiZla) under
a simulated hawk attack. They assumed that this would force birds to put maximal effort
into their escape speed and angle. They were concemed that on a normal take off, a fatter
bird might conserve energy by reducing take off speed and angle and that this would lead
to an overestimation of the effects of fat on tlight ability (Le- for Metcalfe and Ure 1995).
They found that birds with a Iarger fat load were slower and had a lower angle of ascent
than leaner birds. Interestingly. however. the effect of fat on speed and angle were
considerably Iess pronounced than those found by Metcalfe and Ure (1993). This rnay
indicate that fatter birds do indeed try to conserve energy on a normal take off, although
some of the difference rnay be due to speciss differences. Nevertheless, high fat reserves
do reduce flight ability even during a simulated predatory attack.
1.4- 1 Starvation Risk Versus Predation Risk
It appears, there fore. t hat there rnay be a trade-O K between starvat ion risk and
predation risk. As birds get heavier. their starvation risk declines, but their predation rïsk
rnay increase. Similady, if a bird [oses weiglit. it rnay lower its predation nsk, but
11
increase its stawation nsk- Theoretically, birds should regulate their weight according to
whether starvation or predation is the greater threat- Therefore. birds facing a predation
risk should lower their fat levels because predation is the larger threat (Lima 1986).
Experimental resdts, however. have not been clear cut-
Gosler et ai. (1995) found that a population of great tits ( P u m major) in England
maintained higher fat reserves dunng a penod of years when sparrowhawks (Acc@iter
nisus) were absent (due to pesticide poisoning). They then maintained lower fat reserves
when the sparrowhawks retumed. These changes were due to changes in the mass of
individual tits and not due to selection of heavier tits by the hawks. Wrens, a species
rarely taken by the sparrowhawks, showed no significant change in body m a s over this
time period.
uiterestingly, when sparrowhawks were present, the great tits were leaner in years
when the great tits' preferred food, beechmast, was abundant than in years when it was
not abundant (Gosler et al. L995). When sparrowhawks were absent. however, mass was
unaffécted by beechrnast abundance. This suggests that when food is plentiful, the
reduced starvation nsk aliows birds rnaintain Lower fat reserves. This, in tum, Iowers
predation nsk. When predatos are absent. however. there is no cost to maintaining
higher fat reserves. The birds can therefore aKord to protect more thoroughly against
starvation risk. This strongly supports the theory of a trade-off between starvation risk
and predation risk.
12
Only two experiments have directly tested the effect of a perceived predation
threat on body weight. Lilliendahl ( 1997) tound that greenfinches (Corduelis chlori")
maintained a lower evening body mass in response to a mounted hawk The rnount, or a
plastic bottle (the control). was rotated around the room in a circle five times a day. Body
m a s was lower &et a hawk trial than afier a control trial- Birds were also slower to
resume foraging afier seeing the hawk than the control. This study supports the
prediction that birds wili maintain a Iower body weight under a predation risk.
In contras& Pravosudov and Gmbb ( 19%) found that tufted titmice (Parus
bicolor) maintained a higher weight under a perceived predation risk. They exposed the
titmice to a taxidermie mount of either a mouming dove (Zenaida rnacroura) (no ttireat
control) or a sharp-shinned hawk (titmouse predator). Birds perched and flew during
dove exposure, but fioze during hawk exposure. Both vigilance and delay in ceturning to
foraging were significantly greater following hawk exposure. Birds therefore appeared to
be responding to an increased predation risk. Evening body mass and mean daily mass
gain were significantly greater during the hawk treatment. The increase in gain rate seen
during the treatment period. suggests that the birds fed more intensively throughout the
day, even though they intempted al1 activity during exposure to the hawk model.
Pravosudov and Grubb's findings do not support the prediction of a starvation - predation risk trade-off and differ from the results of Gosler et al- (1995) and Lilliendahl
(1997). It is possible that different species may have different tactics. Greenfinches feed
13
in open areas and fty to couer when under attack. This rnay make flight ability very
important (Lilliendahl 1997). Titrnice. on the other hand, tend to feed under cover. which
rnay mean that they can freeze when a predator is in the area rather than having to fly to
cover. Altematively, Pravosudov and Gmbb (1 998) point out that the random
interruptions of feeding caused by hawk exposure rnay have affiected starvation risk and
lead the birds to carry excess fat as a b a e r against fasùng periods spent under cover. In
nature. however, food suppIy rnay be Iimited and unpredictable and birds rnay not be able
to increase their body m a s quickly between predator appearances. Therefore, in the
wild, body weight rnay decrease as a consequence of reduced foraging time and not
because carrying fat is costly.
The results of Pravosudov and Gmbb ( 1 998) suggest that carrying more weight is
not necessarily associated with a higher risk of predation. More work is, however.
needed to determine why the results of this study differ from the theory of a predation -
starvation risk trade-off.
1 -4.2 Predation Risk and Food-Stonng Birds
Food-storing birds have an option which other birds do not have: they can store
food reserves as intemal fat reserves or in external cache reserves. Both snategies have
costs and benefits. Fat reserves wiil increase body mass, which rnay increase predation
Bsk and energy expenditure, as discussed above. On the other hanci, fat reserves can be
accessed and metabolized 21 hours a day. Making and retrieving caches consumes
14
energy and lowers vigilance for predators (Pravosudov and Gmbb 1997). Caches can
also be lost due to memory loss and pilferage (McNamara et al. 1990).
1 -4.3 Regulation of Fat Reserves and Cache Reserves
Food-storing birds appear to cegulate both their fat reserves and their cache
reserves. Both types of reserves play an important role in swivai - fat reserves are just
as important for food-stocing species as for non-storing species. For example,
Pravosudov and Gnibb (1997) found that the body mass and caching rate of tufted titrnice
bo th increased under an ;npredictable food supply. S imilarly. subordinate willow tits.
who have a less predictable food supply than do dominant birds. tend to carry greater fat
reserves than dominant birds (Clark and Ekman 1995. Ekman and Lilliendahl 1993.
