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Intraspecific nest parasitism in bar-headed geese, Anser indicus
Anim. Behav., 1991, 41, 677-688
lntraspeeifie nest parasitism in bar-headed geese, Anser indicus CHRISTINE WEIGMANN & JURG LAMPRECHT* Max-Planck-lnstitut fiir Verhaltensphysiologie, Seewiesen, D-8130 Starnberg, Germany (Received 27 December 1989; initial acceptance 15 March 1990; final acceptance 15 September 1990; MS. number: 3507)
Abstract. Egg dumping among 54 individually marked, known-age female bar-headed geese in a semicaptive flock was studied. All-day observation of 40 nests combined with several nest inspections per day showed various behavioural differences between parasitic and non-parasitic birds. Parasites avoided nests with incubating females, and distributed their eggs over several nests. High-ranking females were more often parasitized than low-ranking females. Hatching success of parasites' eggs was 5-6%, and of nest owners' eggs 67% in non-parasitized nests and 29% in parasitized nests. Nest owners reduced the rate of parasitism by nest defence, by not incubating the majority of eggs already present when they first occupied the nest, and by not retrieving eggs from outside the nest bowl. Owners did not parasitize. Two types of parasites were found: (1) 2-year-old females (paired) which did not attempt to breed, and (2) older lowranking females ready to breed when they could obtain a nest site.
In many animal species with parental care the fathers may rear young that are not their own. Among geese and a variety of other birds the females too cannot be certain of their parenthood because some of them may save the costs of parental care by laying their eggs in the nests of conspecifics. Such egg dumping or intraspecific nest parasitism occurs in many egg-laying species from insects to birds, especially in the Anseriformes (see reviews by Yom-Tov 1980; Andersson 1984; Eadie et al. 1988; Rohwer & Freeman 1989). Eadie et al. (1988) prefer the neutral term brood amalgamation, as the word 'parasitism' implies an advantage for the dumper and a disadvantage for the host, and for the majority of species this has not been verified. We adhere to the usual terminology, however, because our results indicate that the term parasitism is adequate in this case. As the eggs of hosts and parasites are very similar, intraspecific brood parasitism is not easy to detect. Observations of known females (e.g. Clawson et al. 1979; Syroechovsky 1979; Heusmann et al. 1980), the analysis of egg proteins (Manwell & Baker 1975) and the use of genetic markers (Cooke & Mirsky 1972; Redfield 1973; Lank et al. 1989a, b) and D N A markers (Quinn et al. 1987) have yielded reliable proof of parasitism for some species. However, the majority of studies are based on indirect evidence *To whom reprint requests should be addressed. 0003-3472/91/040677 + 12 $03.00/0
such as differences in shape or colour among the eggs in a clutch, addition of more than one egg per day, appearance of new eggs after the start of incubation, or the occurrence of abnormally large clutches (see review by Yom-Tov 1980). The many hypotheses offered to explain the evolution of egg dumping have been reviewed by Yom-Tov (1980), Andersson (1984), Eadie et al. (1988) and Lank et al. (1989a). The following both assume a benefit to the parasite and a cost to the host, and make testable predictions. (1) A low-return but 'cheap' reproductive strategy of young and/or unpaired females if the costs of reproduction are especially high for young or lowranking birds. Such females would not be expected to breed themselves even if they could obtain a nest. (2) A low-return salvage tactic of females who have lost their nest or have been unable to acquire one. Such females would be expected to breed as soon as a nest became available. (3) A method to increase annual reproductive success beyond what can be achieved by just rearing one's own clutches. The observation of females who parasitize while producing normal-sized clutches in their own nests would support this hypothesis. (4) An unconditional alternative to nesting being maintained in the population through frequencydependent selection, because at some parasite/ breeding ratio the lifetime fitness gain of both types
9 1991 The Association for the Study of Animal Behaviour 677
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Animal Behaviour, 41, 4
would be equal. This hypothesis requires females either always to adopt one or the other strategy, or to use both with fixed probabilities. Andersson (1984) also suggested that the evolution of egg dumping would be facilitated by close relatedness between hosts and parasites. The testing of such hypotheses requires observations of individually known females, but only a few field studies provide such data (see also Yom-Tov 1980; Andersson 1984). In some studies the parasites were mostly young females (Weller 1959; Grenquist 1963; Lank et al. 1989b), and females that had lost their nests (Rosene 1969). In one study females of all ages dumped eggs (Clawson et al. 1979). In several studies particular females laid eggs both in alien and their own nests (Mackie & Buechner 1963; Hoogland & Sherman 1976; Clawson et al. 1979; Heusmann et al. 1980; Brown 1984). In general, the behaviour does not seem restricted to particular individuals or age classes. In contrast to the majority of other studies, we have data based on continuous observations of individuallyknown females. We tried to answer the following questions. (1) What is the extent of nest parasitism? (2) Which females lay parasitic eggs? (3) Are there other behavioural differences between parasitic and non-parasitic females? (4) Which nests and geese are parasitized? (5) Are hosts and parasites closely related? (6) Do parasites profit from dumping their eggs? (7) Does parasitism harm the hosts?
ANIMALS AND METHODS The Birds
Asian bar-headed geese winter in the lowlands of Southern Asia and breed on lakes and rivers of the highlands north of the Himalayas. They tend to nest in colonies on small islands with often less than 1 m between adjacent nests. The clutch size is usually four or five, but nests with up to 10 eggs have also been recorded. Eggs scattered between nests have been observed in dense colonies (Bailey 1910; Kydyraliew 1967; Gole 1982). In March 1988, our semi-captive flock contained 96 birds of 2 or more years (all birds of the previous year had been removed). There were 37 pairs, while five males and 17 females were unpaired. They were all individually ringed; the females were additionally marked on the head with hair dyes of different colours. They lived on the small lake (7.8 ha) at the
Max-Planck-Institut in Southern Germany with some 1000 m 2 of grazing area, the whole area being fenced in against disturbance and predation. Pellet food was available ad libitum in, and sometimes outside, a big cage with a trapdoor where birds were caught for sexing (by cloacal inspection) and ringing in autumn. Permanent food and an ice-free section of the lake kept them from leaving in winter. Since all had been ringed in their first autumn, their ages and genealogies were known. As in previous years (see Lamprecht 1986a, b), 40 nestboxes supplied with straw were placed singly or pairwise on 24 floating platforms (2.5x2-5m) anchored over part of the lake's surface area at the beginning of April. The wooden boxes (90 x 50 cm) with a narrow entrance on one of the short sides were open at the top and had walls 30 cm high. All entrances were oriented towards an observation tower on the shore, from which all occurrences in the nests could be observed. Data Collection
Rank order From 1 March 1988 until the nestboxes were supplied on 7 and 8 April 1988 we recorded agonistic interactions between identified social units (pairs or individuals) whenever possible. From these data we determined a success score for each social unit as the percentage of all observed interactions won. A success score of zero was given to all units with fewer than five observed interactions in order to prevent unrealistically high success scores. These 18 birds or pairs had avoided the proximity of others and had never won an interaction. The social units were grouped into four dominance classes, Of the 36 units with more than five interactions, class 1 comprised the 12 with the highest success scores, class 2 the next 12, and class 3 the 12 units with the lowest success scores. A class 4 was created for the 18 units with fewer than five interactions and thus a zero success score. Nest checks During the laying period (up to 18 May) we visited all nests by boat twice daily, at dawn (around 0600 hours) and dusk (around 2000 hours). Up to three additional checks during the day were made during the peak laying period (18 April-I 0 May). In each nest the eggs were counted, their positions (inside/outside nest bowl) noted and
Weigmann & Lamprecht: Nest parasitism in geese
679
new eggs labelled with numbers. The geese got used to these disturbances at the nest, and breeding birds immediately resumed incubation when the boat left. Later checks were less regular and after 23 May we mainly visited nests where the female had terminated incubation, to note which eggs had hatched.
nest by a female who was not nor ever became the owner was termed a parasitic egg. A nest containing eggs not laid by the nest owner was termed a parasitized nest. The eggs could be parasitic as defined above or laid by a previous owner of the nest, thus being also foreign to the new owner.
Nest observation
For statistical analysis non-parametric procedures (Siegel 1956; Sachs 1984) were usedl All P-values are two-tailed.
From 9 April to 18 May the tower was occupied about 13 h per day by one or two observers recording details of every visit of a female to a platform or nest. The identity of the female, the platform and/ or nest numbers, arrival and departure times, reason for departure (voluntary or forced), and the types of behaviour performed in the nest were recorded.
