Developmental Abnormalities in Wild Populations of Birds: Examples from Lesser Snow Geese (Chen caerulescens caerulescens)

Copyright q American Museum of Natural History 2003 ISSN 0003-0082

P U B L I S H E D B Y T H E A M E R I C A N M U S E U M O F N AT U R A L H I S T O RY

CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024

Number 3400, 14 pp., 13 figures March 27, 2003

Developmental Abnormalities in Wild Populationsof Birds: Examples from Lesser Snow Geese

(Chen caerulescens caerulescens)

R.F. ROCKWELL,1 B.M. PEZZANITE,2 AND P. MATULONIS3

ABSTRACT

Changes in the frequency of individuals with gross abnormalities can be used as an indicatorof changes in the occurrence of biologically significant levels of developmental toxicants in thehabitats of natural populations. The precise nature of the defects and their relative distribution canoften provide clues as to the type of contamination. Such inferences clearly require baseline dataon the frequency of such deformities, and that is the purpose of this paper. For Mid-continentlesser snow geese (Chen caerulescens caerulescens) nesting at La Perouse Bay, the current rateof gross external abnormalities among embryos and near-hatch goslings at hatch is 3.937 3 1024

per egg (95% confidence limits 1.7053 3 1024 to 6.507 3 1024) and is consistent with estimatesmade for other species in minimally or uncontaminated habitats. Among the abnormal specimens,however, the relative distribution of defects of the beak and eye is not consistent with rates ofspontaneous abnormalities reported for chickens. If the higher relative frequency of beak defectspersists in future or other geographic samples displaying overall levels of abnormalities higherthan our benchmark, then contaminants acting as type 1 teratogens should be suspected. Of thecompounds this increasingly agriculturally dependent species is exposed to, insecticides rather thanherbicides would be the more likely class of candidates. We urge others who may have similardata on other species to make it more broadly available since such benchmarks are crucial for theuse of birds as bioindicators of environmental conditions. To that end, we offer our web site as aplace where data on and images of abnormal specimens can be posted and, within certain con-straints, will curate submitted specimens.

1 Research Associate, Division of Vertebrate Zoology (Ornithology), American Museum of Natural History; Pro-fessor of Biology, The City College of CUNY. e-mail: [email protected]

2 Student, Division of Vertebrate Zoology (Ornithology), American Museum of Natural History. e-mail:[email protected]

3 Student, Division of Vertebrate Zoology (Ornithology), American Museum of Natural History. e-mail:[email protected]

2 NO. 3400AMERICAN MUSEUM NOVITATES

INTRODUCTION

Developmental abnormalities can resultfrom random accidents of ontogeny, singlemutations, inbreeding, nutritional constraints,climatic factors, or the action of compoundswith teratogenic effects (Romanoff, 1972). Aclear example of the teratogenic action of anenvironmental contaminant was seen at Kes-terson National Wildlife Refuge in 1983where embryos and hatchlings from 16% ofthe eggs of several aquatic bird species dis-played gross anatomical abnormalities (Hoff-man et al., 1988). These birds were occu-pying portions of the refuge where levels ofselenium were more than 100 times those incontrol areas (Ohlendorf et al., 1986, 1988;Hoffman et al., 1988). Similar situationshave been reported for the Great Lakeswhere, in 1988 for example, deformed em-bryos and hatchlings were found among 6–15% of Double-crested Cormorant (Phala-crocorax auritus) and 3–28% of CaspianTern (Sterna caspia) eggs sampled from sitesdisplaying elevated levels of persistent or-ganochlorine contaminants (PCDDs, PCDFs,PCBs, and DDEs) (Yamashita et al., 1993;Ludwig et al., 1995, 1996; Custer et al.,1999). Other such examples are summarizedin Fox et al. (1991b) and Rykman et al.(1998).