Witter and Cuthill 1993).
It is possible that birds may regulate their fat and cache reserves differenrially and
may favour one mode of storage over the other depending on the situation. Many factors
affect the division of food reserves between fit and caches, such as predictability of the
food supply, dominance aatus, ambient temperature and the presence of predatos (Grubb
and Pravosudov 1 994, McNarnara et al. 1990. Pravosudov and Gmbb 1997). For
example, Hurly ( 1992) found that marsh tits increased caching, but not body weight.
under an unpredictable food supply.
How food-storing birds regulate caching and îàt reserves under a predation risk
has not been examined.
1-5 Current Studv
This thesis explores the putative trade-off between the starvation risk and the
predation risk of carrying increased fat reserves. The contradictory resultî of Pravosudov
and Grubb (1 998) and LiIiiendahl ( 2 997) indicate that there is much to be learned in this
area. We exarnined the effects of a perceived predation risk on the body mass and
foraging behaviour of black-capped chickadees. In particular. we were interested in how
chickadees regulate their fat and cache reserves.
1-6 Reference List
Alestam. T. & Lindstrom. A. 1990. Optimal bird migration: the relative importance of
time, energy and safety. In: Bird Mimtion: the ~hvsioioerv and ecoohysioloev
(ed. E. Gwinner), pp. 3 3 1 -3 5 1. Berlin: S pringer-Verlag.
Bairlein, F. 1991. Body mass of garden warblers Sylvio borin on migration: a review of
fieId data. Voeelwarte, 36,4806 1 -
Bent, A.C. 1937. Life histories o f North American birds of prey. US. Natural Museum
Bulletin. 167 (Dover edition. 196 1. part 0.
Bent, A.C. 1946. Life histories o f North American jays, crows and titmice. U S . Natural
Museum Bulletin. 19 1 (Dover edition. 1964. part II).
Blem, C.R. 1975. Geographic variation in wing loaduig of the House Spmow. Wilson
Bulletin, 87, 543-549.
Blem C.R. 1990. Avian energy storage. Current O m i t h o l o ~ 7,594 13.
Clark, C. W. & Elcman, LB. 1995. Dominant and subordinate fattening strategies: a
dynamic game. Oikos. 72.205-2 11.
CIarkson, K.. Eden, S.F., Southerland, W.J. 81 Houston A l 1986. Density dependence
and magpie food hoarding. Journal of Animal Ecolow. 55, 1 11-121.
Ekmm JB. & Hake, M.K. 1990. Monitoring starvation risk: adjusmients of body
reserves in greenfuches (Cardzielis chloris L.) during periods of unpredictable
foraging success. Behavioral EcoIo~v, 1.62-67.
Ekman, J.B. & Lilliendahl. K. 1993. Using priority to food access: fattening strategies in
dominance-struc tured wil1ow tit (Punis montanus) Bocks. Behavioral Eco 10 W. 4.
232-23 8.
Gaddis, P. 1980. Mixed flocks, accipiten. and antipredator behavior. Condor, 82.348-
349.
Gosler, AG., Greenwood. J.J.D. & Perrins. C. 1995. Predation risk and the cost of king
fat. Nature, 377,621-623,
Griminger, P. 1 986. Lipid metabolism. In: Avian ohvsioloey (ed. P.D. S turkie), pp.
345-358. New York: S prïnger-Verlag.
Gmbb, T.C. Jr. & Pravosudov, V.V. 1994. Toward a generai theory of energy
management in winterïng birds- Journal of Avian Biolow. 25,255-260.
Hedentrom. A. 1992. Flight performance in relation to fuel load in birds. Journal of
theoretical Biolopy, 158.535-537-
Helms, C.W. & Drucy, W.H.. Jr. 1960. Winter and migratory weight and fat: fietd
studies on some North Arnencan buntings- Bird-bandin% 3 1, 1-40.
Houston, A L & McNamara, J.M. 1993. A theoretical investigation of the fat reserves
and mortality levels O € small birds in winter. Omis Scandinavica, 24,205-2 1 9.
Houston, AL, McNam- J.M. & Hutchinson, J.M.C. 1993 - Generai results concerning
the trade-off between gaining energy and avoiding predation. Philosoohical
Transactions of the RovaI Societv of London. Series B, 34 1,375-397.
Hurly, T.A. 1 992. Energetic reserves of mars h t its (Parus palu~rris): food and fat storage
in response to variable food supply. Behavioral E c o l o ~ ~ 3, 18 1-1 88.
King, I.R. 1972. Adaptive penodic fat storage by birds. Proceedings of the 15"
International Ornitholoev - - Coneress. pp. 200-2 17.
Kullberg, C., Fransson. T. & lakobsson. S. 1996. hpaired predator evasion in fat
blackcaps (Sylvra atricapilla)- Proceedings of the Roval Societv of London,
Series B, 263, 1671-1675.
Lilliendahl, K. 1997. The effect o f predator presence on body mass in captive
greenfinches. Animai Behaviour. 53.75-8 1. .
Lima, S.L. 1986. Predation risk and unpredictable feeding conditions: determinants of
body mass in biids. Ecolow, 67.377485.
Lima, S.L. L 993. Ecological and evolutionary perspectives on escape from predatory
attack: a s w e y of North Amencan birds. The Wilson Bulletin, 105, 147.
Lima, S.L, & Dill, L.M. 1990. Behavioral decisions made under the risk of predation: a
review and prospectus. Canadian Journal of Zoolow, 68,6 19-640.
