The response of the Eagle Owl (Bubo bubo) to an outbreak of the rabbit haemorrhagic disease

The response of the Eagle Owl (Bubo bubo)to an outbreak of the rabbit haemorrhagic disease

Jose Antonio Martınez1 and Inigo Zuberogoitia2

1 Departamento de Ecologıa, Edificio Los Arcos, Universidad de Alicante, Aptdo. 99, E-03080 Spain.Email: [email protected] (for correspondence);

2 Lab. Zoologıa, Dpto. de Zoologıa y Dinamica Animal. Fac. Ciencias. Universidad del Pais Vasco,Aptdo. 644, E-48080 Bilbao, Spain. Email: [email protected]

Summary

The Eagle Owl (Bubo bubo) is a generalist predator that in Mediterranean areas feeds

mainly on Rabbits (Oryctolagus cuniculus) At the end of 1997, a local outbreak of the rab-

bit haemorrhagic disease (RHD) decimated Rabbit populations in the area of Alicante

(eastern Spain) so that Rabbit numbers in 1998 crashed to almost nil. Prior to the outbreak

we had found 19 occupied Eagle Owl territories, and the owls had been feeding mainly on

Rabbits. After the RHD epidemic, we found only six occupied territories and the owls were

still feeding mainly on Rabbits. Diet composition was very similar between the periods,

indicating that the owls did not diversify their diet in response to main prey scarcity. No

significant differences in the proportion of Rabbit in the diet were found between the peri-

ods, suggesting that the impact of predation on Rabbits may be independent of the density

of Rabbit populations (type I functional response). This response is not typically associated

with generalist predators. In the territories that were still occupied after the outbreaks, the

owls took substantial numbers of Hedgehogs (Erinaceus europaeus) and Red-legged Par-

tridges (Alectoris rufa). Rats (Rattus spp), a common alternative prey, were not taken in

the study area. Six breeding attempts were recorded before the RHD, and none after the

RHD. This leads a to believe that only the combination of Hedgehog and Red-legged Par-

tridge availability with the readier availability of sick Rabbits allowed a small population

of owls to survive in the area, but did not allowed breeding. The predator-prey system

formed by Eagle Owls and Rabbits in Mediterranean regions is more fragile than previ-

ously thought.

Keywords: diet, predation, breeding, foraging, conservation.

Zusammenfassung

Die Reaktion des Uhus (Bubo bubo) auf einen Ausbruchder hamorraghischen Krankheit bei Kaninchen (Oryctolagus cuniculus)

Der Uhu (Bubo bubo) ist ein wenig spezialisierter Greifvogel, der sich im Mittelmeerraum

hauptsachlich von Kaninchen ernahrt. Ende 1997 wurde die Kaninchenpopulation im Ge-

biet von Alicante (Ostspanien) durch einen Ausbruch der hamorrhagischen Krankheit

(RHD) so stark dezimiert, dass der Kaninchenbestand 1998 nahezu zusammengebrochen

war. Vor dem Ausbruch der Krankheit waren 19 Uhu-Reviere besetzt, und die Uhus lebten

J. Ornithol. 142, 204–211 (2001)ª Deutsche Ornithologen-Gesellschaft/Blackwell Wissenschaftsverlag, BerlinISSN 0021-8375

U.S. Copyright Clearance Center Code Statement: 0021-8375/2001/14202–0204 $ 15.00/0

hauptsachlich von Kaninchen. Nach dem RHD-Ausbruch zahlten wir nur noch sechs be-

setzte Reviere; die Uhus ernahrten sich aber immer noch hauptsachlich von Kaninchen.

