Why do snow geese adopt eggs?

Nesting female lesser snow geese (Anser caerulescens caerulescens) usually adopt eggs that are laidadjacent to their nests by potential intraspecific nest parasites. The host female rolls the parasite'segg up into the nest, using the same behavior patterns used to retrieve her own eggs if theyare displaced from the nest. The reproductive consequences of adopting eggs are unclear. Weconsider three selective scenarios that might maintain adoption behavior in geese: (1) eggadoption is of no reproductive consequence to the host; (2) egg adoption augments hostreproductive success relative to that of unparasitized nests; and (3) egg adoption is making thebest of a bad situation, once a female's options are constrained by the presence of an eggadjacent to the nest; we also consider (4) the possibility that adoption, if not concordant withthe selective regime, is maladaptive. Nest parasitism is costly to the host, making hypotheses 1and 2 unlikely. However, adopting eggs significantly decreases the risk of total nest failureduring laying, more than offsetting other probable host costs. This is consistent with hypothesis3. Experiments show that geese have limited abilities to retrieve eggs, which accounts for mostcases of nonadoption of nearby eggs. We conclude that adoption of eggs is an adaptive trait,a form of nest protection. Adopting eggs is the best option within the species' repertoire tothe threat to nest survival created when a parasite lays an egg next to the nest. [Behav Ecol1991;2:181-187]

David B. LankMarjorie A. BousfieldFred CookeDepartment of Biology,Queen's University,Kingston, OntarioK7L 3N6, Canada

Robert F. RockwellDepartment of Biology,City College of New York,New York, NY 10031, USAandDepartment of Ornithology,American Museum ofNatural History,Central Park West at79th Street,New York, NY 19924, USA

Conspecific egg adoption, denned as theactive incorporation of unrelated eggs

into a clutch by a nesting individual, has beenreported among lesser snow geese Anser ca-erulescens caerulescens at three sites (Lank etal., 1989b; Litvin and Syroechkovskiy, 1984;Prevett and Prevett, 1973; Syroechkovskiy,1979) and has also been observed in otherarctic-nesting geese (Branta leucopsis: For-slund P and Larsson K, personal communi-cation; B. leucopsis, A. albifrons and A. fabalis:Litvin KE and Syroechkovskiy EV, personalcommunication). The retrieval of eggs into anest by geese is a classic example of an etho-logical fixed-action pattern described for nu-merous waterfowl (Lorenz and Tinbergen,1957), which is of obvious adaptive value whenthe egg has been laid by the nesting female.Use of this behavior pattern to adopt eggs,however, raises questions about the selectiveregime operating on this behavior and thespecies' response to it.

Egg adoption in snow geese occurs in con-junction with attempts at intraspecific nestparasitism. Successful nest parasitism is com-mon in this species, accounting for 2%—9% of

the goslings hatched annually at the well-stud-ied colony at La Perouse Bay, Manitoba, Can-ada (Lank et al., 1989a) and potentially farhigher proportions in some years at morenortherly breeding colonies (Cooch, 1958;Syroechkovskiy, 1979). Parasitic females usu-ally attempt to lay directly into occupied nestsbut often cannot dislodge the attendant fe-male (Gurtovaya, 1990; Lank et al., 1989b;Syroechkovskiy, 1979). The parasite may thenlay adjacent to the nest and depart, leavingbehind a large, white egg. For parasitism tosucceed in such cases, the host female mustsubsequently adopt the egg by rolling it intothe nest, and she usually, but not always, doesso (Lank et al., 1989b; Litvin and Syroech-kovskiy, 1984).

Why do snow geese adopt eggs? Adoptionof eggs utilizes behavior that evolved in thecontext of retrieval of a female's own dis-placed eggs. Retrieval is found in most relatedspecies of geese and is thus primitive relativeto adoption. The behavior has not obviouslybeen modified in any way for its use in thecontext of adoption. One might thus consideradoption as a clear exaptation (Gould and

Address reprint requests toF. Cooke.Received 10 September 1990Revised 3 April 1991Accepted 5 April 1991

1045-2249/91/52.00© 1991 International Societyfor Behavioral Ecology

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Vrba, 1982): a character co-opted for a newuse. We are evaluating the selective regimeoperating on the character in its new context.