Lucas, J.R. & Walter. L.R. 199 1. When should chickadees hoard food? Theory and
experimental results. Animal Behaviour, 4 1.57960 1.
Marden, J.H. 1987. Maximum Iift production during take-off in flying animals. Journal
of Experïmental Biolow, 130,235-258.
McNamara, J.M. IWO. The starvat ion-predation trade-O ff and some behavioral and
ecological consequences. In: Behavioral Mechanisms of Food Selection (Ed. By
R.N. Hughes), pp.39-58. Berlin: S pringer-Verlag.
McNamara, J .M- & Houston- A L 1990- The value of fat reserves and the trade-off
between starvation and predation, Acta Biotheoretica, 38-3 7-6 1.
McNamara, LLM, Houston, A L & Krebs, LR- 2990- Why hoard? The economics of
food storing in tits, Parzrs spp. Behavioral Ecolooy, 1. 12-23.
Metcalfe, N.B. & Ure, S.E. 1995. Diumal variation in flight performance and hence
potentiai predation risk in small birds- Proceedinrrs of the Royd Society of
Series6 1,395400,
Norberg, U.M. 1990. VertebrutejZight. Berlin: Springer-Verlag.
Odum, E.P. 1942. Annual cycle of the black-capped chickadee 3. Auk, 59,499-53 1.
Pravosudov, V.V. & Gmbb, T C . Jr. 1997. management of fat reserves and food caches
in tufted titmice (Panîs bicolor) in relation to unpredictable food supply.
Behavioral Ecolow, 8.332439-
21
Pravosudov, V.V. & Gmbb. T C . Jr. 1998. Management of fat reserves in tufied titmice
Baelophus bicolor in relation to risk ~Epredation. Animal Behavior, 56,4944.
Rogers. C.M. 1987. Predation risk and fasting capacity: do wïntering birds maintain
optimal body mas? Ecolonv7 68. 1 OS 1 - 1 O6 1.
Rogers, C.M. 1995. Experimental evidence for temperature-dependent winter lipid
storage in the dark-eyed junco (Junco hyernalis oreganus) and song sparrow
(Melospua melodirr morphna). P hvsio loeical Zooloa: 68,277-289.
Scott, I., Mitchell, P.I. & Evans. PR, 1996. How does variation in body composition
affect the basal metabolic rate of birds? Functional Ecolow, 10,307-3 13.
Sherry, D.F. 1984. Food storage by black-capped chickadees: memory for the location
and contents of caches. Animai Behaviour, 32,45 1-464.
Sherry, D.F. 1985. Food storage by birds and mammals. Adv. Studv Behav., 15. 153-
188.
Sih. A. 1992. Prey uncertainty and the balancing of antipredator and feeding needs. The
American Naîuralist, 139, 1052- 1069-
37 -- Smith. S.M. 199 1. The Black-capped Chickadee. Comell Univ. Press, Ithaca, New
York.
Waite, T.A. L 987. Vigilance in the White-breasted Nuthatch: effects of dominance and
sociality. Auk, 1 04.429-434.
Witter, M.S. & Cuthill, LC. 1993. The ecological costs of avian fat storage.
Philosoohical Transactions of the Roval Societv of London. Senes B,340,73-92.
Witter, M.S., Cuthill, I.C. & Bonser. R.H.C. 1994. Expenmental investigations of mass-
dependent predation risk in the European Starling, Sfurms vulgaris. Animal
Behaviour, 48,20 1-222.
Witter, M.S.. Swaddle, J.P. & Cuthill. I.C. 1995. Periodic food availability and strategic
regdation of body mass in the European Starling, Sturnus vulgaris. Functional
E C O ~ O ~ ~ L 9,568-574.
Chapter 2
Effect of a perceived predation threat on chickadee body weight and foraging
A.E. Gordon and D.F. Sherry
Submitted to: h i m d Behmiozrr
2- 1 Introduction
The body mass of small passerines shows Iarge seasonal and daily changes. Birds
are heavier in the \inter, but they aiso build up their fat reserves each day and then
deplete them ovemight (Metcaife and Ure 1995)- [n the winter, birds may Lose 7-1 5% of
their body m a s overnight (Hurly 1992). Fat reserves have been shown to account for
most of these variations in mass (Huriy 1992)-
It is generdy assumed that the more fat reserves a bird carries, the lower the cïsk
of starvation the bird faces. These fat reserves protect against cold tempemes, long
overnight fmts and unpredictable food supplies @lem 1990, King 1972). In theocy,
therefore, birds should always carry the mavimum fat reserves that they are able to. but
this almost never occurs in nature (Witter and Cuthill L993). This suggests that there are
costs associated with carrying fat.
Several studies have shown that excess fat may impair flight ability by increasing
the energetic costs of flight and decreaçing acceleration (Metcalfe and Ure 1995, Witter et
al. 1994). Lima (1986) pointed ouf however. that if fat reserves are indeed required for
swival, then they should be maintained regardless of the decrease in flight efficiency.
That is, birds may have Little choice but to pay the cost of decreased flight eficiency if it
is necessary to maintain large fat reserves in order to survive. Given that birds do not
maintain maximum fat reserves, however. there must be some additional factor that
influences how much fat a srnail bird carries.
25
Therefore, it has been suggested that one reason birds do not maintain maximum
fat reserves is that this would increase predation risk (Gnibb and Pravosudov 1 994, Lima
1986. McNamara 1 W02 McNamara and Houston 1990)- As discussed by Lima (1986)
this could happen in two ways. First of dl, maintaining increased fat reserves requires
the bird to spend more t h e foraging. which increases the likelihood of encountering a
predator. Secondly, the decrease in flight ability may increase the chances of k ing
caught by a predator- A smail bird threatened by a hawk must be able to take off rapidly
because most avian predaton rely on surptise attacks and have a greater chance of
success before the prey is fulIy airborne (Metcal fie and LJre 1995). The bird must also be
manoeuvrable in the air in order to avoid any subsequent attacks. An increase in weight
wiI1 decrease take off angle, linear acceleration. climb rate and manoeuvrability and thus
even minor variations in the speed and agility of smail birds may have a major impact on
their risk of predation. Kullberg et al. ( 1996) showed that under conditions of a
perceived predation threat. fatter birds are indeed stower and have a lower angle of ascent
than ieaner birds.