Die Zusammensetzung der Nahrung war in beiden Perioden sehr ahnlich, was darauf hin-

weist, dass Uhus ihr Beutespektrum nicht erweitern, wenn ihr hauptsachliches Beutetier

knapp wird. Dies legt nahe, dass die Anzahl geschlagener Kaninchen unabhangig von de-

ren Populationsdichte ist (Typ I funktionelle Reaktion). Diese Reaktion ist untypisch fur

nicht spezialisierte Greifvogel. In den Revieren, die nach dem Ausbruch der Seuche noch

bewohnt waren, fraßen die Uhus eine betrachtliche Anzahl Igel (Erinaceus europaeus)

und Rebhuhner (Alectoris rufa). Auf gewohnliche alternative Beutetiere wie Ratten (Rat-

tus spp) wurde im untersuchten Gebiet nicht zuruckgegriffen. Sechs Brutversuche waren

vor dem RHD-Ausbruch verzeichnet worden, danach kein einziger. Demzufolge lasst sich

vermuten, dass nur der vereinte Effekt eines Igel- und Rebhuhnvorrats und daruber hinaus

ein großeres Vorhandenseins kranker Kaninchen einer kleinen Anzahl der Uhus das Uber-

leben in dem Gebiet ermoglichte, das Bruten jedoch nicht zuließ. Das im Mittelmeergebiet

aus Uhu und Kaninchen bestehende Raubtier-Opfer-System ist anfalliger als bisher ange-

nommen wurde.

Introduction

In a given area, changes in prey density can in-

duce variations in predator numbers (the nu-

merical response) and changes in the number

of prey killed per predator (the functional re-

sponse; Hollings 1959). The extent of the total

response is expected to vary between general-

ist and specialist predators. For example, num-

bers of a specialist predator, such as the Short-

eared Owl (Asio flammeus) feeding largely on

voles (Microtus spp.), show dramatic between-

year fluctuations that follow changes in vole

populations (Cramp 1985), while generalist

species often switch to other prey if their staple

food species declines (Ratcliffe 1993). Short-

age of prey may also induce low reproductive

output (Newton 1979, Taylor 1994, Zuberogoi-

tia 2000), or lead individuals to move to alter-

native breeding areas (Galushin 1974, Hamer-

strom 1979, Smith et al. 1981, Korpimaki &

Hongell 1986, Korpimaki et al. 1987, Korpi-

maki & Norrdall 1991, see also Newton 1993,

Newton 1998), or to remain in their nesting

territories without attempting to breed (Village

1981).

The Eagle Owl (Bubo bubo) is considered to

be a generalist predator because it can feed on

a wide prey spectrum (Mikkola 1983). In Med-

iterranean areas, however, the owl depends

heavily on Rabbits (Oryctolagus cuniculus)

(see Serrano 1998), perhaps partly because of

the high food value of this animal and partly

because of the absence of other prey of similar

size (Hiraldo et al. 1976, Jacksic & Marti

1984, Donazar et al. 1989). Accordingly, it has

been suggested that Rabbit density may influ-

ence the proportion of Eagle Owl pairs that ini-

tiate breeding attempts (Donazar 1990).

In late 1997, a sudden crash in Rabbit num-

bers occurred in a large part of the province of

Alicante (SE Spain). The decline was due to a

local outbreak of the viral hemorrhagic disease

(RHD) of the Rabbit, and it was first noticed

when Rabbit hunting bags crashed abruptly to

almost nil (Bermejo 2000). Consequently,

Rabbit hunting was called to a halt during

1998 and 1999 in the study area (Bermejo

2000). In other situations hunting bags have

proved a good index of prey availability for

the Eagle Owl (Donazar 1986) and for other

raptors (Newton 1979, Redpath & Thirgood

1997). The outbreak of this human-induced

epizootic disease provided us with a new, un-

expected scenario that enabled us to gain fur-

ther insight into predator-prey relationships. It

might have been expected that under shortage

of main prey, a generalist predator would show

J. A. Martınez & I. Zuberogoitia · Eagle Owls and rabbit haemorrhagic disease 205

a faint total response to Rabbit decline because

it could switch to alternative prey, remain on

territory and attempt breeding (Hollings 1959,

Crawley 1992, Redpath & Thirgood 1997).

The aims of this study were: (1) to examine

diet composition of Eagle Owls before and

after the RHD outbreak and (2) to check for

possible effects of low Rabbit density on the

number of occupied territories and on breeding

success.