These exceptionally high rates of gross ab-normalities in aquatic bird species wereamong the first indicators that compoundsaccumulating in these habitats had reachedbiologically problematic levels. Since a mul-titude of compounds with potential terato-genic action persist or continue to accumu-late in the environment (e.g., McGinn, 2000;Officer and Page, 2000; Hoffman et al.,2001; Pimm, 2001), it is important to contin-ue monitoring a variety of wild populationsfor abnormalities. On the one hand, we needto be vigilant in monitoring the health of spe-cies. On the other hand, the detection of dif-ferences in abnormality rates among habitatsor of temporally changing rates of abnor-malities in general may serve as an earlywarning of biologically significant environ-mental deterioration (or improvement) ofspecific or general habitats. Using birds asbioindicators of environmental change has along and successful history (e.g., Peakall and

Boyd, 1987; Fox and Weseloh, 1987; Fox etal., 1991a, 1991b; Rykman et al., 1998).

In some cases, observed rates of deformityin suspected habitats can be compared tothose in less or putatively uncontaminatedcontrol areas. This was the approach taken atKesterson National Wildlife Refuge whererates of deformity in the contaminated areawere compared with those at an uncontami-nated control site, the Volta Wildlife Area(Ohlendorf et al., 1986, 1988; Hoffman et al.,1988). Similar spatial comparisons wereused, for example, in examining deformitiesand contaminants in Double-crested Cormo-rants, Herring Gulls (Larus argentatus) andboth Caspian and Forster’s Terns (Sterna cas-pia and S. forsteri) (Hoffman et al., 1987;Fox et al., 1991b; Gilbertson et al., 1991; Ya-mashita et al., 1993; Larson et al., 1996; Bluset al., 1998; Rykman et al., 1998).

Unfortunately, control sites as such maynot always be available. In some cases, theremay be no clear indication of what the po-tential contaminant is, so identifying an ap-propriate control site is simply not possible.Alternatively, the contaminants may be sowidespread that an uncontaminated (or evenless contaminated) site simply does not exist.While a correlation between rates of defor-mity and degree of contamination amongsites varying in assayed contaminants pro-vides some insights, results are complexsince sites often differ in which contaminantsare present. Further, assigning causality isusually complicated by the presence of com-plex mixtures of contaminants, often withspatially correlated concentrations (e.g., Ya-mashita et al., 1993; Geisy et al., 1994; Lud-wig et al., 1995, Nisbet, 1998; Custer et al.,1999).

As an alternative, rates of spontaneous ab-normalities occurring in the absence of ter-atogenic compounds could be used as pointsof reference for current estimates (Hays andRisebrough, 1972; Romanoff, 1972). Unfor-tunately, baseline rates from controlled stud-ies are not available for many species. Be-yond that, there is no guarantee that sponta-neous abnormality rates for model speciessuch as domestic chickens or for any speciesobtained under controlled conditions are ap-propriate reference points for populations ofvarious species in natural habitats.

2003 3ROCKWELL ET AL.: DEVELOPMENTAL ABNORMALITIES IN BIRDS

Abnormality rates can be estimated forspecies currently occupying natural habitats.Owing to the present state of the environ-ment, however, such ‘‘current’’ abnormalityrates may not reflect true baseline (no con-taminant) abnormality levels but rather serveas contemporary abnormality rate bench-marks. As noted by Fox et al. (1991b: 159),‘‘If the incidence and prevalence of thesemalformations were monitored routinely,they could serve as sensitive indicators of thepossible prevalence of biologically signifi-cant concentrations of developmental toxi-cants in the food chain.’’ Evaluations ofchanges among temporal samples of suchrates for Double-crested Cormorants havebeen used in this fashion to monitor changesin environmental conditions in the GreatLakes (e.g., Fox et al., 1991b; Larson et al.,1996; Rykman et al., 1998), although infer-ences with respect to causal linkage to spe-cific toxicants can again be complicated (e.g.,Ludwig et al., 1995, Nisbet, 1998; Custer etal., 1999). More generally, and at the veryminimum, an increase above a currently es-tablished benchmark rate would serve as anindicator that contamination has potentiallyreached a biologically critical level and suchan increase could be used to warrant (andpossibly justify funding of) direct screeningof chemical contamination.