There rnay be, thmefore. a trade-off between starvation risk and predation risk.
Birds facing a predation risk should lower their fat levels because predation is the larger
threat (Lima 1986). Experïmental results. however. have not been clear cut. Lilliendahl
(1997) found supponing results with greenfinches (Crirdueiis chloris). The greenfinches
maintained a lower body weight in the presence of a mounted spmwhawk. A recent
study by Pravosudov and Gmbb ( 1 998). however. found that tufied titrnice (Buelophus
26
bicolor) rnaintained a higher body wei& when faced with a perceived predation ïisk.
The titmice tended to remaîn fiozen while the stuffed hawk was in the aviary.
Pravosudov and Gmbb (1 998) proposed that the birds may carcy excess fat as a buffer
against potential hture interruptions of feeding caused by the hawk.
These d i f f e ~ g results rnay indicate that diffierent species have diEerent tactics. or
that the original theocy, of a predation-starvation risk trade-off, needs to be adjusted. We
examined the effects of a perceived predation risk on the body mass and foraging
behaviour of black-capped chic kadees (Purus utricapillus).
Chickadees are a food-ston'ng species. They cache (or hide) seeds in different
places and then corne back to retrieve them at a later time. This means that they can deal
with a perceived predation threat by adjusting both extemal food stores (caches) and
intemal food stores (fat reserves). Chickadees rnay regulate the two types of stores in a
similar or different manner. For example. by increasing their cache reserves, but not their
fat reserves, they could avoid gaining weight while still gathering food reserves. The
results of this experirnent will help clarify how chickadees manage both their extemal and
their intemal food stores under a perceived predation threat-
2 2 Methods
2.2.1 Subjects
Seven experimentally naive b lack-capped chic kadees were used in this
experiment. All birds were captured on the campus of the University of Westem Ontarîo.
London, Ontario, Canada (43O1 I ' N 8 1°1 8'W)- They were housed individuaily in wire
mesh cages (36 x 36 x 6 1 cm). The birds were kept in captivity for at least one week
before and afier the experiment and were then released.
Birds were maintained on a descending Iight cycle (in an attempt to promote food
storing). On Day 1, the lights were on for an approximate 10: 14 L:D cycle. The length of
the light phase decreased by 4 min a day for the remainder of the experiment (light onset
2 min later each moming and offset 2 min earlier each evening). During the day, birds
were provided with ad Libitum rnash. peanuts and striped sunflower seeds. Four birds
were tested in November 1998 and three were tested in January/February 1999.
2.22 Desim
A taxidermic mount of a juvenile sharp-shimed hawk was used to simdate a
predation threat (the mount was borrowed €rom the Zoology Department Museum at the
University of Westem Ontario). Sharp-shinned hawks are chickadee predators in the wild
and previous studies have successfiilly used a taxidermic mount in the lab to simulate a
predation threat (i.e. Pravosudov and Gmbb 1998)- The control mount was a juvenile
red-winged bIackbird (ilgelaius phoenicvrrr). which in nature poses no threat to
chickadees. The experiment was conducted as a within subjects design.
Two habituation days (in the aviary) preceded testing. The 18 day testing penod
was divided into three 6-day b tocks: redwing 1. hawk. redwing 2. Within each block, we
alternated mount presentation days and baseline days (when birds were released hto the
aviary, but no mount was shown). The birds saw each mount three times during each
block-
2.2.3 Procedure
Testing was done six days a week between 0800 and 1 ZOO h. Birds were food
deprived ovemight (approximately 17 h) in order to stimulate keding and caching
behaviours. The order in which individual birds were tested was balanced across days.
Each testing session lasted 45 min- Birds were released individually into an aviary (7m x
3m) and observed through a one-way mirror. Behaviour (see below) was recorded on a
computer event recorder.
A bowl of black oil sunflower seeds and a bowl of water were provided. Six
branches were distributed around the aviary. The branches were approximately 2 m high
and 5 cm in diameter, held venically in stands. Each branch contained 10 storage sites,
each 1 cm deep and 0.5 cm in diameter. A dowel perch, 5 cm long, was placed 3 cm
below each site. The positions of the branches were changed slightly each day, in order
29
to promote caching. The branches- however. did not move far and generdly maintained
their spatid relationship to each other.
On mount presentation days, the rnount was inserted into the aviary, through a
small window, after 10 min had elapsed in the trial and placed on a stand for
approximately 1 min- Birds were weighed irnrnediately d e r each trial and agah just
pnor to food deprivatlon at the end of the day (1600-1 700 h). Birds were caught by hand.
placed in a mesh bag and weighed on a digital scale (accurate to 0.01g). Weight gain was
calculated by subtracting moming weight from aftemoon weight and treating gain as a
percentage of the moming weight-
A number of behaviours were recorded during each triai. First, the number of
seeds eaten and cached dunng a trial were recorded. Caches were checked at the end of
each trial and removed- Second, al1 flights and perch locations were recorded. Each tree
was divided into three zones-the upper. middle and bottom. Only movements within a
zone of over 10 cm were recorded, while ail movements between zones or branches were
recorded. This data was used to estimate the distance each bird fiew during the trial. as
welI as the time spent in each branch and zone. Third, vigilance was estimated by the
average time between head-ups made while eating or handling a sunflower seed (as in
Pravosudov and Gmbb L 998)- A head-up was scored when a bird raised its head to at
least the level of its shoulders and looked either left or right. A long head-up was scored
when the head-up lasted longer than 2 sec or the bird "scanned" the room, looking both
30
right and lefi. Long head-ups w-ere scored as a percentage of regular head-ups. Founh.
we examined how long each bird spent inactive during each trial (inactivity was defined
as no flight or foraging activity for more than 2 min; however, the bird may have k e n
preening or lookuig around the room). FinaIly. the trial was divided into nine 5-min
segments and the distribution ofcaches. number ofseeds eaten. distance flown and head-
ups over these segments were calculated.