We consider three selective scenarios thatmight maintain adoption behavior in geese:(1) egg adoption is of no measurable repro-ductive value to the host; (2) egg adoptionaugments host reproductive success relativeto that of unparasitized geese; and (3) eggadoption is the lower cost option to nona-doption, once a female's choices are con-strained by the presence of an egg beside thenest; specifically, adoption may decrease theprobability of avian predators discovering anddestroying a nest. We also consider (4) thepossibility that the behavior is maladaptive;that is, it is not concordant with the selectiveregime.

We first evaluate these hypotheses by in-tegrating literature and presenting originaldata from the La Perouse Bay colony on thecosts and benefits of adoption (see Rockwellet al., 1983, for general field methods). Wethen examine variation in the probability ofegg adoption through analysis of goose be-havior after experimental displacement of eggsfrom the nest and relate this variation to thehypotheses. Finally, we consider the relevanceof hypotheses suggested to account for allo-parental care in other groups of animals.

Evaluation of selective hypotheses

Hypothesis 1: adoption is of no reproductivesignificance for the hostIf adoption were of little or no reproductiveconsequence, there would be no selective ad-vantage or disadvantage to treating potentialparasitic eggs differently from the nestingfemale's own. Thus, the behavior might persistas an unselected, genetically "fixed" actionpattern in response to the perception of anyegg outside a nest.

Nest parasitism is not benign to snow goosehosts (Lank et al., 1989a, 1990). Althoughaddition of one supplemental egg does notsignificantly change the host's probability oftotal nest failure, addition of multiple eggsseriously decreases nest survival. Hosts hatchan estimated 66% of their own eggs as com-pared with 72% for nonhosts. Egg loss duringnesting is at least in part directly attributableto parasitic activity. In captivity, the rate ofegg breakage is directly proportional to thenumber of extra eggs in the nest, and eggbreakage has been observed during parasitismattempts (Bousfield MA, unpublished data).There are no compensatory reproductive orsurvival advantages for hosts in other fitnesscomponents (Lank et al., 1990). Although thecost of a single additional egg is not large,

parasitism is not advantageous, and thus weinfer that adoption is not a selectively neutralcharacter. We assume that some direct or in-direct form of discrimination of host versusparasitic eggs could evolve (see below). Thus,the hypothesis that egg adoption is a selec-tively neutral, unselected byproduct of eggretrieval is not supported.

Hypothesis 2: adoption augments host femalereproductive success relative to that ofunparasitized geeseSeveral authors have proposed that host wa-terfowl might directly benefit from parasitismby enlarging their brood size or by other mech-anisms (Eadie and Lumsden, 1985; Eadie etal., 1988; but see Amat, 1987; Eadie, in press).Since nest parasitism is disadvantageous tosnow goose hosts, the hypothesis that adop-tion occurs to facilitate parasitism does notapply. Nor do snow geese appear to obtainindirect reproductive benefits by adopting eggslaid by kin (Lank et al., 1989b), as hypothe-sized by Anderson (1984) for female philo-patric waterfowl.

Hypothesis 3: adoption is favored, giventhe constraint imposed by parasiticlaying next to the nestBecause being parasitized is costly, hostsshould attempt to prevent parasitic laying,which they do through nest-site defense (Lanket al., 1989b; Mineau and Cooke, 1979). Ifsuch defense fails, however, and an egg is laidnear a nest, the host's options are limited. Eggadoption under these conditions may be a low-er cost alternative to nonadoption. Adoptionmay be a form of nest protection. Snow goosenests are normally cryptic during laying, pri-marily to deter detection by predators(Kretchmar and Syroechkovskiy, 1978). Lanket al. (1989a) speculated that unattended,conspicuous eggs might attract avian preda-tors to the nest site and thereby threaten thesurvival of the nest. Return of predators tonest sites after taking a single egg has beendocumented for hooded crows (Corvus corone;Salathe, 1987; Sonerud and Fjeld, 1987) andarctic skuas (Stercorarius parasiticus; Enquist,1983). Arctic skuas and herring gulls (Larusargentatus) are the principal avian predatorson snow goose nests at the La Perouse Baycolony near Churchill, Manitoba, Canada. Weexamined data collected at this site between1973 and 1990 to test whether adoption ofeggs was associated with nest survival.