Because species differ in sensitivity tocontamination (e.g., Ohlendorf et al., 1986,1988; Hoffman et al., 1988), the use of ab-normalities in birds as bioindicators of en-vironmental change requires data from a va-riety of species (Peakall and Boyd, 1987;Gilbertson et al., 1987). Unfortunately, suchbenchmark values are not available for mostwild populations primarily because the esti-mation of relatively rare events requires sam-ple sizes so large that specific studies to es-tablish benchmark abnormality levels wouldnot likely be mounted or funded. However,such benchmark estimates could be madewith little additional effort using data andspecimens collected as part of other largerand long-term studies (e.g., Threlfall, 1968;Austin, 1969; Smith and Diem, 1971; Ryderand Chamberlain, 1972; Gochfeld, 1975; No-gales et al., 1990; Craves, 1994; Volponi,1996; Custer et al., 1999). In addition to es-timating the benchmark rates, it is important

that such studies include detailed descrip-tions of the deformed specimens since thetypes of abnormalities can provide insight asto the identity of potential teratogenic agents(e.g., Landauer, 1967; Romanoff, 1972; Gil-bertson et al., 1976; Hoffman and Albers,1984; Hoffman, 1990).

In this paper, we present data on defor-mities in a wild population of Lesser SnowGeese (Chen caerulescens caerulescens,henceforth snow geese) nesting at La Pe-rouse Bay, near Churchill, Manitoba, Cana-da. These data were collected during a long-term ecological study of the species (Cookeet al., 1995). While these birds do not nestin an area that we know to be contaminated,they make extensive use of agricultural landsand industrialized coastal marshes during thewinter and on both fall and spring migra-tions. These areas are (and have been) ex-posed to a variety of pesticides, herbicides,fungicides, and industrial toxicants (e.g.,White et al., 1982; Flickenger and Bolen,1979). Nutrients and any associated contam-inants acquired by females feeding in latewinter and early spring in those areas aretransported north to the nesting grounds andthe stored nutrients are used in producingeggs (e.g. Ankney and MacInnes, 1978).Since any contaminants transferred to theeggs could act as teratogenic agents, our datarepresent the current benchmark status forthis wild population.

METHODS

Research on the breeding biology and pop-ulation dynamics of snow geese at La Pe-rouse Bay (58843.59N, 93827.89W) has beenongoing since 1969. Basic field proceduresare summarized in Cooke et al. (1995). Thisstudy uses data from three sets of collectionsmade during that study. As part of our gen-eral work, some nests each year were moni-tored daily, allowing, among other things, aprecise estimate of the frequency of eggs andnear-hatch goslings that were abandoned byparents who left the nesting area with theirsuccessful goslings. Abandoned eggs (pippedand not pipped) from those nests were col-lected the day after the hatched goslings left,and the precise status (e.g., infertile, embryo,near-hatch gosling) was recorded (set 1). A


larger number of less intensively monitorednests were visited irregularly until hatchingwas detected. Those nests (referred to thenas hatching nests) were revisited the next dayand all abandoned eggs (pipped and notpipped) were collected (set 2). In three years(1989, 1994, and 1995), 2 pipping eggs werecollected from each of approximately 100randomly selected and otherwise successfulnests each containing 4 pipping eggs (set 3).The hatching rate of pipping eggs from suchnests is sufficiently high (.99% per pippingegg; Rockwell, unpubl. data) that most of thespecimens would have left their nests hadthey not been collected. Embryos and near-hatch goslings from the three sets of collec-tions were preserved in 10% neutral forma-lin, transported to the American Museum ofNatural History, and transferred to 70% eth-anol.