2-2.4 Analvsis
A three-way repeated measures ANOVA was used with one factor k i n g the block
(redwing 1, hawk and redwing 2). one being mount presentation (mount or baseline) and
one being days (the three successive mount or baseline days within a block). This
analysis was done for each dependent variabIe separately, with the exception of those
variables discussed below. Post hoc cornparisons were made using Tukey's HSD test.
Significance was set at the 0.05 level. Long head-ups and weight gain were percentage
variables, and so were arcsine transfomied prior to analysis (in order to nonnalize them).
Only hawk mount and baseline days were compared for the time spent in each
branch and zone and for the distribution ofbehaviours over t h e . Tukey's HSD test was
used to compare the time spent in branches and zones. The distribution of behaviours
over time were each analyzed using a two-way ANOVA, with one factor king mount
presentation (mount or baseline) and one being interval (the nine intervals per trial).
2-3 Results
The chickadees immediately responded to the presentation of the hawk mount
with vocalizations and a dramatic increase in erratic movementsl They continued to
forage normally durÏng the presentation of the redwing mount-
2-3-2 Wei&
There was a significant main effect of days on morning weight (ANOVA:
F(2,12)=L4.054, P=O.OO 1 ). with no interaction with any other factors. Weight on day 3
was significantly greater than either day 1 or day 2 (Pc 0.0 1). The days variable was
completely nested within blocks and mount presetations, so a heavier weight on day 3
indicates that the birds tended to t'rnish each part of the experiment heavier than they
began it. That implies that morning weight increased over the experiment.
Afiemoon weight was significantly lower on hawk mount days compared to hawk
baseline days (Tukey: Q(16)=3 -9 19. PcO.05) (Fig.2.1). Aftemoon weight dropped off
markedly on the first hawk mount day and showed a distinct altemation of high and low
weight on hawk mount and baseiine days respectively (Fig.2.2).
Birds gained significantly more weight on baseline days than on mount days
(ANOVA: F(1,6)=6.830. P4.04) (Fig.Z.3 ). This was particularly clear on hawk baseiine
days compared to hawk mount days (Tukey: Q(16)=1.174, P<O.OS). No difference was
found between mount and baseline days for redwing 1 or redwing 2.
Hawk
Bbck
Fieure 2.1 : Mean aftemoon body weight (2 SE) over the three expenmental blocks for experiment one. Dark bars are mount presentation days and light bars are baseline days.
Redwing 1
1 1-50
M B M
Hawk T
B M B M B
D ~ Y
Figure 2.2: Mernoon weight (+ SE) over the 18 trial days in experiment one. Each point is the mean afiemoon weight of al! seven birds on that day. Dark diamonds are mount presentation days and Light diamonds are baseline days.
Redwing 1
r
Hawk
BI&
Figure 2.3: Mean weight gain per trial (5 SE) in experiment one. Dark bars are mount presentation days and light bars are baselint days.
2.3.2 Eating
ïhere was a significant main effect of block on the number of seeds eaten per triai
(ANOVA: F(2,1 î)=S,673, P=O-O 1 8)- Post hoc tests showed that birds ate more seeds
during redwing 2 than during either redwing 1 or hawk (P<0.05). There was no
interaction with mount,
2.3-3 Cachinp
OnIy the birds in the group tested in November cached regularly and so data are
only presented for those four birds. Caching showed a significant interaction between
mount and block (ANOVA: F(2.6)=7.265. P=O.OZS) (Fig.2.4). Post hoc tests revealed
t h a ~ birds cached fewer seeds on hawk mount days than on hawk baseline days and also
cached fewer seeds on redwing I baseline days than on hawk baseline days (P<O.05 for
both).
There were no significant effects for the distance birds flew (ANOVA:
F(2,12)=0-302, NS) or for time spent inactive during each triai (ANOVA: F(2,12)=0-993,
NS).
Birds spent more time in the branch that was furchest fiom the hawk mount during
hawk mount days than during hawk baseline days (Tukey: Q(16)=3.704. P<O.OS). They
Fieure 2.4: Mean caching rate per trial (5 SE) in experiment one. Values shown include only the four birds observed in November. Dark bars are mount presentation days and light bars are baseline days.
37
also spent more time in the branch that was closest to the hawk on hawk mount days than
on hawk baseline days (Tukey: Q(17)=3.304 Pc0.05). This may be because the birds
were flying back and forth between the m-O trees. The birds also spent more time in the
tops of the branches during hawk mount days than durhg hawk baseline days (Tukey:
Q( l2)=3.17 1, P<0.05). There was no significant effect for the middle and Iower parts of
the branches-
There was no interaction beiween mount and interval for the distribution of
caches, number of seeds eaten. head-ups or distance flown over time. ui other words. the
number of caches, number of seeds eaten. head-ups or distance flown per each of the nine
5-min intervals did not differ between hawk mount and hawk baseline days. This
indicates bat there were no major differences in behavioural pattern during the 35 min
following hawk exposure on hawk mount and hawk baseline days.