Methods

The local outbreak of the RHD occurred in an area

of 500 km2 of somewhat rugged terrain, with alti-

tudes ranging from 0 to 1208 m.a.s.l. Main habitats

are scrubland and non-irrigated farmland. The cli-

mate is arid and semi-arid Mediterranean, with an-

nual rainfall below 350 mm.

Territory occupancy was established by a variety

of methods: listening for spontaneous vocalisations

of territorial males from November to May, watch-

ing for departing owls at dusk and determining the

presence of pellets and food remains. A minimum of

four visits were made to each territory to search for

signs of occupancy (Olsson 1997). In order to ascer-

tain breeding, we tried to locate occupied nests by

searching suitable cliffs and listening for the beg-

ging calls of nestlings (Olsson 1997).

The diet of Eagle Owls during the breeding sea-

son was assessed by analysing pellet contents and

fresh food remains (see Watson et al. 1992, Oro &

Tella 1995, Ontiveros & Pleguezuelos 2000) col-

lected during visits to territories both before (1997)

and after the RHD outbreak (1998). We identified

and counted each prey item using the most fre-

quently found bone or feather, in order to give the

minimum number of individuals present in the sam-

ple (Olsson 1979).

Similarity of diet composition before and after

the RHD outbreak was assessed using Pianka’s

(1973) symmetrical overlap index: 0 = Spi * Sqi/

Spi2 * Sqi

2, where pi is the proportion of prey items

of category i in one data set and qi is the proportion

of food items of category i in the other data set. The

index varies from 0 (no overlap between the two da-

ta sets) to 1 (complete overlap). Above-species level

of prey identification leads to overestimates of food

overlap (Greene & Jaksic 1983), but since we used

specific level identification for prey remains in al-

most all of the cases (Table 1), this effect should be

negligible in our study.

We compared the abundance of main prey in diet

between territories that were occupied both before

and after the RHD (Wilcoxon Matched-Pairs

Signed-Ranks Test, Zar 1996). With data from 1997,

we also tested for possible differences in diet com-

position between territories that were abandoned in

1998 and those still occupied in 1998 (Mann Whit-

ney Test, Zar 1996). The null hypothesis was that

there were no differences in main prey composition

between groups of territories.

Results

Number of occupied territories

We located 19 occupied territories in 1997,

compared with only six in the same area in

1998. RHD was first detected in this area in

August 1997. We found six occupied nests in

1997, and listening for begging nestlings and

witnessing prey deliveries just before dusk al-

lowed us to locate a minimum of seven fledg-

lings, whereas no nests or nestlings were found

in 1998.

Diet composition

We obtained pellets and fresh food remains

from 11 territories before RHD appeared and

from six territories after (Table 1). Similarity

in diet composition before and after the RHD

was almost complete (O = 91.6 %), indicating

that the owls preyed on the same range of prey

in the two periods. O. cuniculus, Erinaceus

europaeus, Rattus, spp., Alectoris rufa and

Turdus spp. accounted for 65.4 % of prey

items. We therefore focused on these species

for the following analyses. In keeping with the

high similarity of diet, we could not find differ-

ences in the abundance of main prey between

the years 1997 and 1998 (Table 2). The tactic

of remaining in a territory under conditions of

Rabbit scarcity would be feasible if an alterna-

tive prey is already available there. Thus, for

1997, we tested for differences in main prey

composition between territories that became

vacant and territories that remained occupied

206 Journal fur Ornithologie 142, 2001


Table 1. Diet of the Eagle Owl during the breeding season based on the analysis of pellets and fresh foodremains, before and after the outbreak of the RHD.Tab. 1. Zusammensetzung der Nahrung (ermittelt aus Gewollen und Nahrungsresten) des Uhus wahrendder Brutzeit in den einzelnen Revieren vor und nach dem RHD-Ausbruch.