Definitions Paired females were those that, after 15 March, were always (except during incubation) seen together with the same gander, while unpaired females were often alone or in the vicinity of different ganders. Young females were all females known to be 2 years old. A female was called the owner of a particular nest on a certain day if the following conditions applied on this and the two following (or preceding) days. (1) More than 50% of her platform visits of the day were to the same platform. If the platform held two nestboxes, more than 50% of her nest visits were to the same nest. (2) The time she spent in this nest on this day was equal to or greater than the sum of the time spent in this nest by all other geese. Females (or pairs) fitting this definition visited one nest almost exclusively and did not visit any other nests regularly. They also defended their nests or consistently attempted to return when driven off by dominant conspecifics. Incubating females kept their eggs warm, did not leave the nest more than five times a day and defended it against other birds. They did not visit other platforms or nests. They were called breeders when incubating a clutch for more than 14 days. Those females that laid at least one egg in a nest they did not own then or later were termed parasitic. Some females were parasitic, but later incubated a clutch of their own. For some of the following calculations they were treated as parasitic, for others as breeder females. An egg laid in a
Analyses
RESULTS
The Extent of Nest Parasitism A total of 360 eggs were laid by the 54 females in the 40 ncstboxes offered, 308 in 34 nests which were then incubated for at least 14 clays (breeders' nests) and 52 in the other six nests where no bird incubated the clutch for an extended period. We could attribute 57 eggs to individual parasitic females; either laying was observed directly or only one female had visited the nest since the last check. A further 3 l eggs could be recognized as parasitic (although the laying females were unknown) according to the following criteria. (1) The new egg had been found in the morning and the nest owner also laid an egg during the same day, so the first egg was assumed to be parasitic, since geese have never been found to lay more than one within about 24 h (Wiirdinger 1973; Bezzel 1985; for chicks, Gallus gallus domesticus, Romanoff & Romanoff 1949 showed that the minimum interval between two eggs was longer than 24 h). (2) The new egg appeared in a clutch that had already been incubated for more than 2 weeks. Geese stop laying when they start incubation (W/irdinger 1973). (3) The new, unlabeUed egg was found in front of a nest where the owner had incubated for more than 3 days. None of the 84 eggs that could be attributed to nest owners was ever laid outside the nest bowl. (4) Eight eggs were laid in two nests which both remained ownerless. As such eggs are potentially taken over and incubated by another female claiming the nest, they were regarded as parasitic. Thus we could identify 88 eggs as parasitic. Additionally, in 10 instances two new eggs were found in a nest in the morning. Due to the physiological constraints mentioned above, at least one of
Animal Behaviour, 41, 4
680
Table 1. Distribution of the 98 parasitic eggs over the 40 nests Number of parasitic eggs 0 Numberofnests
1
2
3
4
5
6
7
8
10 10 4
3
4
3
3
2
1
Table II. Relationship between behaviour and type of female Behaviour
Female
Pure parasite (13) (direct evidence)
Unpaired female (7) Young paired female (5) Older paired female (1)
Pure parasite (4) (indirect evidence)
Unpaired female(1) Young paired female (3)
Parasite, then nestowner (3)
Unpaired female (I) Older paired female (2)
Non-parasitic breeder (30)
Unpaired female(8) Older paired female (22)
Parasite, then breeder (4)
Older paired female (4)
The number of females belonging to each type is given in parentheses. Young femaleswere known to be 2 years old. For other definitionssee text. them was very likely to be parasitic in each case, but we could not tell which. In total, at least 98 (27-2%) of the 360 eggs were parasitic. From one to eight parasites" eggs were found in 30 of the 40 nests (Table I). Of the 34 breeders' nests, 25 (73.5%) were parasitized; of the six nonincubated nests, five (83.3%) contained one or more parasitic eggs. Identity of Parasitic Females The majority of parasitic females were identified because we could attribute to them at least one parasite egg (direct evidence). In four females we only noted their extended belly which indicated the presence of fully developed eggs. As no eggs were found outside nests, these females must have laid their eggs in nests of others (indirect evidence, Table II).
Thirty of the 34 breeders were never observed to dump eggs (Table II). With one exception (see below) females were never observed to dump eggs on others while they were owners of a nest. Among females that had dumped eggs at some time there were fewer nest owners than among nonparasites (Table III). Parasitic females were more often low in rank, more often young, i.e. 2 years old, but not more often unpaired (Table III). Fewer parasitic than non-parasitic females had experienced earlier breeding attempts and breeding successes (Table III). However, if young parasitic females under 4 years old are excluded, eight of the remaining 12 had bred in previous years. The parasitic females did not seem to be a unitary group. There were seven females that first parasitized, but later owned a nest or even became a breeder (Table II). They laid their first egg earlier in the season than the 13 females observed to parasitize exclusively (Mann-Whitney U-test, P < 0-05). They also showed features typical of breeders (see below), in that they tended to spend more time in a nest while laying an egg, although not significantly so (P<0.06) and were significantly less often chased from a nest after laying (P < 0-002) than the 13 purely parasitic females. Compared with the 30 non-parasitic breeders they became nest owners significantly later in the season (P < 0-02). The eight young paired females, on the other hand, never owned a nest and parasitized exclusively, while of the 17 unpaired females, eight bred without being parasitic (Fisher test, P < 0"05). Only three (37.5%) of the young paired females were in the lowest rank category (category 4), as were 13 (76"5%) of the unpaired females. Although the difference was not significant (Fisher test, P < 0' 16), the paired young females tended to rank higher (not lower as might be expected) than the (older) unpaired females. Since rank correlates positively with the probability of obtaining a nest (Lamprecht 1986b), the above difference in breeding probability suggests a lower breeding propensity of young females.
Behaviour of Females Differences in the behaviour between parasites and non-parasites may indicate that parasitic females are not dumping eggs 'by mistake', but are aware of being in a nest that is not their own. In fact 56 eggs of known parasitic females were laid when
Weigmann & Lamprecht: Nest parasitism in geese
681
Table III. Parasitic (N= 20) and non-parasitic (N= 30) females classified according to different variables Variable Nest owner Previous breeding attempts Previous breeding successes Rank category Age Female type
Parasites
Non-parasites
7 13 11 9 16 4 4 16 5 15 12 8
30 0 3 27 I0 20 19 11 0 30 22 8
Yes No 0 >0 0 >0 1+ 2 3+4 2 years Older Paired Unpaired
P*
<0.001 < 0.002 <0.003 < 0.006 <0-02 >0.49
*Fisher exact probability test.
Table IV. Behavioural differences between parasitic and non-parasitic females Parasites
Breeders
Variable
N
Median
N
Median
P*
Mean no. of different platforms visited per day No. of days not visiting any platforms Mean no. of platform visits before egg laying Mean no. of nest visits before egg laying Mean no. of different platforms visited before egg laying Mean no. of different nests visited before egg laying Time spent on nest at egg laying (min) % of egg depositions with female being bitten % of leavings after laying, due to harassment Mean no. of platform visits on same day after laying Mean no. of nest visits on same day after laying Mean no. of return visits to same nest on same day after laying
16 16 20 20 20 20 20 20 20 20 20
2.22 6-5 6.6 4.25 2.85 2.6 28.25 41.5 83.5 0.0 0.0
34 34 32 32 32 32 32 32 32 32 32
1.32 0.5 5.0 4.50 1.0 1.0 183.0 0.0 0.0 2.0 2.0
<0.0001 <0.0001 <0.075 >0.7 <0.001 < 0.001 <0.001 <0.001 <0.001 <0.001 <0.001
20
0.0
32
2.0
<0.01
*Mann-Whitney U-test.
the females did n o t o w n nests. The only exception was by a female who laid her last parasitic egg o n the first day o f b e c o m i n g a nest owner. Investigating b e h a v i o u r a l aspects o f the entire laying season (9 A p r i l - 1 8 May), we c o m p a r e d the 16 females observed to be n o n - b r e e d i n g d u m p e r s with the 34 breeders (see Table II). W h e n dealing with aspects o f particular egg depositions, we used all observations of egg d u m p i n g (20 parasitic females) a n d o f laying non-parasitic eggs (32 breeder females). As tests were m a d e with the
females as units o f comparison, the d a t a on several egg depositions o f a female were averaged. C o m p a r e d with breeders, parasitic females visited m o r e different nest platforms per day a n d h a d m o r e days with n o p l a t f o r m visits at all during the entire laying season (Table IV). O n days w h e n a n egg was laid, parasitic females visited more different platforms a n d nests before laying the egg t h a n did breeders (Table IV). This was n o t because parasites laid later in the day a n d thus were observed for longer. In fact m e a n pre-
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Animal Behaviour, 41, 4
laying observation time was longer for breeders (median 9 h) than for parasites (median 4 h, U-test, P<0.001). During the laying of an egg, parasites spent less time in a nest than breeders, and were more often bitten by other geese (Table IV). They more often left the nest after laying because of harassment (usually by the nest owners). After laying an egg, a parasite rarely visited platforms or nests that same day, while breeders did so regularly (Table IV). In those situations, breeders almost exclusively revisited the same (their own) nest, but only one parasitic female once revisited the nest in which she had dumped an egg. Parasitized Nests The 98 parasitic eggs were all laid on 33 out of 37 days between 17 April and 23 May. Of these, 45.9% were laid in nests without owners (phase 1), 32.7% in nests with an owner in the laying period (phase 2), and 21.4% in nests with owners already incubating a clutch (phase 3). As the number of nests in a certain phase changed daily, we calculated the percentage of nests in the different phases for each day. This gave the expected proportions of eggs laid in nests of the different phases, supposing that parasitic females did not discriminate between nest phases. The observed proportions for each day were the percentages of parasitic eggs actually laid in nests of the three different phases. With Wilcoxon tests we investigated, for each nest phase, whether observed and expected proportions differed in any systematic way (N= 33 days, Fig. 1). Parasitic eggs were laid more often than expected into nests in phase 1 (P < 0.02) and more rarely than expected in phase 3 nests (P < 0.001). There was no significantdifference with respect to nests in phase 2 ( P > 0.22). If individual females that laid several eggs had general preferences for particular nest phases, it would be misleading to treat each egg laying as an independentevent. We therefore recalculated on the basis of the 20 females to which a total of 57 parasitic eggs could be attributed. When a female had laid several eggs the differences between expected and observed proportions for each nest phase were averaged. Wilcoxon tests gave the same results as above: parasitic females laid more often than expected in nests of phase 1 (P<0.01), there was no significant difference with respect to phase 2 nests (P>0.1), and they laid more rarely than expected in phase 3 nests ( P < 0.001).