Goose nests are most vulnerable to egg lossand failure from avian predators during thelaying period, when the nest is often unat-tended (Mineau and Cooke, 1979; Rockwell

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et al., 1987). Data were available for 109 nestswhere newly laid (unnumbered) eggs werefound outside nests on daily nest visits duringthe laying period and for which the nest wasnot abandoned or destroyed the day after theextra egg appeared. The latter restriction onthe data set assured us that the nesting femalehad returned to the nest and had had theopportunity to adopt the egg. Although someof the eggs in this sample may have been laidby the nesting female, at least 85% were laidby parasites (Lank et al., 1990).

Nests where the egg was retrieved were morelikely to survive to the onset of incubationthan those where the egg was not retrieved(Table 1), consistent with the nest-defense hy-pothesis. Twelve percent of nests where eggswere not retrieved failed (n = 99), as com-pared with 0 in the sample where eggs wererolled in (n = 24). This lowered risk of totalnest failure would more than offset the ap-proximate 6% lower hatchability of host eggsconcomitant with parasitism. Egg adoption isfavored under these conditions.

Detailed examination of the fates of eggs inthe nests that failed supports the hypothesisthat attraction of predators was the mecha-nism responsible for lower nest survival wheneggs were not adopted. In none of the 12failed nests did an egg inside the nest disap-pear before the disappearance of the egg out-side the nest. In six cases, the outside eggdisappeared first, followed on subsequent daysby the egg or eggs in the nest. In the remainingcases, the outside egg disappeared on the sameday as at least some of the eggs in the nest.At four nests, newly laid eggs continued to belost from the nest after the egg outside thenest had been taken. These patterns of dis-appearance suggest that predators first dis-covered and took the egg outside the nest andsubsequently returned to the site, causing to-tal nest failure.

Hypothesis 4: adoption is maladaptiveBecause we have identified a net advantage toadoption, despite a cost of parasitism, we con-clude that the behavior is adaptive, that is,concordant with the selective regime. Severaladditional points require discussion. First, onemight suggest that adoption of eggs was main-tained to prevent the possibility of failing toretrieve a host's own egg that rolled out ofthe nest. The small cost of adopting a singleegg might be more than offset by minimizingthe risk of failing to retrieve one's own eggs.Egg retrieval is important in this population;in our survey of nest records, 89 of 261 eggsfound outside nests had previously been in-side. If adoption did not serve the additionalrole of nest protection, the selective regime

Table 1Survival frequencies of nests at which a newly laidegg found outside of the nest was or was not rolledin by the host"

Nest survivalto incubation

Behavior of host Yes No

Egg rolled in 24 0Egg not rolled in 74 11

G=5.81,df = 1p = .016

° This sample does not reflect the proportions of nestswhere eggs are or are not rolled in because in most caseseggs are adopted or retrieved before nest visits andtherefore are not detected.

would favor the evolution of discriminationagainst parasitic eggs, as occurs through in-traspecific egg recognition in some bird spe-cies (Arnold, 1987). In snow geese, discrimi-nation against parasitic eggs need not involveegg recognition. Unlike species in which par-asitic eggs are laid in nests while hosts areabsent, snow geese could respond to the be-havioral cue of an intense agonistic interac-tion just before the presence of an egg outsidethe nest. Selection would then favor a de-crease in the propensity to roll eggs after suchencounters. Snow geese may in fact discrim-inate their own eggs from others probabilisti-cally on the basis of their distance from thenest (see below). Because it appears advan-tageous to adopt eggs, the avoidance of re-trieval hypothesis is unnecessary. However,were this the selective factor involved, wewould consider the behavior to be maladap-tive.

Second, it is clear that at least under ex-perimental conditions, birds will adopt eggsto the point of inducing nest failure. Litvinand Syroechkovskiy (1984) report that geesepresented with up to 10 experimental eggscontinued to roll them into a nest, which al-most certainly would result in incubation fail-ure. It is unclear how often such situationsmay occur in nature, but very large clutch sizesdo occur and usually result in abandoned nests(Cooch, 1958; Syroechkovskiy, 1979).