Because the specimens were collected forother purposes, they were examined non-de-structively for gross external deformities.Following especially Romanoff (1972),Hoffman and Albers (1984), Ohlendorf et al.(1986), and Hoffman (1990), the specimenswere examined for gross abnormalities of theeyes (including anophthalmia, buphthalmia,cyclopia, exophthalmos, and microphthal-mia), legs and wings (e.g., micromelia, ame-lia, asymmetry, orientation, and duplication),feet (e.g., ectrodactyly and clubfoot), beak(asymmetrical, missing, reduced, crossed),brain (e.g., hydrocephaly and exencephaly)and any general abnormalities of the axialskeleton. A specimen was considered ‘‘ab-normal’’ for one or more of these featureswhen the defect was obvious to the nakedeye. Descriptions (including a general quan-tification of the extent of the defect) wererecorded for each abnormal specimen. Allabnormal specimens were photographed aspart of establishing a permanent record. Insome cases (see below), we supplementedour visual examination with X-rays.

Although focusing on easily identifiablegross anatomical defects underestimates thefrequency of total (including finer level) ab-normalities, the approach was used for con-sistency with previous literature (above) andto allow the examination of more specimensin the fixed time available for this portion ofa larger field ecology project. As long as the

same criteria are used for other samples, thedetection of changes in rates of gross abnor-malities and attendant inferences regardingpotential contamination will not be biased(cf. Fox et al., 1991b).

Confidence limits for the proportion of ab-normalities found among the collected spec-imens were calculated using sample size andthe F distribution following methods in Zar(1999). A modification of that method usingthe variance of products (see Barrowcloughand Rockwell, 1993) was used to calculatethe confidence limits of the proportion of ab-normalities rescaled to a ‘‘per egg present inthe nest at hatching’’ basis (see below).

RESULTS

We collected 890 abandoned embryos andnear-hatch goslings between 1987 and 1996(sets 1 and 2 above), of which 12 (all founddead) displayed gross external abnormalitiesof the types described above. This number ofabnormalities was too small to allow an eval-uation of temporal change, and the entire col-lection was pooled. The overall proportion ofthese gross external abnormalities is 1.348 31022 (95% confidence limits 0.069 3 1022 to2.328 3 1022). To standardize this to a ‘‘peregg’’ basis, we used an estimate of the pro-portion of eggs present in the nest at hatchingthat were abandoned either as near-hatchgoslings, pipped eggs, or unpipped eggs con-taining embryos. This estimate is 2.919 31022 (with 95% confidence limits 2.485 31022 to 2.935 3 1022; n 5 6473; Cooke etal., 1995). Combining these, we arrive at anoverall estimate of 3.937 3 1024 (95% con-fidence limits 1.7053 3 1024 to 6.507 31024) as the proportion of eggs displayingobvious external abnormalities for this pop-ulation of lesser snow geese. Note that thisrescaling is with reference to the number ofeggs present in the nest at hatching, a valuesomewhat less than the number of eggs ini-tially laid (see Cooke et al., 1995).

It is possible that scavengers might re-move abandoned eggs and near-hatch gos-lings from hatching nests before we couldrevisit them. This could reduce the totalnumber of abnormalities found and result inunderestimation of the true abnormality rate,especially if, for some reason, abnormal


abandoned eggs and near-hatch goslingswere removed preferentially. To examine thepotential magnitude of this bias, we analyzeddata from a set of daily monitored nestswhere all eggs were marked, and on the daythe nest was considered to be ‘‘hatching’’ allbut one of the eggs was pipped. Revisitingthe nest the next day, we found that themarked, originally unpipped egg was missingin fewer than 1% of the cases (n 5 324;Rockwell, unpubl. data). Thus, althoughscavenging of abandoned eggs may causeour estimate of abnormality rate to be re-duced, we think the extent of the effect isminimal.