Identity of Hosts
The number of parasitic eggs laid in a nest with an owner (phase 2 or 3) correlated positively with the dominance rank (success score) of the owner (Spearman r s = 0-493, N = 37 nests, P < 0.001). Thus high-ranking females were more often parasitized. If high-ranking females owned nests earlier than low-ranking ones, there would be more time to parasitize their nests, giving rise to the above correlation. But the date at which nest ownership started did not correlate with the number of parasitic eggs in the nest (rs = 0'038, N=37, P > 0"6), and the dominance rank of an owner did not correlate significantly with the date on which she acquired the nest (rs = 0"237, N = 37, P > 0'2). We could not decide definitely whether parasitic females selected nests of dominant females directly or tended to dump their eggs in generally attractive nests, which were mainly held by dominant females. The second possibility seems less likely because the correlation between the dominance rank of a breeder and the total number of parasitic eggs in its nest, including those eggs present when taking possession of the nest, is not significant (rs= 0-27, N = 34 nests, P>0.11). Kin Selection and Nest Parasitism
Of the 20 parasitic females, 10 had close relatives breeding in the flock (four mothers, five sisters, and one daughter). But only two females dumped one egg each in the nest of a mother and a sister. Three and five eggs could be attributed to these two parasitic females, yet they used a different nest for each egg, not apparently concentrating on nests of close relatives. During egg laying they spent only 12 and 15 min in the nests and were harassed and bitten by the mother and sister, respectively. The Benefit to Parasites
Five parasitic eggs, and one in those egg pairs where one egg or the other must have been parasitic, hatched in four different nests, giving a hatching success of 5"1% (or 6.1%) among the 98 parasitic eggs. Including these, 80 goslings hatched that year. Thus 6.25% (or 7.50%) of them were not the direct descendants of their 'mothers'. From the 84 eggs that could with certaintY be attributed to breeding females, 38 (45.2%) hatched. Thus the success rate of non-parasitic eggs appears to be about nine (or seven) times greater than that of parasitic eggs.
Weigmann & Lamprecht: Nest parasitism in geese
683
9
I00
9
*
(a)
50
I
I00
I
;
-
I
I
I
~.~.
[
~.~.
I _
-
I
9
9
{b)
to
9
9
50-
Z
IOO - -
go
9
9
Co)
9 9
50
I
15
= .
. . . . . . . . . . .
20 April
25
50
t
5
IO
15 Mey
:
1
2"0
Figure 1. Percentage of nests in different phases on each day: (a) no owner; (b) laying owner; and (c) incubating owner ( ). Corresponding percentages of parasitic eggs laid in nests of the different phases (O). The five (or six) parasitic eggs that finally hatched had all been laid in nests with owners during the laying period. The Disadvantage
to the Hosts
Of the 34 breeders' nests, 25 were parasitized and nine were not; we used all eggs laid in these nestboxes for our comparison. In many nests it was impossible to attribute each egg to a particular female. We therefore treated every egg that was not clearly parasitic according to our criteria (see
Results: Extent of Nest Parasitism) as the breeder's. One hatched egg that could have been either was regarded as the host's egg. For each nest we calculated the percentage of parasitic eggs (degree of parasitism) and the percentage hatched of the remaining (the host's) eggs (host's success rate). There was a significant negative correlation between degree of parasitism and the host's success rate (Fig. 2). The host's median success rate was 67% in nonparasitized nests and 29% in parasitized nests (U-test, P<0.05). While some eggs hatched in all
Animal Behaviour, 41, 4
684
,~176 I o
9
50 T
0
50
I00
% Parasitic eggs in nest
Figure 2. Relationship between the percentage of parasitic eggs in the clutch and the percentage of host eggs hatched (N = 34 breeders' nests): r s = - 0' 59, P < 0-001. Regression: Y= - 0.94X+ 68.
Table V. Ejection of eggs from the nest bowl by owners of nests that did or did not contain foreign eggs Nests without any foreign eggs
Nests with foreign eggs
Nest no.
Clutch size
No. of eggs later found outside nest
Nest no.
No. of eggs taken over
No. of these later found outside nest
1
6
2 3 4 5 6 7 8 9
5 7 5 4 5 3 5 7
0
1
3
3
0 2 2 0 0 0 0 0
2 3 4 5 6
5 6 9 8 9
3 5 6 8 6
'Foreign eggs' or 'eggs taken over' were eggs already in the nest when the female became the owner of the r~est.
non-parasitized nests, all failed nests contained some parasitic eggs. The disadvantage to the hosts was p r o b a b l y due to the enlarged size o f the clutches with parasitic
eggs. The hatching rate (%) o f all eggs in the nest showed a high negative correlation with the total n u m b e r ( r a n g e = 3 - 1 9 ) o f eggs present ( r s = - 0 . 7 1 3 , N = 3 4 , P < 0 ' 0 0 0 1 ) , and the n u m b e r o f
Weigmann & Lamprecht: Nest parasitism in geese parasitic eggs was strongly related to the total number of eggs in the nest (rs=0"943 , N = 3 4 , P<0"0001). Defensive Measures of Hosts
There are two ways in which a female may be induced to incubate eggs she has not laid herself: (1) by becoming the owner of a nest that already contains eggs, and (2) by having eggs laid in her nest while she owns it. Six females became owners of nestboxes relatively late in the season and so obtained boxes that already contained eggs. These were not incubated by any female and were usually scattered in the straw, and no nest bowl had been built. The females then laid their own eggs and constructed a nest bowl. They never included all previous eggs into the clutch they incubated (Table V). On average only 22.5% of such alien eggs were incubated. In nests without any foreign eggs only 9"3% of the eggs were later found outside the nest bowl (Table V). Nest owners (usually assisted by their mates) often attacked other females that came close to or into their nests. Thus parasitic females were often harassed during egg laying (see above). However, many females sitting on their eggs did not move (or attack) when another female entered the nestbox to lay an egg. This was why a number of parasitic eggs were laid outside nests. No nest owner was ever observed to lay an egg outside the nest bowl. Of the 15 parasitic eggs laid beside nests (less than 50 cm from the rim) only three were later found in the nest bowl, apparently retrieved by the hosts. Incubating females of various goose species retrieve all eggs within 90 cm of the rim of the nest bowl (Poulsen 1953; Prevett & Prevett 1973). Poulsen (1953) found that species belonging to the same avian order showed almost the same tendencies for egg retrieval. Thus we expected our bar-headed geese to retrieve all eggs at such close range. However, significantly fewer eggs than expected were retrieved (KolmogorovSmirnov goodness-of-fit test, P<0"001). As four nests had two marginal eggs, only 11 females faced the decision whether or not to retrieve them. Three of them retrieved one egg each. This result differs significantly from the expectation that all females should retrieve marginal eggs (Kolmogorov-Smirnov test, P<0.001).
685
DISCUSSION The Term 'Parasitism'
It would be appropriate to call egg dumping a case of parasitism if the dumpers profited at the expense of the hosts. Indeed in our goose flock 56% of the parasite eggs hatched. This corresponds to the sittiation in wild lesser snow geese, Chen caerulescens caerulescens, where 5.3% of the goslings appeared to have hatched from parasitic eggs (Lank et al. 1989a). The gain of reproductive success through egg dumping was about seven to nine times lower than through rearing one's own clutch, but higher than if no eggs had been produced. The present study also demonstrates the reproductive costs of being parasitized. The reduction of the hosts' hatching rate through the presence of dumped eggs from 67% to 29% seems very high, yet effects of similar size have been found in starlings, Sturnus vulgaris, and goldeneye ducks, Bucephala clangula (Yom-Tov 1980). The alternative interpretation, that it was inattentive breeders that had poor success and were often parasitized is unlikely, as it was the dominant breeders that were more often parasitized, and these breed more successfully than low-ranking nest owners (Lamprecht 1986b). Such costs of being parasitized can explain the evolution of the three means of defence of nest owners against parasitic eggs: (1) chasing other geese from the nest (see also Mineau & Cooke 1979; Owen & Wells 1979); (2) not adopting eggs already present when the nest is first occupied (see also Pienkowski & Evans 1982 for the shelduck, Tadorna tadorna); and (3) inhibition of egg retrieval when nest parasitism is common (Prevett & Prevett 1973). The Extent of Parasitism
Fifty-seven per cent of owner-nests were parasitized. This is similar to the figures reported for wild birds. Among shelducks 30-50% of nests (Pienkowski & Evans 1982) and among mergansers, Mergus serrator, 64% of nests (Young & Titman 1988) were estimated to contain dumped eggs, and lesser snow geese goslings hatched from parasitic eggs were found in 22% of nests (Lank et al. 1989a). Given the low hatching rate of parasitic eggs the number of parasitized nests may have been much higher. There may be several reasons for the high rate of parasitism found in our flock.