2.3 -5 Vinilance
Long head-ups showed a main effect of block (ANOVA: F(2,12)=9.295,
P=0.004), with birds making a greater proportion of long head-ups during redwing 2 and
hawk than during redwing 1 (Pc0.0 1 for both). There was also a significant interaction
between block and days (ANOVA: F(4,24)=7.460, P=0.000) (Fig.2.5). Birds made more
long head-ups on Day 3 of hawk than day 2 or day 1 of hawk (P<O.O 1), more on day 2 of
hawk than day 1 of hawk (P<O.OS) and more on day 1 of redwing 2 than day 2 or day 3 of
redwing 2 (P~0.05). This indicates that the proportion of long head-ups increased during
Redwing 1 Redwing 2
B M B M B
Figure 2.5: Long head-ups (+ SE) over the 18 t d days in experiment one. Long head- ups are expressed as a percentage of regular head-ups. Each point is the mean for ail seven birds on that day.
the hawk block and decreased during the redwing 2 block.
There was a significant main effect of block for regular head-ups (ANOVA:
F(2. L Z)= 14.905, P=0.00 1 ). There was more time between head-ups during redwing 1
than during either hawk or redwing 2 (P<0.01). This suggests that vigilance increased
over the experiment.
2.4 Discussion
2.4.1 Body Weight and Foraeing
Morning weight showed no etrect of the treatments. which is expected because the
birds were weighed immediately following rach trial. It is unlikely that a chickadee could
significantly adjust its weight in the 35 min that immediately followed mount
presentation. The effect of days is restricted to the slight tendency to increase weight
over the course of the experiment-
Aftemoon weight and weight gain were lower on hawk mount days and higher on
the following baseline day. This suggests that the chickadees maintained a lower weight
while a hawk was in the area and then maintained a higher weight on the following day.
perhaps to compensate for the drop in weight on the previous day.
The number of seeds eaten per trial increased over the course of the experiment,
although birds showed a slight. but not significant. tendency to eat fewer seeds during the
trials on hawk mount days than on hawk b a d i n e days.
Birds also cached fewr seeds on haw-k mount days than on hawk baseline days.
Caching was highest on hawk baseline days and tended to drop off during redwing 2.
2-42 Channe in Activitv
Chickadees did not change the distribution oftheir activity over the vial or their
overall activity levels on hawk mount days. This suggests that the reduction in caching
was not merely a side effect of a change in activity.
There were some changes in where birds spent their t h e after seeing the hawk-
Birds spent more time in the two branches that were the Furthest and the closest. to the
hawk on hawk mount days. The chickadees may have been alternately avoiding the hawk
and inspecting it-
2-43 Vigilance
Both regular and long head-ups increased d e r the hawk exposure and remained
high for the rest of the experirnent. The proportion of long head-ups increased over the
three hawk days and declined slowly during redwing 2. These two measures of vigilance
indicate that not only did the birds look up more ofien while handling a seed, but they
also made a greater proportion of long looks.
41
Birds spent significantly more time in the top third of the branches on hawk
mount days than on hawk baseline days. This suggests that the birds were k i n g more
vigilant on hawk mount days-perching in the top of the branch may d l o w a more
unobsuucted view, although it would likely also make the bird more visibie to a predator.
3-44 Conciusions
Overail, on the day they saw the hawk. chickadees decreased cachuig. weight gain
and afternoon weight and increased vigilance. The drop in body weight would
presumably increase flight ability and make the bird more likely to escape attack. On the
following day. it appears that the chickadees increased caching, weight gain and
afiemoon weight The drop in body rveight on the previous day may have led to a
perceived increase in starvation risk. Body weight therefore retumed to (or above)
normal levels. The increase in caching may protect the bird against tiiture interruptions in
feeding caused by predator exposure. Consequently. it would appear that on hawk mount
days behaviour minimized predation risk and on hawk baseline days minimized starvation
risk.
The results aIso showed that chickadees regulate both extemal cache reserves and
intemal fat reserves in a similar manner. Both dropped on hawk rnount days and
increased on hawk baseline days.
It is important to note that these resuits are seen after the birds s aw the hawk for
42
only 1 min. Body weight changes are. presumably. the result ofa change in eating andor
rnetabolism over the remainder of the day when birds were in their home cages with ad
libitum food. This suggests that even a brief hawk erposure may have fairly long term
effects on chickadee behaviour-
in fact hawk exposure may have had carry over effects that lasted into the
redwing 2 block. Behaviour appeared to be altered during redwing 2 compared to
redwing 1. Vigilance remained high throughout redwing 2 and body weight. eating and
caching showed a tendency to be higher during redwing 2 than redwing 1. It suggests that
once the birds had encountered a hawk in the are* they made long-term adjustments to
their behaviour.
2.4.5 Other Explanations
The expenment lasted 18 days and consequently habituation to the aviary rnay
have been responsible for the differences between redwing 1 and 2. A general increase in
weight or caching cannot, however. account for the marked differences between hawk
mount and baseline days. Moreover. the chickadees do not appear to have habituated to
the hawk. Indeed, long head-ups increased over the three hawk exposures. indicating that
the birds were becoming more. not less. vigilant.
We decided to food deprive the chickadees ovemight in order to promote caching
and eating dunng the trial. Food deprivation is. however, a potential confound. The
43
birds Likely perceived a starvation nsk. which would have acted to increase their weight
(Pravosudov and Gnibb 1997). Weight tended to increase over the experiment.
Nevertheless. weight clearly decreased on hawk mount days.
Our daily handling of the birds may have been perceived as a predation threat in
and of itself (Lilliendahl 1997). The capturing and handling of wild birds is known to
increase corticosterone levels (Wingfield et ai. 1992); however. nothing is known about
how quickly captive birds habituate to being handled. It is therefore possible that the
hawk presentation was perceived as an additional predation threat.