1997 (Before RHD) 1998 (After RHD)

Territory 1 2 3 4 5 6 7 8 9 10 11 1 2 3 4 5 6 Total Total %

Prey species

Mammals

Oryctolagus cuniculus 32 45 16 22 12 14 67 18 49 35 28 22 39 13 18 8 34 472 33,8

Lepus granatensis 2 7 – 4 – – 2 – – – – – – – – 1 – 16 1,1

Rattus spp. 16 11 10 9 3 2 24 7 5 8 3 19 5 16 5 8 20 171 12,3

Apodemus sylvaticus – 1 – 5 3 2 6 – – 1 – – 1 – – 3 – 22 1,6

Arvicola sapidus 1 3 – 3 3 1 – 1 6 – – 1 – – – 4 1 24 1,7

Eliomys quercinus 1 1 3 4 – – 12 1 – – – – 6 – – 1 4 33 2,4

Erinaceus europaeus 10 9 4 15 7 5 9 3 – 3 – 17 14 6 7 8 10 127 9,1

Atelerix algirus 8 2 – 8 – – 1 – – – – 9 – 1 – – 3 32 2,3

Felix spp. 1 – – 2 – – 1 – – – – 2 – – – 1 – 7 0,5

Vulpes vulpes – 1 1 – – 1 – – – 1 – – 1 – – 1 – 6 0,4

Total Mammals 71 80 34 72 28 25122 30 60 48 31 70 66 36 30 35 72 910 65,2

Aves

Tyto alba – 1 – – 1 – – – – 1 – – 1 – – – 1 5 0,4

Athene noctua 2 3 4 1 2 – – – – 2 – 3 3 1 – 2 1 24 1,7

Otus scops 1 – – – 2 – 3 – – – – – – 1 3 – – 10 0,7

Falco tinnunculus – 1 – – 2 – – 1 – – – – – 1 – 1 – 6 0,4

Corvus monedula 2 5 – – 5 – 6 4 7 9 – 1 – – 5 – 2 46 3,3

Pica Pica 2 – – 4 – – 1 6 3 2 – 1 – – 1 – – 20 1,4

Alectorix rufa 5 16 4 10 8 5 3 – – 2 9 8 8 – 12 – – 90 6,5

Columba spp. 6 2 9 10 3 5 – 3 – 2 4 – – 3 2 – – 49 3,5

Streptopelia turtur – 2 – 1 – 2 – – – – – – – – 1 – – 6 0,4

Gallinula cholorpus – 9 – – – – – – – – – – – – 1 2 – 12 0,9

Upupa epops 3 – – – 4 – 3 – – – 5 – – 3 1 2 – 21 1,5

Turdus spp. 7 15 – – 7 – 5 1 3 – 5 – 2 3 3 1 – 52 3,7

Delichon urbica – – – – – – 3 – – – 9 – – – 4 1 – 17 1,2

Hirundo spp. – – – 6 1 – – – – – 4 – 6 – – 1 – 18 1,3

Galerida cristata – – – – – – 15 – – – 1 2 5 – – – 3 26 1,9

Lullula arborea 3 – – – – 9 4 5 – – 1 – 2 2 – – – 26 1,9

Total Aves 31 54 17 32 35 21 43 20 13 18 38 15 27 14 33 10 7 428 30,7

Other prey

Lacerta lepida 1 – – 2 – – – – – – 1 – 2 – – 1 – 7 0,5

Coleoptera 2 4 – 14 – 4 – – 7 – – – 10 – – 6 3 50 3,6

Total Other Prey 3 4 – 16 – 4 – – 7 – 1 – 12 – – 7 3 57 4,1

TOTAL 105138 51120 63 50165 50 80 66 70 85105 50 63 52 82 1395

after the RHD outbreak. We found that, prior

to the outbreak, owls preyed significantly

more on Hedgehogs (Erinaceus europaeus)

and Red-legged Partridges than in territories

that became vacant (Table 3).

Discussion

The functional response

The proportion of Rabbits in the diet of the Ea-

gle Owl at low Rabbit density (after the RHD)

was less than at high density (before the RHD)

although differences were not significant be-

tween periods. This suggests that the impact of

the Eagle Owl predation on Rabbit populations

may be independent of prey density (see also

Donazar 1986), according to a type I function-

al response. This is a surprising result, for gen-

eralist raptors typically show type II responses

(Keith et al. 1977, Kenward 1986, Wilkman &

Linden 1981, Redpath & Thirgood 1997) or

type III responses (Redpath & Thirgood 1997).