686
Animal Behaviour, 41, 4
(1) Through detailed observations of individual birds' behaviour many eggs were identified as parasitic that would not have been recognized by cruder methods. Several authors admit that their estimates of parasitized nests were probably too low (Gibbons 1986; Lank et al. 1989a). (2) Competition for nest sites may have been exceptionally high. But a field report of bar-headed geese by Sch/ifer (1938) indicates that nest sites are also rare and contested in the wild. (3) As young females are especially likely to parasitize, a high proportion in the flock could explain a high parasitism rate. Yet in our flock the proportion of 2-year-old females was only slightly higher (14.8%) than in the snow goose population (12.1%) studied by Lank et al. (1989b).
Behaviour of Parasitic Females Many of the behavioural differences between parasitic and breeder females might be explained by the different conditions met at a nest site. Territorial aggression of nest owners may have caused parasites to visit several nests, spend less time on a nest at egg laying, and terminate egg laying when harassed. But we often observed the same behavioural features in parasitic females when nest owners were absent or non-existent. This and the following differences from nest owners indicate that a parasitic female is aware of the fact that she is not laying in a nest of her own. (1) She rarely visits nests on non-laying days. (2) She shows no tendency to visit the same nest repeatedly, even when no harassment took place. (3) She rarely visits nests after having laid an egg, and (4) if she does, it is not the nest where she laid. Apparently a parasitic female shows a pronounced interest in nests onlywhen she needs one for depositing an egg. Her tendency to choose a different nest for each egg ('scattered laying', el. wood duck: Heusmann et al. 1980) may be adaptive, because it slows the increase of clutch size and consequent decline of the hatching rate (see discussion by Andersson 1984).
Identity of Parasitic Females Parasitic females were those who did not own a nest at the time of laying, and some never owned a nest. Yet in spite of this common feature, the parasites comprised at least two different kinds of females. (1) The eight young (2-year-old) females that were paired but apparently did not try to claim a
nest. One 'older' paired female that was also purely parasitic (Table II) was only 3 years old. (2) The older, unpaired or paired females that later in the season became breeders or at least nest owners. Even when dumping eggs, these seven females differed from the other parasites and behaved similarly to breeder females. They gave the impression of trying to establish a nest of their own, but were unable t~ hold it against competitors, The eight unpaired parasites, all of them older than 2 years, may have belonged to either group.
Parasitized Nests Parasitic females preferred to lay in ownerless nests and avoided laying in nests with an incubating female. They probably preferred nests with a lower possibility of being attacked, since parasites tended to suffer fewer attacks at nests without owners than at nests defended by a female or pair, although not significantly so (Wilcoxon matched-pairs signedranks test, P<0"06). Lank et al. (1989b) observed that parasitic snow goose females tended to lay in nests with the ownerspresent, yet admitted that their sample of six observations may have been biased; as the majority of their birds were unmarked, they were able to tell owners from parasites only when agonistic interactions occurred. The presence of nest-like structures (boxes with straw) with no owners may have been an artefact in our setup. If they did not occur in nature, parasites would only find nests that belonged to the females that built them. In this case, and if parasitic geese adhered to the rule of laying in nests where they were not attacked immediately, eggs would most often be dumped in laying phase nests, as laying geese are not continuously present at the nest. Parasitic females preferred the nests of dominant owners. This would be advantageous, as highranking pairs usually have higher hatching and fledging success than low-ranking pairs (Lamprecht 1986b). High-ranking birds were more often parasitized and thus suffered higher costs than low-ranking birds. But among the 54 females, dominance (i.e. the success score) still correlated positively with the number of eggs hatched (rs = 0-42, P < 0.003). The costs of being parasitized do not seem to be reduced much through kin selection. Only two females dumped an egg with close relatives, although half of the parasitic females had closely related nest owners in the flock.
Weigmann & Lamprecht: Nest parasitism in geese
Conclusions The behavioural observations suggest that female geese do not dump eggs into other nests 'by mistake', but are aware that the nest is not their own. Egg dumping seems to be adaptive, probably serving different functions in different individuals. (1) It seems to be a 'salvage strategy' (Lank et al. 1989a) of females older than 2 years prevented from breeding by competition for nest sites. They stop dumping eggs as soon as they get an opportunity to breed. (2) It also appears to be part of a conditional lifehistory strategy: females tend to dump eggs when young and breed when older than 2 years. Grice & Jones (1965, cited in Heusmann et al. 1980) suggested that young female wood ducks first passed through a parasitic stage. This seems also to apply to bar-headed geese. As geese are long-lived it may be advantageous to refrain from costly breeding when young, inexperienced and low-ranking, if this increases future reproductive output and/or survival. But why should young females produce eggs at all? F r o m observations in previous years we know that 2-year-old females are physiologically able to breed. One actually fledged young. If breeding costs depended on prevailing conditions that were unpredictable before arrival on the breeding grounds, even a young female should be prepared to breed if conditions turned out to be favourable. If not, there is still the alternative of dumping the eggs in the nests of others, though reproductive success will be low. Since females did not parasitize when they had nests of their own, egg dumping does not seem to be used in addition to own breeding, as it is in some swallows (Brown 1984; Moiler 1987) and sparrows (Kendra et al. 1988). M o s t parasitic females had bred in previous years or bred later. Thus fixed specialists for either nesting or parasitizing do not seem to occur, and in most females egg dumping appeared contingent upon the lack of a defensible nesting site.
ACKNOWLEDGMENTS We thank J. Schneider, A. Meilinger, T. Friedl and H. Buhrow for their unfaltering help during data collection, J. M. Black, J. Schneider and W. Wickler for helpful comments on the manuscript, B. Knauer for drawing the figures and P. Rechten for help in correcting the English.
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REFERENCES Andersson, M. 1984. Brood parasitism within species. In: Producers and Scroungers (Ed. by C. J. Barnard), pp. 195-228. London: Chapman & Hall. Bailey, F. M. 1910. The nesting of the bar-headed goose (Anser indicus) in Tibet. J. Bombay nat. Hist. Soc., 19, 366-369. Bezzel, E. 1985. Kompendium der V6gel Mitteleuropas: Nonpasseriformes. Wiesbaden: Aula-Verlag. Brown, C. R. 1984. Laying eggs in a neighbor's nest: benefit and cost of colonial nesting in swallows. Science, 224, 518-519. Clawson, R., Hartman, G. & Fredrickson, L. 1979. Dump nesting in a Missouri wood duck population. J. Wildl. Mgmt, 43, 347-355. Cooke, F. & Mirsky, P. J. 1972. A genetic analysis of lesser snow goose families. Auk, 89, 863-871. Eadie, J., Kehoe, F. P. & Nudds, T. D. 1988. Pre-hatch and post-hatch brood amalgamation in North American Anatidae: a review of hypotheses. Can. J. Zool., 66, 1709-1721. Gibbons, D. W. 1986. Brood parasitism and cooperative nesting in the moorhen, Gallinula chloropus. Behav. Ecol. Sociobiol., 19, 221-232. Gole, P. 1982. Status ofAnser indicus in Asia with special reference to India. Aquila, 89, 141-149. Grenquist, P. 1963. Hatching losses of common goldeneyes in the Finnish Archipelago. Proc. int. ornithol. Congr., 13, 685-689. Heusmann, H. W., Bellville, R. & Burrell, R. 1980. Further observations on dump nesting by wood ducks. J. Wildl. Mgmt, 44, 908-915. Hoogland, J. L. & Sherman, P. W. 1976. Advantages and disadvantages of bank swallow (Riparia riparia) coloniality. Ecol. Monogr., 46, 33-58. Kendra, P. E., Roth, R. R. & Tallamy, D. W. 1988. Conspecific brood parasitism in the house sparrow. Wilson Bull., 100, 80-90. Kydyraliew, J. 1967. Die Streifengans (Anser indicus) im Tienschan Gebirge (Translated from Russian). Ornithologija, 8, 245-253. Lamprecht, J. 1986a. Structure and causation of the dominance hierarchy in a flock of bar-headed geese (Anser indicus). Behaviour, 96, 28-48. Lamprecht, J. 1986b. Social dominance and reproductive success in a goose flock (Anser indicus). Behaviour, 97, 50-65. Lank, D. B., Cooch, E., Rockwell, R. F. & Cooke, F. 1989a. Environmental and demographic correlates of intraspecific nest parasitism in lesser snow geese Chen c. caerulescens. J. Anita. Ecol., 58, 29-45. Lank, D. B., Mineau, P., Rockwell, R. F. & Cooke, F. 1989b. Intraspecific nest parasitism and extra-pair copulation in lesser snow geese. Anim. Behav., 37, 74-89. Mackie, R. J. & Buechner, H. K. 1963. The reproductive.. cycle of the chukar. J. Wildl. Mgmt, 27, 246-260. Manwell, C. L. C. & Baker, M. A. 1975. Molecular genetics of avian proteins. XIII. Protein polymorphism
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in three species of Australian passerines. Austral. J. Biol. Sci., 28, 545-557. Mineau, P. & Cooke, F. 1979. Territoriality in snow geese or the protection of parenthood: Ryder's and Inglis's hypotheses re-assessed. Wildfowl, 30, 16-19. Moller, A. P. 1987. Intraspecific nest parasitism and antiparasite behaviour in swallows Hirundo rustica. AnOn. Behav., 35, 247-254. Owen, M. & Wells, R. 1979. Territorial behaviour in breeding geese: a re-examination of Ryder's hypothesis. Wildfowl, 30, 20-26. Pienkowski, M. W. & Evans, P. R. 1982. Clutch parasitism and nesting interference between shelducks at Aberlady Bay. Wildfowl, 33, 159-163. Poulsen, H. 1953. A study of incubation responses and some other behavior patterns in birds. Vidensk. Meddr dansk naturh. Foren., 115, 1-131. Prevett, J. P. & Prevett, L. S. 1973. Egg retrieval by blue geese. Auk, 90, 202-204. Quinn, T. W., Quinn, J. S., Cooke, F. & White, B. N. 1987. DNA marker analysis detects multiple maternity and paternity in single broods of the lesser snow goose. Nature, Lond., 326, 392-394. Redfield, J. A. 1973. The use of incomplete family data in the analysis of genetics and selection at the Ng locus in the blue grouse (Dendrogapus obscurus). Heredity, 31, 35-42.