We did not alter the temperature in the lab and so the birds were brought from a
colder environrnent into a warmer environment- There is some debate about whether
temperature is a proximate cue for weight changes (Witter and Cuthill 1993). Some
studies have found that birds maintained higher fat reserves when temperature was
decreased in the lab, while other studies found no effect of temperature on fat reserves
(Witter and Cuthill 1993). [t seems likely that if the birds had reacted to the change in
temperature. they would have maintained lower fat reserves. Weight tended to increase
over the experiment, which suggests that temperature was not a major influence.
This experiment found evidence for short-term adjustments in body weight
following hawk exposure. A ditTerent type ofexperiment would be required to determine
whether any long-term adjustments in body weight result from hawk exposure.
2-4.6 Sienificance of Results
This experïment clearly found an effect of hawk exposure on chickadee body
weight and caching Chickadees ap&r to keep their weight low on the day they see a
hawk and to increase their weight on the next day. Predation and starvation nsk,
therefore. appear to aiternate with each other as the major determinants of behaviour.
Body mass may influence predation risk by either decreasing flight ability or by
increasing foraging time. Either (or both) factor(s) may be at play in this experiment.
although the fact that caching was reduced does suggest that at least foraging time was
being reduced. [t is dificult to Say whether the observed drap in weight would be
suficient to dismpt flight ability. Kullberg et al. (1996) found that. under a predation
threat. only fairly large changes in the body weight of blackcaps (Sylvia atricapik) had
an impact on flight ability- They found a significant impairment of take-off ability when
fat load was greater than 40% of fat fiee body mass. It is dificuit to compare this value
to the chickadee data, but typically fat loads of over 50% of fat fiee body mass are only
seen in migratory birds crossing wide barries. such as the Sahara (Bairlein 1991).
The results of this study appear to support the prevailing theory that birds should
decrease their body weight in the presence oPa predator (Le. Lima 1986). Gosler et al.
( 1 995) found that great tits cany less fat during years of greater predation risk. Witter et
al. (1 994) found that birds cany more fat in the presence of protective cover and
45
Lilliendahl(l997) found that greenfinches decreased evening body weight after exposure
to a hawk mount.
These results, however. contradict the findings oFPravosudov and Gmbb (1998)
who found that tufied titmice increasrd their body weight f i e r seeing a hawk. This
discrepancy may be explained by differences in experimental design. Pravosudov and
Gmbb employed a more naturaiistic set-up, housing birds individuaiiy in an outdoor
aviary and presenting the mount at van-ous intervals throughout the day. They did not
food depnve their birds, atthough this should actuaily have Iowered the risk of starvation.
Moreover, the titrnice saw the hawk mount for a total of 16 min a day. with no
intervening baseline days. This may have Lead to a greater interruption of feeding and
there fore a greater starvation risk than the chickadees in our study,
Of course, the two species rnay use different escape tactics. although according to
Lima (1993) al1 parid species tvpically dive for cover- We did not provide cover in our
aviary. which may have forced the chickadees to employ a different escape mechanism.
The favoured parid strategy. illusrrated by
while the hawk is in the area- This would
the titmicé. may be to disrupt foraging and hide
make starvation nsk the major determinant of
their behaviour. On the other hand. if cover is unavailable, parids may remain active,
making predation risk and avoidinp an actual attack the major determinant of their
be haviour.
Altematively. it could be argued that the chickadees in the present experiment
were in fact increasing their body weight htfter seeing the hawk and that the increase just
did not occur until the following baseline day, The increased body weight on hawk
baseline days may have acted as a buffer which allowed birds to lower their weight on
hawk rnount days, when they actually saw the hawk. The mean of mount and baseline
days for aftemoon weight tends to be higher during hawk than during redwing 1. Ws
would suppoa the findings of Pravosudov and Gnibb (1998).
Both of these experiments were conducted in an aviary where food was readily
available, making it difficult to generalize the results to wild birds. Foraging in the wild
requires more effort than simply flying down to a food dish £311 of seeds, and perhaps a
greater sacrifice of vigilance. The reduction in caching and body weight observed in this
experiment may be even more pronounced in the wild. Alternatively. perhaps the birds
could affiord to reduce foraging precisely because food was so plentiful, while in nature
they rnay not have this Iuxury,
Obviously there is much more to learn about the effect of predation nsk on
passerines. Further studies using a more naturalistic design with unpredictabie food
access, available cover and longer hawk exposure would be helpful. Monitoring intake
will also cl&@ whether changes in body weight are mediated by changes in intake or in
metabolism. It would also be interestinp to compare food-storing species with non-storîng
species to see what effect the ability to store Food has on a bird's reaction to a predator.
2-5 Reference List
Bairlein, F. 1991. Body mass ot'garden warblers Svlvia borin on migration: a review of
field data, Vo~elwarte- 36.48-6 1.
B lem, C.R. 1990. Avian energy storage. Current Ornitholow. 7.59-1 13.
Gosler, A.G., Greenwood. J.J.D, & Pemins. C. 1995. Predation risk and the cost of king
fat. Nature, 377.621-623.
Grubb. TC. Jr. & Pravosudov. V.V. 1994. Toward a generai theory of energy
management in wintering birds. Journal of Avian Biolow, 25,255-160.
Hurly. T.A. 1992. Energetic reserves of marsh tits (Partrs pulustris): food and fat storage
in response to variable food supply. Behavioral Ecoloev. 3. 18 1-1 88.
King, J.R. 1972. Adaptive periodic fat storage by birds. Proceedines of the 1 Sh
International Ornithologv Conmess. pp. 200-2 17.
Kuliberg, C.. Fransson. T. & kkobsson. S. 1996. lmpaired predator evasion in fat
blackcaps (Sylvia atricapiZZn). Proceedings of the Roval Societv of London,
Lilliendahl. K. 1997. The effect of predator presence on body mass in captive
greenfinches- Animal Behaviour, 53,758 1,
Lima S.L. 1986. Predation risk and unpredictable feeding conditions: detemiinants of
body mass in birds. Ecolow. 67.3 77-3 85.