In Mediterranean areas, the absence of prey of

similar food value to the Rabbit (Hiraldo et al.

1976) would account for the fact that the re-

sponse of the Eagle Owl to Rabbits resembles

that of a specialist predator.

This and many other studies on the food hab-

its of the Eagle Owl largely rely on the as-

sumption that the proportion of Rabbits in the

diet reflects the number that are killed. This is

not necessarily the case, because the number

of Rabbits taken also depends on wether the

owls breed. With no change in the proportion

in diet, the owls will need much more food in

total in a year in which they raise some chicks

than in a non-breeding year. If owls breed only

in good Rabbit years, they will then be able to

take more Rabbits to feed their young, and so

the impact of Eagle Owl predation may not

necessarily be independent of Rabbit density.

Several studies on the food habits of the Ea-

gle Owl have reported diet diversification as a

consequence of Rabbit scarcity (Hiraldo et al.

1976, Jaksic & Marti 1984, Donazar et al.

1989). However, diet composition was almost

identical between the two years in our study

area. Thus, if owls increased their food search-

ing effort to compensate for Rabbit scarcity

(for example, by increasing their foraging

area), this did not result in a more diverse diet.

Another way to achieve diet diversification

is to concentrate predation upon other prey


Table 2. Comparison of medians of frequency ofoccurrence (Wilcoxon Matched-Pairs Signed-Rankstest) between territories occupied in 1997 and 1998for the main prey species.Tab. 2. Vergleich der mitteleren Haufigkeiten derbevorzugten Beute (Wilcoxon Vorzeichen-Rang-test) in Revieren, die 1997 und 1998 besetzt waren.

prey species 1997 1998 Z 2-tailed p n

Oryctolaguscuniculus 19 20 –0.94 0.35 6

Rattus spp. 9.5 12 –0.83 0.41 6

Erinaceuseuropaeus 8 9 –0.94 0.34 6

Alectoris rufa 6.5 4 –1.57 0.11 6

Turdus spp. 3.5 1.5 –1.21 -0.22 6

Table 3. Comparison of medians of frequency ofoccurrence of prey items found in 1997 (Mann-Whitney test) between territories that became va-cant in 1998 (7 – 11) and the remaining territoriesoccupied in 1997 (1 – 6).Tab. 3. Mediane Haufigkeit bevorzugter Beute inRevieren, die 1997 und 1998 (Reviere Nr. 1–6)bzw. nur 1997 besetzt waren (Reviere Nr. 7–11)(Mann-Whitney-Test).

1997

1–6 7–11 U 2-tailed p n

Oryctolaguscuniculus 19 35 6 0.10 11

Rattus spp. 9.5 7 13.5 0.78 11

Erinaceuseuropaeus 8 3 3.5 0.03 11

Alectorix rufa 6.5 2 4 0.04 11

Turdus spp. 3.5 3 13.5 0.77 11

within the available spectrum. Although the

size of rodents is below that of Rabbits (Hiral-

do et al. 1976), rats are still good alternative

prey for the Eagle Owl (Olsson 1979, Perez-

Mellado 1980, Cugnasse 1983, Real, et al.

1985, Bayle et al. 1987, Donazar 1986, Serra-

no 1998), and pairs feeding mainly on rats are

able to breed successfully (Thiollay, 1969,

Olsson 1979, Lesne & Thevenot 1981). In

Spain, however, Donazar (1987) documented

an inverse correlation between the frequency

of Rabbits and rats in the diet of the owls. Rats

are abundant in watercourses, rubbish dumps

and in heavy anthropogenic environments

(Real et al. 1985, Gosalbez & Noguera 1987),

and such land uses were scarce in our study

area. This would explain why the number of

rats did not increase after the RHD (Table 2).