Rohwer, F. C. & Freeman, S. 1989. The distribution of conspecific nest parasitism in birds. Can. J. Zool., 67, 239-253. Romanoff, A. L. & Romanoff, A. J. 1949. The Avian Egg. New York: John Wiley. Rosene, W. 1969. The Bobwhite Quail. New Brunswick: Rutgers University Press. Sachs, L. 1984. Angewandte Statistik. 6th edn. Berlin: Springer Verlag. Sch~ifer, E. 1938. Ornithologische Ergebnisse zweier Forschungsreissen nach Tibet. J. Ornithol., 86, 1-349. Siegel, S. 1956. Nonparametric Statistics for the Behavioral Sciences. New York: McGraw Hill. Syroechkovsky, E. V. 1979. The laying of eggs by white geese into strange nests (Anser c. caerulescens). Zool. Zhur., 5g, 1033 1041. Weller, M. W. 1959. Parasitic egg laying in the redhead (Aythia americana) and other North American Anatidae. Ecol. Monogr., 29, 333-365. Wfirdinger, I. 1973. Breeding of bar-headed geese (Anser indicus) in captivity. Int. Zool. Ybk, 13, 43-47. Yom-Tov, Y. 1980. Intraspecific nest parasitism in birds. Biol. Rev., 55, 93-108. Young, A. D. & Titman, R. D. 1988. Intraspecific nest parasitism in red-breasted mergansers. Can. J. Zool., 66, 2454-2458.
lntraspeeifie nest parasitism in bar-headed geese, Anser indicus CHRISTINE WEIGMANN & JURG LAMPRECHT* Max-Planck-lnstitut fiir Verhaltensphysiologie, Seewiesen, D-8130 Starnberg, Germany (Received 27 December 1989; initial acceptance 15 March 1990; final acceptance 15 September 1990; MS. number: 3507)
Abstract. Egg dumping among 54 individually marked, known-age female bar-headed geese in a semicaptive flock was studied. All-day observation of 40 nests combined with several nest inspections per day showed various behavioural differences between parasitic and non-parasitic birds. Parasites avoided nests with incubating females, and distributed their eggs over several nests. High-ranking females were more often parasitized than low-ranking females. Hatching success of parasites' eggs was 5-6%, and of nest owners' eggs 67% in non-parasitized nests and 29% in parasitized nests. Nest owners reduced the rate of parasitism by nest defence, by not incubating the majority of eggs already present when they first occupied the nest, and by not retrieving eggs from outside the nest bowl. Owners did not parasitize. Two types of parasites were found: (1) 2-year-old females (paired) which did not attempt to breed, and (2) older lowranking females ready to breed when they could obtain a nest site.
In many animal species with parental care the fathers may rear young that are not their own. Among geese and a variety of other birds the females too cannot be certain of their parenthood because some of them may save the costs of parental care by laying their eggs in the nests of conspecifics. Such egg dumping or intraspecific nest parasitism occurs in many egg-laying species from insects to birds, especially in the Anseriformes (see reviews by Yom-Tov 1980; Andersson 1984; Eadie et al. 1988; Rohwer & Freeman 1989). Eadie et al. (1988) prefer the neutral term brood amalgamation, as the word 'parasitism' implies an advantage for the dumper and a disadvantage for the host, and for the majority of species this has not been verified. We adhere to the usual terminology, however, because our results indicate that the term parasitism is adequate in this case. As the eggs of hosts and parasites are very similar, intraspecific brood parasitism is not easy to detect. Observations of known females (e.g. Clawson et al. 1979; Syroechovsky 1979; Heusmann et al. 1980), the analysis of egg proteins (Manwell & Baker 1975) and the use of genetic markers (Cooke & Mirsky 1972; Redfield 1973; Lank et al. 1989a, b) and D N A markers (Quinn et al. 1987) have yielded reliable proof of parasitism for some species. However, the majority of studies are based on indirect evidence *To whom reprint requests should be addressed. 0003-3472/91/040677 + 12 $03.00/0
such as differences in shape or colour among the eggs in a clutch, addition of more than one egg per day, appearance of new eggs after the start of incubation, or the occurrence of abnormally large clutches (see review by Yom-Tov 1980). The many hypotheses offered to explain the evolution of egg dumping have been reviewed by Yom-Tov (1980), Andersson (1984), Eadie et al. (1988) and Lank et al. (1989a). The following both assume a benefit to the parasite and a cost to the host, and make testable predictions. (1) A low-return but 'cheap' reproductive strategy of young and/or unpaired females if the costs of reproduction are especially high for young or lowranking birds. Such females would not be expected to breed themselves even if they could obtain a nest. (2) A low-return salvage tactic of females who have lost their nest or have been unable to acquire one. Such females would be expected to breed as soon as a nest became available. (3) A method to increase annual reproductive success beyond what can be achieved by just rearing one's own clutches. The observation of females who parasitize while producing normal-sized clutches in their own nests would support this hypothesis. (4) An unconditional alternative to nesting being maintained in the population through frequencydependent selection, because at some parasite/ breeding ratio the lifetime fitness gain of both types
9 1991 The Association for the Study of Animal Behaviour 677
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would be equal. This hypothesis requires females either always to adopt one or the other strategy, or to use both with fixed probabilities. Andersson (1984) also suggested that the evolution of egg dumping would be facilitated by close relatedness between hosts and parasites. The testing of such hypotheses requires observations of individually known females, but only a few field studies provide such data (see also Yom-Tov 1980; Andersson 1984). In some studies the parasites were mostly young females (Weller 1959; Grenquist 1963; Lank et al. 1989b), and females that had lost their nests (Rosene 1969). In one study females of all ages dumped eggs (Clawson et al. 1979). In several studies particular females laid eggs both in alien and their own nests (Mackie & Buechner 1963; Hoogland & Sherman 1976; Clawson et al. 1979; Heusmann et al. 1980; Brown 1984). In general, the behaviour does not seem restricted to particular individuals or age classes. In contrast to the majority of other studies, we have data based on continuous observations of individuallyknown females. We tried to answer the following questions. (1) What is the extent of nest parasitism? (2) Which females lay parasitic eggs? (3) Are there other behavioural differences between parasitic and non-parasitic females? (4) Which nests and geese are parasitized? (5) Are hosts and parasites closely related? (6) Do parasites profit from dumping their eggs? (7) Does parasitism harm the hosts?