Finally, one can imagine additional adaptiveoptions for hosts, including covering the par-asitic egg, rolling it away from the nest, oreating it. These behaviors do not commonlyoccur. Snow geese occasionally move theirnests to encompass nearby eggs (Bousfield MA,personal observations; Prevett and Prevett,1973), perhaps in cases where they are unableto retrieve eggs (see below). In general, how-ever, maintaining a second nest would be atime- and material-consuming activity. Eggsin some cases are found farther from neststhan they previously had been; however, wesuspect that this is an unintentional result of

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trying to retrieve eggs (see below). Snow geeseeat broken eggs (Bousfield MA, personal ob-servations; Ryder, 1969) and could benefitsubstantially by consuming an egg at a timeof year when food is scarce. However, thereis no suggestion that snow geese damage orconsume intact eggs, parasitic or otherwise.Breaking and consuming an egg near the nestmight release odors and attract mammalianpredators; for whatever reasons, eating intacteggs does not occur in snow geese, nor in anyother avian species, as a defense against in-traspecific nest parasitism. Although we canimagine other, perhaps more advantageousoptions for snow geese faced with parasiticeggs lying near their nests, adoption of eggsis nonetheless adaptive.

Why are some eggs not adopted?

Not all snow goose eggs found outside of nestsare retrieved. During the laying period at LaPerouse Bay, at least 7% of parasitic eggs re-main outside attended nests (Lanket al., 1990).Cooch (1958) reported that females failed toretrieve naturally displaced eggs at 10 nests;however, retrieved eggs were probably not de-tected (Cooch FG, personal communication).Prevett and Prevett (1973: 202) reported thatthey "often saw eggs lying outside nests" dur-ing laying. If selection favors retrieval, whyare some eggs left out? Does nonretrieval ofthese eggs reflect adaptive behavioral vari-ability in adoptive behavior, discriminationagainst parasitic eggs, or are geese simply un-able to retrieve eggs under certain conditions?

Egg retrieval by snow geese is similar to thatof greylag geese (Litvin and Syroechkovskiy,1984; Lorenz and Tinbergen, 1957; Prevettand Prevett, 1973). Geese face eggs, thengently roll them toward their feet with theirlower mandibles. If the egg is more than aneck length away from the nest, the goosemoves the egg in stages, returning to the nestbetween single rolling attempts. The detaileddescription of the behavior by Lorenz andTinbergen (1957) makes clear that, althoughgeese are able to move eggs, they are not es-pecially facile at doing so.

Do all females attempt to retrieve eggs? Weexperimentally displaced an egg 1 m from itsnest during incubation and made behavioralobservations for 20 min after a female's re-turn. The probability of egg retrieval does notvary with stage of incubation (Lank et al.,1989b; Litvin and Syroechkovskiy, 1984;Prevett and Prevett, 1973). All 30 females ob-served attempted to retrieve the egg within30 s of their return. The most persistent fe-male made 10 distinct attempts during 10.5min before succeeding in retrieving the egg.Seven females failed to retrieve the egg during

the observation period, despite at least oneattempt. Giving-up times varied from 40 s to5 min following return. Similar findings werereported by Litvin and Syroechkovskiy (1984).It is unclear whether the variation in persis-tence in our experiments reflects variation inthe egg's mobility and the goose's assessmentof it or real variation in retrieval motivation.However, all females at least attempted to re-trieve the eggs.

Unretrieved eggs were returned to all nestsafter our experiments. Successful egg retriev-al was not correlated with the nest's subse-quent survival to hatching (G = 0.85, df = 1,p = .35). This makes unlikely the hypothesisthat failure to retrieve eggs in nature reflectsthe behavior of lower-quality females, whichcould be advanced as an alternative explana-tion for the pattern in Table 1.