Our estimate would also be smaller thanthe true benchmark rate for the gross defor-mities we are scoring if some hatchlings withthose deformities left the nesting area withtheir parents. To examine this, we scored thenear-hatch goslings removed from the pippedeggs collected from otherwise successfulnests (set 3 above) for the same deformitiesassessed in the 890 abandoned embryos andnear-hatch goslings. Among the 624 near-hatch goslings examined, we found none ofthese deformities. Although a larger sampleof these ‘‘controls’’ might have shown an ab-normality rate slightly above 0, we think thatour estimate of 3.937 3 1024 per egg in thenest at hatching does not seriously underes-timate the true rate of these gross abnormal-ities for this population of lesser snow geesefor the period 1987–1996.

Photographs and brief descriptions of eachdeformed individual are provided in figures1 through 13. We provide a more detaileddescription in the following. Except wherenoted, none of the specimens had pippedtheir egg shell and all other aspects of eachspecimen was normal.

LPB001 (fig. 1). This multilimbed embryois approximately 75% the size of a hatchlingand has numerous deformities. It is missingthe posterior portions of the frontal bones,the majority of the parietal and squamosalbones, and the bulk of the occipital complexproximal to the foramen magnum. Whetherthese skull ‘‘defects’’ reflect true deformitiesor simply incomplete ossification related to ayounger age (assumed from size) is notknown. There are two separate upper man-dibles with the right one being half the length

of the left. The lower mandible is also du-plicated but fused medially. It is the samelength as the left upper mandible. There aretwo normal-sized eye sockets and eyes on thelateral sides of the head and a single fusedmedial socket in the front of the skull thatcontains two eyes. The specimen displays ex-treme scoliosis. The left- and rightmost legsare near normal. The central third ‘‘leg’’ iscomprised of separate, normal feet and tar-sometatarsi. Proximal to the lateral condyle,there are two separate tibiotarsi that are en-cased in a single skin sheath. Because we didnot wish to destroy the specimen to make astained skeletal preparation, we examinedLPB001 further with X-rays. From those (fig.2), it is clear that there are two vertebral col-umns, two femurs, and the bulk of two pelvicgirdles. Interestingly, there is no indicationof more than two wings. Broom (1897) re-ported on a chick with four legs and wingswhich, upon dissection, revealed the pres-ence of two complete vertebral columns.Diard (1897), in contrast, reported on a four-legged duck which possessed only one ver-tebral column. In that case, the second pairof (stunted) legs originated directly from thevertebral column, immediately anterior to thefirst caudal vertebra. Tornier (1901) also re-ports on several multilegged chicks andducks that have single vertebral columns.

LPB002 (fig. 3). This hatchling-size spec-imen displays duplication of both upper andlower mandibles with the lower ones beingmedially fused except for the most distal25% of their length. There are two normal-sized eye sockets and eyes on the lateralsides of the head and a single fused medialsocket in the front of the skull that containstwo eyes. X-ray evaluation reveals no ver-tebral column duplication posterior to theskull (fig. 4).

LPB003 (fig. 5). The fully formed left eyehas developed external to the cranial socket(monoexophthalmos). A sibling of this indi-vidual was also abandoned but displayed noabnormalities. Both the specimen and its sib-ling had pipped their shells.

LPB004 (fig. 4). The upper and lowermandibles are symmetrically reduced to ap-proximately 65% of their normal size.

LPB005 (fig. 7). This specimen displaysseveral deformities. Both feet are clubbed,


Fig. 1. Multilimbed embryo (LPB001) that also displays numerous deformities of the head. Ventral(left) and dorsal (right) views of the head region.

with the left being more extreme. The thirddigit of the left foot includes only a terminalphalanx, while the second and fourth digitsare reduced in overall length by approxi-mately 50%. The digits of the right foot arereduced in overall length to approximately50%. The distal portion of both tarsometa-tarsi are rotated so the feet are oriented in-ward by nearly 908. The head (not shown) isasymmetrical, with the left eye socket dis-placed anteriorly toward the beak with an ap-parent reduction in the anterior portion of theleft frontal bone. The upper and lower man-dibles are rotated 458 to the specimen’s rightand are slightly crossed.