ANIMALS AND METHODS The Birds
Asian bar-headed geese winter in the lowlands of Southern Asia and breed on lakes and rivers of the highlands north of the Himalayas. They tend to nest in colonies on small islands with often less than 1 m between adjacent nests. The clutch size is usually four or five, but nests with up to 10 eggs have also been recorded. Eggs scattered between nests have been observed in dense colonies (Bailey 1910; Kydyraliew 1967; Gole 1982). In March 1988, our semi-captive flock contained 96 birds of 2 or more years (all birds of the previous year had been removed). There were 37 pairs, while five males and 17 females were unpaired. They were all individually ringed; the females were additionally marked on the head with hair dyes of different colours. They lived on the small lake (7.8 ha) at the
Max-Planck-Institut in Southern Germany with some 1000 m 2 of grazing area, the whole area being fenced in against disturbance and predation. Pellet food was available ad libitum in, and sometimes outside, a big cage with a trapdoor where birds were caught for sexing (by cloacal inspection) and ringing in autumn. Permanent food and an ice-free section of the lake kept them from leaving in winter. Since all had been ringed in their first autumn, their ages and genealogies were known. As in previous years (see Lamprecht 1986a, b), 40 nestboxes supplied with straw were placed singly or pairwise on 24 floating platforms (2.5x2-5m) anchored over part of the lake's surface area at the beginning of April. The wooden boxes (90 x 50 cm) with a narrow entrance on one of the short sides were open at the top and had walls 30 cm high. All entrances were oriented towards an observation tower on the shore, from which all occurrences in the nests could be observed. Data Collection
Rank order From 1 March 1988 until the nestboxes were supplied on 7 and 8 April 1988 we recorded agonistic interactions between identified social units (pairs or individuals) whenever possible. From these data we determined a success score for each social unit as the percentage of all observed interactions won. A success score of zero was given to all units with fewer than five observed interactions in order to prevent unrealistically high success scores. These 18 birds or pairs had avoided the proximity of others and had never won an interaction. The social units were grouped into four dominance classes, Of the 36 units with more than five interactions, class 1 comprised the 12 with the highest success scores, class 2 the next 12, and class 3 the 12 units with the lowest success scores. A class 4 was created for the 18 units with fewer than five interactions and thus a zero success score. Nest checks During the laying period (up to 18 May) we visited all nests by boat twice daily, at dawn (around 0600 hours) and dusk (around 2000 hours). Up to three additional checks during the day were made during the peak laying period (18 April-I 0 May). In each nest the eggs were counted, their positions (inside/outside nest bowl) noted and
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679
new eggs labelled with numbers. The geese got used to these disturbances at the nest, and breeding birds immediately resumed incubation when the boat left. Later checks were less regular and after 23 May we mainly visited nests where the female had terminated incubation, to note which eggs had hatched.
nest by a female who was not nor ever became the owner was termed a parasitic egg. A nest containing eggs not laid by the nest owner was termed a parasitized nest. The eggs could be parasitic as defined above or laid by a previous owner of the nest, thus being also foreign to the new owner.
Nest observation
For statistical analysis non-parametric procedures (Siegel 1956; Sachs 1984) were usedl All P-values are two-tailed.
From 9 April to 18 May the tower was occupied about 13 h per day by one or two observers recording details of every visit of a female to a platform or nest. The identity of the female, the platform and/ or nest numbers, arrival and departure times, reason for departure (voluntary or forced), and the types of behaviour performed in the nest were recorded.
Definitions Paired females were those that, after 15 March, were always (except during incubation) seen together with the same gander, while unpaired females were often alone or in the vicinity of different ganders. Young females were all females known to be 2 years old. A female was called the owner of a particular nest on a certain day if the following conditions applied on this and the two following (or preceding) days. (1) More than 50% of her platform visits of the day were to the same platform. If the platform held two nestboxes, more than 50% of her nest visits were to the same nest. (2) The time she spent in this nest on this day was equal to or greater than the sum of the time spent in this nest by all other geese. Females (or pairs) fitting this definition visited one nest almost exclusively and did not visit any other nests regularly. They also defended their nests or consistently attempted to return when driven off by dominant conspecifics. Incubating females kept their eggs warm, did not leave the nest more than five times a day and defended it against other birds. They did not visit other platforms or nests. They were called breeders when incubating a clutch for more than 14 days. Those females that laid at least one egg in a nest they did not own then or later were termed parasitic. Some females were parasitic, but later incubated a clutch of their own. For some of the following calculations they were treated as parasitic, for others as breeder females. An egg laid in a
Analyses
RESULTS
The Extent of Nest Parasitism A total of 360 eggs were laid by the 54 females in the 40 ncstboxes offered, 308 in 34 nests which were then incubated for at least 14 clays (breeders' nests) and 52 in the other six nests where no bird incubated the clutch for an extended period. We could attribute 57 eggs to individual parasitic females; either laying was observed directly or only one female had visited the nest since the last check. A further 3 l eggs could be recognized as parasitic (although the laying females were unknown) according to the following criteria. (1) The new egg had been found in the morning and the nest owner also laid an egg during the same day, so the first egg was assumed to be parasitic, since geese have never been found to lay more than one within about 24 h (Wiirdinger 1973; Bezzel 1985; for chicks, Gallus gallus domesticus, Romanoff & Romanoff 1949 showed that the minimum interval between two eggs was longer than 24 h). (2) The new egg appeared in a clutch that had already been incubated for more than 2 weeks. Geese stop laying when they start incubation (W/irdinger 1973). (3) The new, unlabeUed egg was found in front of a nest where the owner had incubated for more than 3 days. None of the 84 eggs that could be attributed to nest owners was ever laid outside the nest bowl. (4) Eight eggs were laid in two nests which both remained ownerless. As such eggs are potentially taken over and incubated by another female claiming the nest, they were regarded as parasitic. Thus we could identify 88 eggs as parasitic. Additionally, in 10 instances two new eggs were found in a nest in the morning. Due to the physiological constraints mentioned above, at least one of
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680
Table 1. Distribution of the 98 parasitic eggs over the 40 nests Number of parasitic eggs 0 Numberofnests
1
2
3
4
5
6
7
8
10 10 4
3
4
3
3
2
1
Table II. Relationship between behaviour and type of female Behaviour
Female
Pure parasite (13) (direct evidence)
Unpaired female (7) Young paired female (5) Older paired female (1)
Pure parasite (4) (indirect evidence)
Unpaired female(1) Young paired female (3)
Parasite, then nestowner (3)
Unpaired female (I) Older paired female (2)
Non-parasitic breeder (30)
Unpaired female(8) Older paired female (22)
Parasite, then breeder (4)
Older paired female (4)
The number of females belonging to each type is given in parentheses. Young femaleswere known to be 2 years old. For other definitionssee text. them was very likely to be parasitic in each case, but we could not tell which. In total, at least 98 (27-2%) of the 360 eggs were parasitic. From one to eight parasites" eggs were found in 30 of the 40 nests (Table I). Of the 34 breeders' nests, 25 (73.5%) were parasitized; of the six nonincubated nests, five (83.3%) contained one or more parasitic eggs. Identity of Parasitic Females The majority of parasitic females were identified because we could attribute to them at least one parasite egg (direct evidence). In four females we only noted their extended belly which indicated the presence of fully developed eggs. As no eggs were found outside nests, these females must have laid their eggs in nests of others (indirect evidence, Table II).
Thirty of the 34 breeders were never observed to dump eggs (Table II). With one exception (see below) females were never observed to dump eggs on others while they were owners of a nest. Among females that had dumped eggs at some time there were fewer nest owners than among nonparasites (Table III). Parasitic females were more often low in rank, more often young, i.e. 2 years old, but not more often unpaired (Table III). Fewer parasitic than non-parasitic females had experienced earlier breeding attempts and breeding successes (Table III). However, if young parasitic females under 4 years old are excluded, eight of the remaining 12 had bred in previous years. The parasitic females did not seem to be a unitary group. There were seven females that first parasitized, but later owned a nest or even became a breeder (Table II). They laid their first egg earlier in the season than the 13 females observed to parasitize exclusively (Mann-Whitney U-test, P < 0-05). They also showed features typical of breeders (see below), in that they tended to spend more time in a nest while laying an egg, although not significantly so (P<0.06) and were significantly less often chased from a nest after laying (P < 0-002) than the 13 purely parasitic females. Compared with the 30 non-parasitic breeders they became nest owners significantly later in the season (P < 0-02). The eight young paired females, on the other hand, never owned a nest and parasitized exclusively, while of the 17 unpaired females, eight bred without being parasitic (Fisher test, P < 0"05). Only three (37.5%) of the young paired females were in the lowest rank category (category 4), as were 13 (76"5%) of the unpaired females. Although the difference was not significant (Fisher test, P < 0' 16), the paired young females tended to rank higher (not lower as might be expected) than the (older) unpaired females. Since rank correlates positively with the probability of obtaining a nest (Lamprecht 1986b), the above difference in breeding probability suggests a lower breeding propensity of young females.
Behaviour of Females Differences in the behaviour between parasites and non-parasites may indicate that parasitic females are not dumping eggs 'by mistake', but are aware of being in a nest that is not their own. In fact 56 eggs of known parasitic females were laid when
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681
Table III. Parasitic (N= 20) and non-parasitic (N= 30) females classified according to different variables Variable Nest owner Previous breeding attempts Previous breeding successes Rank category Age Female type
Parasites
Non-parasites
7 13 11 9 16 4 4 16 5 15 12 8
30 0 3 27 I0 20 19 11 0 30 22 8
Yes No 0 >0 0 >0 1+ 2 3+4 2 years Older Paired Unpaired
P*
<0.001 < 0.002 <0.003 < 0.006 <0-02 >0.49
*Fisher exact probability test.