Litvin and Syroechkovskiy (1984) stated thatfemales sometimes encountered insurmount-able difficulties if eggs became stuck in de-pressions or if the nest structure was too high.However, Prevett and Prevett (1973) reportedsuccessful retrieval regardless of nest-site veg-etation or nest-cup height, citing a case wherea goose rolled an egg up a 12-cm incline afterrepeated attempts. We analyzed nest-cupheight, denned as the distance from lip to theexterior base of the nest, as a predictor ofretrieval success in experiments reported pre-viously, in part, by Lank et al. (1989b). Singleeggs were placed 1 m from nests, and theirstatus was determined 24 h later. Retrievalsuccess was lower at taller nests [Figure 1;logistic regression, using nest-cup height as apredictor of retrieval success or failure: n =104, x2 = 7.18, df = 1, p = .007 (BMDPprogram logistic regression: Dixon, 1985)].Seven of the 28 eggs not retrieved in this sam-ple had actually moved farther away from thenest, probably as an inadvertent result of re-trieval attempts (Bousfield MA, personal ob-servations). Neither the nesting female's age,culmen length, nor the egg's weight predictedthe probability of egg retrieval in these ex-periments (multiple logistic regression, p >.2). (The curious bimodal relationship be-tween clutch size and probability of egg re-trieval reported by Lank et al. (1989b) was aspurious consequence of covariation betweenclutch size and nest-cup height in the sample;clutch size was not a significant predictor ofegg retrieval once nest height was controlledfor [logistic regression, three clutch-size cat-egories (Lank et al., 1989b): n = 101, clutch-size term: x2 = 2.50, df = 2, p = .29].)

Egg-retrieval probability decreases with dis-tance from the nest. Most eggs within about1 m are retrieved, whereas very few are re-trieved from 2 m (Lank et al., 1989b; Litvinand Syroechkovskiy, 1984; Prevett and Prev-

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ett, 1973; Syroechkovskiy, 1979). One possi-ble reason for that is the probability of suc-cessfully manipulating an egg over such adistance may be small in typical nesting situ-ations. Another explanation is that the prob-ability that the egg was laid by the host clearlydecreases with increasing egg-nest distance.In dense nesting areas, eggs 2 m from a nestcould actually be closer to a neighbor's nest.Thus, the decreased retrieval probability withdistance could be interpreted as discrimina-tion against probable nonparental eggs. If nestprotection is important, the predation risk tothe nest due to avian predators should sub-stantially decrease with distances greater than1 m. We have insufficient data to test thisprediction. Retrieval probability as a functionof distance could reflect the joint action ofchanging predation risk and the probabilitythat the egg being retrieved was not laid bythe nesting female.

Do snow geese discriminate against para-sitic eggs when egg-nest distance is controlled?In the 1-m displacement experiment de-scribed above, females failed to retrieve nearlyone-quarter of their own eggs. If half the par-asitic eggs are laid outside nests (Lank et al.,1989b), and 7% of all parasitic eggs remainoutside (Lank et al., 1990), then about 86%of parasitic eggs laid outside nests are adopt-ed, which is more than those retrieved in thisexperiment. In observed cases (Gurtovaya,1990; Mineau P, personal communication),parasitic eggs were nearly always laid closerthan 1 m from the nest, and this would in-crease their adoption rate if no discriminationoccurred. Our evaluation of the selective re-gime does not predict strong selection favor-ing egg recognition in this species. We haveno observations of egg rejections by hosts af-ter experimental supplementation of clutcheswith foreign eggs (Cooke F, unpublished data).

In summary, observational and experimen-tal results suggest that geese have limited abil-ities to manipulate eggs. The lowered proba-bility of retrieval with increasing distance fromthe nest may reflect the reduced probabilitythat more distant eggs were laid by the nestingbird and may reflect behavioral limitations ofegg-manipulation ability. Although individualvariation in retrieval motivation or discrimi-nation against parasitic eggs may exist, neitherappears necessary to account for variation inthe observed patterns of egg-rolling behavior.

Egg adoption in other taxa

Egg adoption by nesting males has been de-scribed for numerous species of fish. Severalhypotheses have been advanced to account forthis, and we briefly consider their relevanceto geese. Coyne and Sohn (1978) suggested

0.0

0.0 2.5 5.0 7.5 10.0 12.5 15.0 17.5

Nest cup height (cm)