LPB006 (fig. 8). The lower mandible isreduced to approximately 25% of normalsize. Its tip is asymmetrical, being both largeron the right and rotated outward in that di-rection. The upper mandible is of normallength but the nasal apertures are raised fromthe surface.

LPB007 (fig. 9). The upper and lowermandibles are reduced to approximately 25%of their normal size and are slightly crossed.They have a pyramidal shape.

LPB008 (fig. 10). The head is asymmet-rical with a reduction in the left anterior fron-tal bone and expansion of the right posteriorfrontal and right squamosal bones. The upper


Fig. 2. X-ray of LPB001 showing duplication of vertebral structures.

and lower mandibles are symmetrically re-duced to approximately 75% of normallength.

LPB009 (fig. 11). The lower mandible isreduced to approximately 50% of normallength, with the tip asymmetrically large on

the left. The anterior frontal bones are slopedrather than rounded, making the specimenseem to have no forehead.

LPB010 (fig. 12). The specimen is missingthe parietal, occipital complex, and posteriorportions of the squamosal bones of the skull.


Fig. 3. Specimen LPB002 displaying duplication of mandibles and fusion of medial eye socket.Entire specimen (left) and details of head region (right).

Fig. 4. X-ray of LPB002 showing that thereis but a single vertebral column.

Prior to preservation, more than 30% of thebrain was externalized.

LPB011 (fig. 13). Both upper and lowermandibles are reduced to approximately 50%of normal length. The specimen had pippedits shell.

LPB012 (not shown). This abandoned em-bryo was approximately 50% normal sizeand decayed. The lower mandible was onlyapproximately 75% the size of the uppermandible.

DISCUSSION

The rate of gross external abnormalitiesamong snow geese at La Perouse Bay is3.937 3 1024 per egg (95% confidence limits1.7053 3 1024 to 6.507 3 1024). This valueis near the upper end of the range of rates(8.0 3 1026 to 4.8 3 1024) reported for sim-ilar deformities among California Gulls (La-rus californicus), Herring Gulls, and SootyTerns (Sterna fuscata) sampled in putativelyuncontaminated habitats (Threlfall, 1968;Austin, 1969; Smith and Diem, 1971). It isalso within the range of abnormality rates re-


Fig. 5. Externalized eye of specimen LPB003.

Fig. 6. Symmetrically reduced mandibles ofspecimen LPB004.

ported for double-crested cormorants (0 to5.7 3 1024) from putatively minimally or un-contaminated reference sites (Fox et al.,1991b; Rykman et al., 1998). Note that all ofthese other estimates were based only on ab-normalities observed among surviving hatch-lings and near-fledging juveniles. Owing tomortality associated with abnormalities inembryos and near-hatch juveniles (classesexcluded in their estimates but included inours), their estimates are expected to be low-er than ours, and even more so for the dou-ble-crested cormorants that included onlybeak defects (Fox et al., 1991b). Allowingfor this, our estimate certainly falls within therange expected for minimally or uncontami-nated habitats.

Consistently, our estimate is substantiallybelow the rates of 1.0 3 1023 to 1.3 3 1022

gross external abnormalities per egg reportedfor Common and Roseate Terns (Sterna hi-rundo and S. dougalli) sampled off the east-ern tip of Long Island and estimated at a timewhen chemical contamination was suspectedin the area (Hays and Risebrough, 1972). Itis also well below the estimates of 1.5 3 1022

and 2.5 3 1022 gross abnormalities per eggfor Double-crested Cormorants and CaspianTerns, respectively, calculated from data onthe same abnormalities we scored that waspresented in Ludwig et al.’s (1996) study ofthe effects of chemical contamination onthese species in the Great Lakes. These com-parisons have the advantage that the data,

like ours, included abnormalities among em-bryos and near-hatch juveniles. Even thoughour estimate for the rate of gross external ab-normalities is well below that for a contam-inated habitat and within the range of ratesexpected for minimally or uncontaminatedhabitats, we prefer to view our estimate as acurrent benchmark rather than a true, con-taminant-free baseline value for this species.Given the agricultural areas where snowgeese winter and forage in the spring and fall(Jefferies et al., 2002), it is possible thatsome level of contaminants are carried northbut appear to be below any threshold of bi-ological (teratogenic) impact.