Another large predator breeding in the study

area, the Bonelli’s Eagle (Hieraaetus fascia-

tus), increased the proportion of pigeons (Co-

lumba spp.) in its diet after the first outbreak of

the RHD in Alicante in 1988 (Rico 1991), but

the Eagle Owl showed no such response with

respect to pigeons even though the density of

pigeons was high (breeding racing pigeons is

common practice in the study area). Owing to

the owls’ high wing load compared to that of

eagles, it may not be energetically profitable

for Eagle Owls to switch hunting to agile, fast

birds such as pigeons.

The Eagle Owl can prey on other birds of

prey (Mikkola 1983). In Spain, there is con-

cern that Eagle Owls may switch to hunting

raptors under conditions of Rabbit scarcity.

Our study does not support this idea. Diurnal

raptors and other owls are abundant in the

study area, but the percentage of birds of prey

and owls in the diet of the Eagle Owl was very

low at high Rabbit density and did not increase

when the Rabbit population crashed (Table 1).

The diet of Eagle Owls that remained in

their territories in 1998 contained larger num-

bers of hedgehogs and Red-legged Partridges

in 1997 than that of owls that deserted their ter-

ritories (Table 3). We conclude that Hedgehogs

and Red-legged Partridges were the main alter-

native prey for Eagle Owls in the study area,

and this made it possible for six pairs of owls

to remain in their territories. This result is in

alignment with other studies that have reported

hedgehogs as important in the diet of the Eagle

Owl (Bezzel et al. 1976, Blondel & Badan

1976, Orsini 1985).

The numerical response

The number of occupied territories in our

study area decreased from 19 in 1997 to 6 in

1998, coinciding with the RHD outbreak de-

tected in August 1997. Since we could not find

any signs of Eagle Owls (vocalisations, pellets,

feathers, droppings, sightings, nests) in 13 ter-

ritories in 1998, we assumed that those territo-

ries had been deserted. It is also possible that

owls died, perhaps through starvation. There

are two alternative tactics to desertion when

prey is scarce. Raptors can stay in their territo-

ries without attempting to breed (Village

1981), or they can behave as “floaters” and be-

come less detectable than territorial owls

(Smith & Arcese 1989, Rohner 1997). Since

owls most likely deserted their territories, or

died, we suggest that the effect of RHD on

Rabbit numbers must have been rather severe.

This, alongside the scarcity of profitable alter-

native prey in these areas (as suggested by low

numbers of hedgehogs and red-legged par-

tridges in the diet prior to the RHD) would in-

evitably force Eagle Owls to desert territories.

The combined effect of a higher availability of

sick Rabbits compared to healthy individuals

(Villafuerte et al. 1996) and the presence of al-

ternative prey evidently allowed some owls to

stay in their territories at low Rabbit density.

However, none of the resident owls bred in

1998, while at high Rabbit densities in the pre-

vious year a minimum of six pairs successfully

raised nestlings to the fledgling stage.

In conclusion, an outbreak of the viral hae-

morrhagic disease of Rabbits in Alicante

caused severe effects on a small Eagle Owl

population by reducing the number of occu-

pied territories from 19 to six over winter, and


preventing the production of young. The effect

of the disease was all the more severe since in

13 territories owls could not find enough prof-

itable alternative prey. Only predation on

Hedgehogs and Red-legged Partridges plus the

higher availability of diseased Rabbits seemed

to compensate for the scarcity of main prey,

thus allowing for residency at low Rabbit den-

sity. Further research is needed to elucidate the

actual shape of the total response of the Eagle

Owl to changing prey densities.

AcknowledgementsWe are most indebted to Michael A. Della Penna for his

help in identifying prey items. Fernando Falco and Alejan-

dro Izquierdo helped in the location of the territories. Ger-

man Lopez provided with helpful comments during the

early stages of the project. Ian Newton reviewed the manu-

script and provided most valuable comments. Conversa-

tions with Jose Enrique Martınez and reviews of his manu-

script on the relationships between Rabbit RHD and eagle

owls inspired and promoted our research. To him we are

most grateful.

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Accepted: 27 December 2000


The response of the Eagle Owl (Bubo bubo) to an outbreak of the rabbit haemorrhagic disease

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Transcript of The response of the Eagle Owl (Bubo bubo) to an outbreak of the rabbit haemorrhagic disease