that adoption in fish is a nonadaptive conse-quence of egg retrieval in general (our hy-potheses 1 and 4), which we reject for geese.A male might directly enhance his reproduc-tive success by adopting eggs (our hypothesis2) if holding a nest site with eggs dilutes thechances of predation on its own young (Mac-Kaye and MacKaye, 1978; Rohwer, 1978) orif the presence of eggs increases the proba-bility of obtaining additional spawnings by fe-males (Constantz, 1985; Ridley and Rechten,1981; Rohwer, 1978; Unger and Sargent,1988). Dilution of predation probability is ap-parently not strong in snow geese, as the sur-vivorship of host eggs from parasitized nestsis lower than that in comparable unparasitizednests (Lank et al., 1989a, 1990). Adoptingeggs will not increase the number of eggs afemale lays, but one might speculate that fe-males are increasing their apparent clutch sizeto increase the level of paternal investment orthe chance of mate retention. This tactic isprobably not occurring in snow geese: divorceis exceedingly rare (Cooke and Sulzbach, 1978;Cooke et al., 1981), and time budgets of par-ents are similar across brood sizes (Lessells,1987). Thus, we doubt the applicability of thesehypotheses to snow geese.

Is the nest-defense hypothesis suggestedhere applicable to fish? In an analogous sit-uation to that suggested for geese, male fishwould probably eliminate a predator attrac-tant by consuming the extranest eggs, whichwe have suggested might also be beneficial forgeese. We know of no piscine situations anal-ogous to the situation in geese.

Where might we expect to find egg adop-tion in other species of birds? A source ofadoptable eggs must be readily available. Thissuggests colonial species or those in whichparasitic females are attempting to foster eggsinto nests. If hosts benefited from incubatingadditional eggs (sensu Eadie et al., 1988), onemight predict theft of eggs from neighbors,either by egg-rolling or carrying intact eggs

Figure 1The proportion of eggsretrieved as a function of theheight of the nest cup,categorized into 2.5-craclasses. Numbers above barsindicate sample sizes.

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in the bill (Brown and Brown, 1988; Trost andWebb, 1986). No example of such behaviorhas yet been reported.

We have argued that selection can favoradoption even if the host does not benefitfrom incubating more eggs, if such eggs rep-resent a threat to the nest when left outsideit. In addition to parasitic situations similar tothose described for geese, the nest-defensehypothesis could apply to cases of nearbyabandoned nests or eggs in a colonial species.Likely candidates are densely nesting speciesof penguins or other seabirds. Species ofcrested penguins occasionally "rake in" near-by eggs (Warham, 1975; Williams TD, per-sonal communication). In species in which eggsappear near nests due to parasitism attempts,the probability of adoption may be a functionof the costs to the host (Rohwer and Freeman,1989) and the host's alternative possibilitiesfor disposing of the eggs. In habitats with densecover, hosts might simply leave eggs by nests.Overwater-nesting species might roll eggs ad-jacent to the nest into the water, as do Amer-ican coots (Fulica americana) (Lyon B, person-al communication). With alternative methodsof egg disposal available, other species do notneed to resort to egg adoption as do snowgeese. It is hardly surprising that adoption isa relatively rare behavior in birds.

CONCLUSION

The action of parasites laying eggs adjacentto nests apparently threatens nest survival.Hosts usually counter this threat through eggadoption. Despite the difficulty in obtainingaccess to defended nests, parasites prefer suchsites to undefended sites, thereby minimizingthe risk of laying in failed or abandoned nests(Lank et al., 1989b, 1990). Egg adoption insnow geese is a method by which host geesecope with intraspecific nest parasitism as bestthey can, adding to those mechanisms pro-posed by Andersson and Eriksson (1982) andPower et al. (1989). Perhaps the most intrigu-ing aspect of this interaction is that the threatto host nest survival from predators is an ul-timate evolutionary force favoring parasitismas a reproductive tactic in this species. In theabsence of predators, laying adjacent to thenest might not result in incubation of parasiticeggs, and parasites would face the more riskyprospect of laying in unattended nests or themore difficult task of displacing females fromtheir nests.

Judy Smith started the egg rolling, so to speak. Ken Abra-ham, Graham Boag, Ric Cole, Nancy Flood, and BruceRattray helped collect data during the experiments. Nesthistories and fates have been gathered by a small army offield workers over the years. Comments by Charles Fran-

cis, Ian Jamieson, and John Eadie improved this paper.Research on breeding snow geese at La Perouse Bay hasbeen supported by the Natural Sciences and EngineeringResearch Council of Canada, the Canadian Wildlife Ser-vice, the Department of Northern and Indian Affairs, theManitoba Department of Renewable Resources, DucksUnlimited Inc., and Ducks Unlimited Canada. Our thanksto all of these people and institutions.

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