Even though the abnormality rate for snowgeese appears to lie within a range consistentwith minimal contamination, the distributionof the types of gross abnormalities is curious.Among the 12 abnormal specimens, there are10 defects involving the beak and only 4 in-volving the eye (this includes defects in bothfor 3 specimens with multiple abnormalities).This is in marked contrast to the relative dis-tribution of spontaneous occurrences of thesegross deformities in chickens, where beakdeformities are only half as frequent as eyedeformities (Romanoff, 1972). Whether thisis a species-specific difference cannot beknown until spontaneous rate data for morespecies are available. In the interim, however,note that although the current rate of abnor-mality for snow geese is not sufficient to in-fer the presence or action of toxicants, an ex-cess of bill deformities was reported for dou-


Fig. 7. Clubbed feet of specimen LPB005.

Fig. 8. Asymmetrically reduced lower man-dible of specimen LPB006.

Fig. 9. Symmetrically reduced mandibles ofspecimen LPB007.

ble-crested cormorants in the Great Lakesduring a period where contamination was el-evated at several locations (cf. Fox et al.,1991b). Defects involving the beak and notthe eye are often a product of type 1 terato-genesis (Hoffman, 1990) and for agricultur-ally related compounds are reported morefrequently in association with the action ofinsecticides (especially organophosphateones) than herbicides (Hoffman and Albers,

1984). Future studies should closely monitorthe relative distributions of types of abnor-malities as well as assess any change in therate.

Our primary purpose was to establish acurrent benchmark of gross abnormalities forlesser snow geese to which future estimatesfrom this or other geographically distinctnesting populations of this species could be


Fig. 10. Skull abnormalities of specimenLPB008.

Fig. 12. Externalized brain of specimenLPB010 that is missing several bones of the skull.

Fig. 11. Asymmetrical reduction in lowermandible of specimen LPB009 that also displaysmisshapen anterior frontal bones.

Fig. 13. Symmetrically reduced upper andlower mandibles of LPB011.

compared. Assuming data are collected in thesame fashion, those comparisons would bestatistically more powerful if based simplyon the rate of abnormalities among aban-doned embryos and near-hatch goslings athatched nests since the rescaling to a per eggbasis requires incorporating the sampling er-ror associated with the conversion factor (seeMethods). Given this and using the upper95% confidence limit of the estimate of ab-normalities per abandoned embryo and near-hatch gosling of 2.328 3 1022 as a point ofreference, it can be calculated that findingonly 36 abnormal specimens for the samesample size of 890 would be sufficient toyield an estimated abnormality rate (4.044 31022) that would be significantly higher thanthe current benchmark of 1.348 3 1022. Us-ing a smaller sample size of 100 abandonedembryos and near-hatch goslings would re-quire finding 7 abnormal specimens and a

rate of 7 3 1022 to demonstrate a significantincrease.