Lima, S.L. 1993. Ecological and evolutionq perspectives on escape fiom predatory
attack: a survey of north arnerican birds. The Wilson Bulletin, 105, 147.
McNamara LM. 1990. The starvation-predation trade-off and some behavioral and
ecological consequences. In: Behu~*ic)ral Mechanisms of Food Selection (Ed. By
R.N. Hughes), pp.39-58. Berlin: Springer-Verlag.
McNamara, J.M. & Houston, A.[. 1990, The value of fat reserves and the trade-off
be tween starvation and predation. -4 LW Biotheoretica. 3 8.3 7-6 1.
Metcalfe, N.B. & Ure. S.E. 1995. Diumal variation in Bight performance and hence
potential predation risk in srnaIl birds- Proc. R. Soc. Lond, B, 26 1.395400.
Pravosudov, V.V. & Grubb. T.C.. Sr. 1998. Management of fat reserves in tufied titmice
19
BueIophus bicoLor in relation to rÏsk of predation. Animai Behavior, 56.49-54.
Wingfield, J-C.. teck, C.M. & Moore. M.C. 1992. Seasonal changes of the
adrenocorticai response to stress in birds o f the Sonoran desert. Journal of
Exmimental Bioloev, 264.4 1 9-428-
Witter, M.S. & Cuthill, K. 19%. The ecological costs of avian fat storage- Phil. Trans.
R- Soc. London B, 340,73-92-
Witter, M.S., Cuthiil, 1-C. & Bonser, R.H.C. 1994- Experimentai investigations of mass-
dependent predation risk in the European Starling, Sts(rnus vdgaris. Animal
Behaviour, 48,20 1-32
Chapter 3
Conclusions and Perspectives
3.1 Conclusions and Pers~ectives
3.1 -1 Sumrnarv of Results
The data presented in this thesis extend our understanding of how predation risk
cari affect the body weight and behaviour o€smaLl birds. We found that black-capped
chickadees lowered their body weight and caching under a perceived predation nsk. This
supports the prediction that there is a trade-off between starvation risk and predation risk
(Lima 1986). It also suggests that chickadees reguiate fat and cache reserves in a similar
marner.
3- 1 -2 Altemate Anti-Predator Behaviours
Wild birds exhibit a wide variety of anti-predator behaviours. which means that
th& anti-predator strategy is likdy to be very plastic according to the situation.
Therefore, a bird with a high predation risk, may alter its behaviour to lower that risk. A
heavy bird, for example, rnay stay closer to cover than lighter birds and thereby equalize
its nsk of predation (Witter and Cuthill 1993).
Consequently, as Witter et al. ( 1994) point out, it is difficult to evaluate the
predation risk associated with a particular factor. ifone factor, such as weight, acts to
increase predation risk, the bird may adjust another factor, such as proximity to cover, to
compensate and lower predation risk. ThereFore, even though chickadees lowered their
body weight in this experiment. it does not necessarily mean that they will always do so
in the wild or that a heavy chickadee is necessdy at more risk than a Lighter chickadee.
3.1 -3 A~~hcabiIitv for Other S~ec ies
Different species typically have different fat levels depending on the niche they
occupy (Lilliendahl 1 997). Ground- feeding birds, for example. are typicdly fatter than
tree- feeding birds (Rogers 1 987). Predator avoidance tactics also differ between habitats
(Lima 1993) and so the cost of being fat is likely very different for different species
(LiIliendahl 1997)- ïherefore. different species would likely react very differently to this
experimental manipulation,
3.1.4 Future Work
Obviously, much more work is needed to completely understand the effect
predation nsk has on the body mass and behaviour of small birds. A series of
experiments comparing the presence and absence of cover and cornparhg species with
different natural histories would be very valuable. It would also be interesting to
compare a predictable food supply with an unpredictable one. Eventually, field studies
will be required to relate the laboratory findings to behaviour in the wild. This is a
promising area for future work-
3-2 Reference List
Lilliendahl. K. 1997. The effect of predator presence on body mass in captive
greenfuches. Animal Behaviour. 53.75-8 1 .
Lima, S.L. 1986. Predation risk and unpredictable feeding conditions: deteminants of
body mass in birds. Ecolow, 67.377-385-
Lima, S.L. 1993. Ecological and evolutionaiy perspectives on escape from predatory
attack: a survey of North Arnerican birds. The Wilson Bulletin, 105, 147.
Pravosudov, V.V. & Grubb, TC. Jr. 1998. management of fat reserves in tufied titrnice
Baelophu biocolor in relation to risk ofpredation. Animal Behavior, 56,49-54.
Rogers, C.M. 1987. Predation rïsk and fasting capacity: do wintering birds maintain
optimal bodymass? Ecolow, 68. 1051-1061-
Witter, M.S. & Cuthill. LC. 1993. The ecological costs of avian fat storage.
Philoso~hical Transactions of the Roval Societv of London, Series B, 340,73-92.
54
Witter, M.S., Cuthill, K. & Bonser. R.H.C. 1994. Experimental investigations of mass-
dependent predation risk in the European Starling, Stumus vutgaris- Animal
Behaviow. 48.20 1-222-
Research and Teaching Activities
Teaching Assistant Department o f P s y c h o l o ~ University of Western Ontario O 1/98 - 05/99
Research Assistant Laboratory of Dr. Cindy Staicer Department of Biology Daihousie University 05/96 - 08/96
Research Assistant Laboratory of Dr. [an Meinectzhagen Department of Psychology Dalhousie University 05/95 - 08/95 and 04/94 - 08/94
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