Table IV. Behavioural differences between parasitic and non-parasitic females Parasites
Breeders
Variable
N
Median
N
Median
P*
Mean no. of different platforms visited per day No. of days not visiting any platforms Mean no. of platform visits before egg laying Mean no. of nest visits before egg laying Mean no. of different platforms visited before egg laying Mean no. of different nests visited before egg laying Time spent on nest at egg laying (min) % of egg depositions with female being bitten % of leavings after laying, due to harassment Mean no. of platform visits on same day after laying Mean no. of nest visits on same day after laying Mean no. of return visits to same nest on same day after laying
16 16 20 20 20 20 20 20 20 20 20
2.22 6-5 6.6 4.25 2.85 2.6 28.25 41.5 83.5 0.0 0.0
34 34 32 32 32 32 32 32 32 32 32
1.32 0.5 5.0 4.50 1.0 1.0 183.0 0.0 0.0 2.0 2.0
<0.0001 <0.0001 <0.075 >0.7 <0.001 < 0.001 <0.001 <0.001 <0.001 <0.001 <0.001
20
0.0
32
2.0
<0.01
*Mann-Whitney U-test.
the females did n o t o w n nests. The only exception was by a female who laid her last parasitic egg o n the first day o f b e c o m i n g a nest owner. Investigating b e h a v i o u r a l aspects o f the entire laying season (9 A p r i l - 1 8 May), we c o m p a r e d the 16 females observed to be n o n - b r e e d i n g d u m p e r s with the 34 breeders (see Table II). W h e n dealing with aspects o f particular egg depositions, we used all observations of egg d u m p i n g (20 parasitic females) a n d o f laying non-parasitic eggs (32 breeder females). As tests were m a d e with the
females as units o f comparison, the d a t a on several egg depositions o f a female were averaged. C o m p a r e d with breeders, parasitic females visited m o r e different nest platforms per day a n d h a d m o r e days with n o p l a t f o r m visits at all during the entire laying season (Table IV). O n days w h e n a n egg was laid, parasitic females visited more different platforms a n d nests before laying the egg t h a n did breeders (Table IV). This was n o t because parasites laid later in the day a n d thus were observed for longer. In fact m e a n pre-
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laying observation time was longer for breeders (median 9 h) than for parasites (median 4 h, U-test, P<0.001). During the laying of an egg, parasites spent less time in a nest than breeders, and were more often bitten by other geese (Table IV). They more often left the nest after laying because of harassment (usually by the nest owners). After laying an egg, a parasite rarely visited platforms or nests that same day, while breeders did so regularly (Table IV). In those situations, breeders almost exclusively revisited the same (their own) nest, but only one parasitic female once revisited the nest in which she had dumped an egg. Parasitized Nests The 98 parasitic eggs were all laid on 33 out of 37 days between 17 April and 23 May. Of these, 45.9% were laid in nests without owners (phase 1), 32.7% in nests with an owner in the laying period (phase 2), and 21.4% in nests with owners already incubating a clutch (phase 3). As the number of nests in a certain phase changed daily, we calculated the percentage of nests in the different phases for each day. This gave the expected proportions of eggs laid in nests of the different phases, supposing that parasitic females did not discriminate between nest phases. The observed proportions for each day were the percentages of parasitic eggs actually laid in nests of the three different phases. With Wilcoxon tests we investigated, for each nest phase, whether observed and expected proportions differed in any systematic way (N= 33 days, Fig. 1). Parasitic eggs were laid more often than expected into nests in phase 1 (P < 0.02) and more rarely than expected in phase 3 nests (P < 0.001). There was no significantdifference with respect to nests in phase 2 ( P > 0.22). If individual females that laid several eggs had general preferences for particular nest phases, it would be misleading to treat each egg laying as an independentevent. We therefore recalculated on the basis of the 20 females to which a total of 57 parasitic eggs could be attributed. When a female had laid several eggs the differences between expected and observed proportions for each nest phase were averaged. Wilcoxon tests gave the same results as above: parasitic females laid more often than expected in nests of phase 1 (P<0.01), there was no significant difference with respect to phase 2 nests (P>0.1), and they laid more rarely than expected in phase 3 nests ( P < 0.001).
Identity of Hosts
The number of parasitic eggs laid in a nest with an owner (phase 2 or 3) correlated positively with the dominance rank (success score) of the owner (Spearman r s = 0-493, N = 37 nests, P < 0.001). Thus high-ranking females were more often parasitized. If high-ranking females owned nests earlier than low-ranking ones, there would be more time to parasitize their nests, giving rise to the above correlation. But the date at which nest ownership started did not correlate with the number of parasitic eggs in the nest (rs = 0'038, N=37, P > 0"6), and the dominance rank of an owner did not correlate significantly with the date on which she acquired the nest (rs = 0"237, N = 37, P > 0'2). We could not decide definitely whether parasitic females selected nests of dominant females directly or tended to dump their eggs in generally attractive nests, which were mainly held by dominant females. The second possibility seems less likely because the correlation between the dominance rank of a breeder and the total number of parasitic eggs in its nest, including those eggs present when taking possession of the nest, is not significant (rs= 0-27, N = 34 nests, P>0.11). Kin Selection and Nest Parasitism
Of the 20 parasitic females, 10 had close relatives breeding in the flock (four mothers, five sisters, and one daughter). But only two females dumped one egg each in the nest of a mother and a sister. Three and five eggs could be attributed to these two parasitic females, yet they used a different nest for each egg, not apparently concentrating on nests of close relatives. During egg laying they spent only 12 and 15 min in the nests and were harassed and bitten by the mother and sister, respectively. The Benefit to Parasites
Five parasitic eggs, and one in those egg pairs where one egg or the other must have been parasitic, hatched in four different nests, giving a hatching success of 5"1% (or 6.1%) among the 98 parasitic eggs. Including these, 80 goslings hatched that year. Thus 6.25% (or 7.50%) of them were not the direct descendants of their 'mothers'. From the 84 eggs that could with certaintY be attributed to breeding females, 38 (45.2%) hatched. Thus the success rate of non-parasitic eggs appears to be about nine (or seven) times greater than that of parasitic eggs.
Weigmann & Lamprecht: Nest parasitism in geese
683
9
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Figure 1. Percentage of nests in different phases on each day: (a) no owner; (b) laying owner; and (c) incubating owner ( ). Corresponding percentages of parasitic eggs laid in nests of the different phases (O). The five (or six) parasitic eggs that finally hatched had all been laid in nests with owners during the laying period. The Disadvantage
to the Hosts
Of the 34 breeders' nests, 25 were parasitized and nine were not; we used all eggs laid in these nestboxes for our comparison. In many nests it was impossible to attribute each egg to a particular female. We therefore treated every egg that was not clearly parasitic according to our criteria (see
Results: Extent of Nest Parasitism) as the breeder's. One hatched egg that could have been either was regarded as the host's egg. For each nest we calculated the percentage of parasitic eggs (degree of parasitism) and the percentage hatched of the remaining (the host's) eggs (host's success rate). There was a significant negative correlation between degree of parasitism and the host's success rate (Fig. 2). The host's median success rate was 67% in nonparasitized nests and 29% in parasitized nests (U-test, P<0.05). While some eggs hatched in all
Animal Behaviour, 41, 4
684
,~176 I o
9
50 T
0
50
I00
% Parasitic eggs in nest
Figure 2. Relationship between the percentage of parasitic eggs in the clutch and the percentage of host eggs hatched (N = 34 breeders' nests): r s = - 0' 59, P < 0-001. Regression: Y= - 0.94X+ 68.
Table V. Ejection of eggs from the nest bowl by owners of nests that did or did not contain foreign eggs Nests without any foreign eggs
Nests with foreign eggs
Nest no.
Clutch size
No. of eggs later found outside nest
Nest no.
No. of eggs taken over
No. of these later found outside nest
1
6
2 3 4 5 6 7 8 9
5 7 5 4 5 3 5 7
0
1
3
3
0 2 2 0 0 0 0 0
2 3 4 5 6
5 6 9 8 9
3 5 6 8 6
'Foreign eggs' or 'eggs taken over' were eggs already in the nest when the female became the owner of the r~est.