In either case, it would be reasonable toinfer that some factor or set of factors hadchanged over time or differed between thesamples. The most likely candidates wouldinclude increased inbreeding, decreased (oraltered) nutritional status of the female pro-ducing the eggs, altered climatic factors, orthe increases in toxicant(s) above a thresholdof teratogenic action (Romanoff, 1972; Foxet al., 1991b). For this species, populationlevels are so high (Abraham and Jefferies,1997) and gene flow is sufficient (Rockwelland Barrowclough, 1987) that inbreeding is


not likely to become a problem. Climaticchanges would most likely require depres-sions of temperature (Romanoff, 1972),changes that are inconsistent with currenttrends and projections for the Hudson Bayand Foxe Basin regions (Skinner et al.,1998). Part of the explosive growth of theMid-continent population of lesser snowgeese is related to an increasing nutritionalsubsidy the birds are acquiring through in-creased use of agricultural areas of the Mid-west (Jefferies et al., 2002). Unless currentagricultural practices are greatly altered, it isunlikely that female snow geese arriving inthe Hudson Bay and Foxe Basin region ofCanada will suffer nutritional deficits.

This increased use of agricultural lands forwintering and both spring and fall staging is,however, the potential route for increased ex-posure to and dietary intake of agriculturalcompounds (e.g., pesticides, fungicides, andherbicides) that could reach levels in eggsthat would be reflected in increased rates ofgross developmental abnormalities. For thisspecies, then, significant increases (or differ-ences with respect to other colonies) in therates of gross abnormalities among embryosand near-hatch goslings abandoned athatched nests should trigger a serious con-sideration of toxicant screening with a spe-cial emphasis on agriculture-related com-pounds. If the high proportion of beak ab-normalities persists, then compounds withknown type 1 teratogenic action such assome organophosphate insecticides should beinitially suspected.

Our more general goal is to encourage oth-ers to follow Fox et al.’s (1991b) suggestionto collect and use data on abnormalities as abio-monitoring tool to assess changes in en-vironmental conditions that are sufficient tohave biological impact. As part of that, it islikely that there are data that will provideestimates of deformity rates hidden in thefield notes of many researchers and likely inthe unpublished reports of many federal,state, provincial and nongovernmental orga-nizations. Part of our purpose here is to en-courage those in possession of such data toeither publish them or at least make themavailable to a broader audience. It is our viewthat by compiling data, even from studiesthat in and of themselves are too small to

publish formally, we will accumulate a da-tabase of historic and current deformity ratesthat will aid in a variety of conservation andmanagement issues. To that end, we offer ourweb site (http://research.amnh.org/users/rfr/hbp) as a place where such data and imagescan be submitted. They will be posted andmade available to anyone interested. Whenpublishing or submitting such data, it is im-portant to either scale the rates to a commonbasis (e.g., deformities per egg) or clearly in-dicate the basis. It is also crucial to includesample sizes or estimates of confidence lim-its.

With certain limitations, we are also will-ing to curate and store specimens displayingabnormalities. Like all specimens at theAmerican Museum of Natural History, they,like the ones reported here, will be availablefor examination to all bona fide researchers.Owing to U.S. Federal regulations, Interna-tional Treaties and AMNH policies, donatedspecimens must have been collected and, ifapplicable, exported under valid permits.Copies of all relevant documents, includingcollecting and exportation permits and a let-ter donating the specimens to the AmericanMuseum of Natural History, must be provid-ed. To avoid problems, it is essential that webe contacted before any specimens areshipped.

ACKNOWLEDGMENTS

We appreciate comments from Ken Abra-ham, Graham Cooch, Paul Flint, Glen Fox,Helen Hays, David Hoffman, and Pierre Mi-neau. This work was done under the auspicesof the Hudson Bay Project and with the co-operation of Wapusk National Park. Fundingfor the Hudson Bay Project is provided inpart by the Arctic Goose Joint Venture, theCentral and Mississippi Flyway Councils, theDepartment of Indian and Northern Affairs(Canada), Ducks Unlimited, the City Uni-versity of New York, and the Olive BridgeFund.

REFERENCES

Abraham, K.F., and R.L. Jefferies. 1997. Highgoose populations: causes, impacts and impli-cations. In B. Batt (editor), Arctic ecosystemsin peril: report of the Arctic Goose Habitat


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Documents

Developmental Abnormalities in Wild Populations of Birds: Examples from Lesser Snow Geese (Chen caerulescens caerulescens)