non-parasitized nests, all failed nests contained some parasitic eggs. The disadvantage to the hosts was p r o b a b l y due to the enlarged size o f the clutches with parasitic
eggs. The hatching rate (%) o f all eggs in the nest showed a high negative correlation with the total n u m b e r ( r a n g e = 3 - 1 9 ) o f eggs present ( r s = - 0 . 7 1 3 , N = 3 4 , P < 0 ' 0 0 0 1 ) , and the n u m b e r o f
Weigmann & Lamprecht: Nest parasitism in geese parasitic eggs was strongly related to the total number of eggs in the nest (rs=0"943 , N = 3 4 , P<0"0001). Defensive Measures of Hosts
There are two ways in which a female may be induced to incubate eggs she has not laid herself: (1) by becoming the owner of a nest that already contains eggs, and (2) by having eggs laid in her nest while she owns it. Six females became owners of nestboxes relatively late in the season and so obtained boxes that already contained eggs. These were not incubated by any female and were usually scattered in the straw, and no nest bowl had been built. The females then laid their own eggs and constructed a nest bowl. They never included all previous eggs into the clutch they incubated (Table V). On average only 22.5% of such alien eggs were incubated. In nests without any foreign eggs only 9"3% of the eggs were later found outside the nest bowl (Table V). Nest owners (usually assisted by their mates) often attacked other females that came close to or into their nests. Thus parasitic females were often harassed during egg laying (see above). However, many females sitting on their eggs did not move (or attack) when another female entered the nestbox to lay an egg. This was why a number of parasitic eggs were laid outside nests. No nest owner was ever observed to lay an egg outside the nest bowl. Of the 15 parasitic eggs laid beside nests (less than 50 cm from the rim) only three were later found in the nest bowl, apparently retrieved by the hosts. Incubating females of various goose species retrieve all eggs within 90 cm of the rim of the nest bowl (Poulsen 1953; Prevett & Prevett 1973). Poulsen (1953) found that species belonging to the same avian order showed almost the same tendencies for egg retrieval. Thus we expected our bar-headed geese to retrieve all eggs at such close range. However, significantly fewer eggs than expected were retrieved (KolmogorovSmirnov goodness-of-fit test, P<0"001). As four nests had two marginal eggs, only 11 females faced the decision whether or not to retrieve them. Three of them retrieved one egg each. This result differs significantly from the expectation that all females should retrieve marginal eggs (Kolmogorov-Smirnov test, P<0.001).
685
DISCUSSION The Term 'Parasitism'
It would be appropriate to call egg dumping a case of parasitism if the dumpers profited at the expense of the hosts. Indeed in our goose flock 56% of the parasite eggs hatched. This corresponds to the sittiation in wild lesser snow geese, Chen caerulescens caerulescens, where 5.3% of the goslings appeared to have hatched from parasitic eggs (Lank et al. 1989a). The gain of reproductive success through egg dumping was about seven to nine times lower than through rearing one's own clutch, but higher than if no eggs had been produced. The present study also demonstrates the reproductive costs of being parasitized. The reduction of the hosts' hatching rate through the presence of dumped eggs from 67% to 29% seems very high, yet effects of similar size have been found in starlings, Sturnus vulgaris, and goldeneye ducks, Bucephala clangula (Yom-Tov 1980). The alternative interpretation, that it was inattentive breeders that had poor success and were often parasitized is unlikely, as it was the dominant breeders that were more often parasitized, and these breed more successfully than low-ranking nest owners (Lamprecht 1986b). Such costs of being parasitized can explain the evolution of the three means of defence of nest owners against parasitic eggs: (1) chasing other geese from the nest (see also Mineau & Cooke 1979; Owen & Wells 1979); (2) not adopting eggs already present when the nest is first occupied (see also Pienkowski & Evans 1982 for the shelduck, Tadorna tadorna); and (3) inhibition of egg retrieval when nest parasitism is common (Prevett & Prevett 1973). The Extent of Parasitism
Fifty-seven per cent of owner-nests were parasitized. This is similar to the figures reported for wild birds. Among shelducks 30-50% of nests (Pienkowski & Evans 1982) and among mergansers, Mergus serrator, 64% of nests (Young & Titman 1988) were estimated to contain dumped eggs, and lesser snow geese goslings hatched from parasitic eggs were found in 22% of nests (Lank et al. 1989a). Given the low hatching rate of parasitic eggs the number of parasitized nests may have been much higher. There may be several reasons for the high rate of parasitism found in our flock.
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Animal Behaviour, 41, 4
(1) Through detailed observations of individual birds' behaviour many eggs were identified as parasitic that would not have been recognized by cruder methods. Several authors admit that their estimates of parasitized nests were probably too low (Gibbons 1986; Lank et al. 1989a). (2) Competition for nest sites may have been exceptionally high. But a field report of bar-headed geese by Sch/ifer (1938) indicates that nest sites are also rare and contested in the wild. (3) As young females are especially likely to parasitize, a high proportion in the flock could explain a high parasitism rate. Yet in our flock the proportion of 2-year-old females was only slightly higher (14.8%) than in the snow goose population (12.1%) studied by Lank et al. (1989b).
Behaviour of Parasitic Females Many of the behavioural differences between parasitic and breeder females might be explained by the different conditions met at a nest site. Territorial aggression of nest owners may have caused parasites to visit several nests, spend less time on a nest at egg laying, and terminate egg laying when harassed. But we often observed the same behavioural features in parasitic females when nest owners were absent or non-existent. This and the following differences from nest owners indicate that a parasitic female is aware of the fact that she is not laying in a nest of her own. (1) She rarely visits nests on non-laying days. (2) She shows no tendency to visit the same nest repeatedly, even when no harassment took place. (3) She rarely visits nests after having laid an egg, and (4) if she does, it is not the nest where she laid. Apparently a parasitic female shows a pronounced interest in nests onlywhen she needs one for depositing an egg. Her tendency to choose a different nest for each egg ('scattered laying', el. wood duck: Heusmann et al. 1980) may be adaptive, because it slows the increase of clutch size and consequent decline of the hatching rate (see discussion by Andersson 1984).
Identity of Parasitic Females Parasitic females were those who did not own a nest at the time of laying, and some never owned a nest. Yet in spite of this common feature, the parasites comprised at least two different kinds of females. (1) The eight young (2-year-old) females that were paired but apparently did not try to claim a
nest. One 'older' paired female that was also purely parasitic (Table II) was only 3 years old. (2) The older, unpaired or paired females that later in the season became breeders or at least nest owners. Even when dumping eggs, these seven females differed from the other parasites and behaved similarly to breeder females. They gave the impression of trying to establish a nest of their own, but were unable t~ hold it against competitors, The eight unpaired parasites, all of them older than 2 years, may have belonged to either group.
Parasitized Nests Parasitic females preferred to lay in ownerless nests and avoided laying in nests with an incubating female. They probably preferred nests with a lower possibility of being attacked, since parasites tended to suffer fewer attacks at nests without owners than at nests defended by a female or pair, although not significantly so (Wilcoxon matched-pairs signedranks test, P<0"06). Lank et al. (1989b) observed that parasitic snow goose females tended to lay in nests with the ownerspresent, yet admitted that their sample of six observations may have been biased; as the majority of their birds were unmarked, they were able to tell owners from parasites only when agonistic interactions occurred. The presence of nest-like structures (boxes with straw) with no owners may have been an artefact in our setup. If they did not occur in nature, parasites would only find nests that belonged to the females that built them. In this case, and if parasitic geese adhered to the rule of laying in nests where they were not attacked immediately, eggs would most often be dumped in laying phase nests, as laying geese are not continuously present at the nest. Parasitic females preferred the nests of dominant owners. This would be advantageous, as highranking pairs usually have higher hatching and fledging success than low-ranking pairs (Lamprecht 1986b). High-ranking birds were more often parasitized and thus suffered higher costs than low-ranking birds. But among the 54 females, dominance (i.e. the success score) still correlated positively with the number of eggs hatched (rs = 0-42, P < 0.003). The costs of being parasitized do not seem to be reduced much through kin selection. Only two females dumped an egg with close relatives, although half of the parasitic females had closely related nest owners in the flock.
Weigmann & Lamprecht: Nest parasitism in geese
Conclusions The behavioural observations suggest that female geese do not dump eggs into other nests 'by mistake', but are aware that the nest is not their own. Egg dumping seems to be adaptive, probably serving different functions in different individuals. (1) It seems to be a 'salvage strategy' (Lank et al. 1989a) of females older than 2 years prevented from breeding by competition for nest sites. They stop dumping eggs as soon as they get an opportunity to breed. (2) It also appears to be part of a conditional lifehistory strategy: females tend to dump eggs when young and breed when older than 2 years. Grice & Jones (1965, cited in Heusmann et al. 1980) suggested that young female wood ducks first passed through a parasitic stage. This seems also to apply to bar-headed geese. As geese are long-lived it may be advantageous to refrain from costly breeding when young, inexperienced and low-ranking, if this increases future reproductive output and/or survival. But why should young females produce eggs at all? F r o m observations in previous years we know that 2-year-old females are physiologically able to breed. One actually fledged young. If breeding costs depended on prevailing conditions that were unpredictable before arrival on the breeding grounds, even a young female should be prepared to breed if conditions turned out to be favourable. If not, there is still the alternative of dumping the eggs in the nests of others, though reproductive success will be low. Since females did not parasitize when they had nests of their own, egg dumping does not seem to be used in addition to own breeding, as it is in some swallows (Brown 1984; Moiler 1987) and sparrows (Kendra et al. 1988). M o s t parasitic females had bred in previous years or bred later. Thus fixed specialists for either nesting or parasitizing do not seem to occur, and in most females egg dumping appeared contingent upon the lack of a defensible nesting site.
ACKNOWLEDGMENTS We thank J. Schneider, A. Meilinger, T. Friedl and H. Buhrow for their unfaltering help during data collection, J. M. Black, J. Schneider and W. Wickler for helpful comments on the manuscript, B. Knauer for drawing the figures and P. Rechten for help in correcting the English.
687
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