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Exposure of Endangered Mississippi Sandhill Cranes to Environmental Pollutants

by

Donald H. White
USGS Patuxent Wildlife Research Center
School of Forest Resources
The University of Georgia
Athens, Georgia 30602


INTRODUCTION
METHODS
RESULTS
SUMMARY
DISCUSSION AND CONCLUSIONS
REFERENCES

INTRODUCTION

The remaining wild population of endangered Mississippi sandhill cranes (Grus canadensis pulla) (Fig. 1) occupies about 7200 ha of pine-savannah habitat (Fig. 2) in coastal Mississippi. The area, now called the Mississippi Sandhill Crane National Wildlife Refuge, was established in 1975 as critical habitat for the bird. The U.S. Fish & Wildlife Service has released captive-reared birds there since 1980 as part of a restocking effort. The population in 1996 numbered about 102 individuals, of which about 76% was captive-reared stock.

Reproduction in the wild population of Mississippi sandhill cranes (MSC) has been low. Refuge biologists estimate that hatching success during 1982-1993 averaged only 36%. Only 51% of the eggs that were laid (138) were viable and only 12 fledglings were produced during the 12-year period (Scott Hereford, pers. comm.). Aside from poor reproduction, another major problem in wild MSCs has surfaced in recent years. In the last decade or so, 67% of adult cranes found dead that were necropsied had cancerous tumors that probably caused their demise. The nature of the tumors, all air sac-related, suggests exposure to a carcinogenic agent(s) via the air. No adult MSCs maintained in captivity at the Patuxent Wildlife Research Center, Laurel, Maryland, have developed cancerous tumors. At the Refuge, air sac-related tumors have only been found in wild birds ~4 years of age, suggesting a site-specific low level exposure rate.

The Refuge is bisected by Interstate Highway 10 (I-10) , and it is <16 km from an industrial complex at Pascagoula, Mississippi. Thus, the potential for exposure of the cranes to environmental contaminants is real. Because the nature and extent of that exposure is unknown, we surveyed likely contaminants in eggs that failed to hatch and in ambient air at the Refuge as a first step in assessing potential impacts.

METHODS

Ten nonviable eggs from wild nests were used in this study. Egg shells were disinfected and three separate swabs were taken for microbial tests from the albumin of each egg via a hole drilled in the shell. Nonviable eggs containing embryos were examined for gross morphology. Egg contents were apportioned into two lots for chemical analyses, one for organochlorine (OC) pesticides, PCBs, and lipid content and the other for dioxins (PCDD) and furans (PCDF). The lower limit of quantification was ~0.1 ng/g, wet mass, for pesticides and ~1 pg/g , wet mass, for PCDDs and PCDFs. Egg samples were analyzed for contaminants at the Patuxent Wildlife Research Center, Laurel, Maryland (White et al. 1994). Microbial tests on swab cultures were conducted at the National Wildlife Health Research Center, Madison, Wisconsin.

Using high-volume air samplers (Fig. 3) designed to simultaneously trap airborne particulates and vapor contaminants, we collected ambient air samples at two locations ~14.2 km apart during May-September 1991. To get an accurate profile of the contaminant burden in air over time, composite samples were taken bimonthly. Within each bimonthly period (15-16 days), four days were randomly selected for air sampling at each station; the machines were run for 24 hours during each session. This approach yielded two four-day composite samples per month per site. Air sampler flow rate averaged ~272 l/min and total volume of air sampled per 24-hr session averaged ~400 m3 . The sampling media were micro-quartz filters in combination with polyurethane foam plugs. Air samples were analyzed for PAHs, PCDDs, PCDFs, and selected coplanar PCBs at Alta Analytical Laboratory, Inc., El Dorado Hills, California, using California Air Resources Board method 428 (White and Hardy 1994).

Figure 1. Mississippi sandhill crane with chick. Photo courtesy of Jonathan Male, Patuxent Wildlife Research Center.

 

Figure 2. Pine-savannah habitat at the Mississippi Sandhill Crane National Wildlife Refuge, Gautier, Mississippi.

 

Figure 3. Air monitoring machine used to sample ambient air at the Mississippi Sandhill Crane National Wildlife Refuge, Gautier, Mississippi.

RESULTS

Egg samples: Tests for microbial contamination in egg contents were all negative. Two nonviable eggs contained late dead embryos, but neither had obvious abnormalities. Residues of OC pesticides in egg samples were present at background concentrations. Chlordane isomers, mirex, and DDE occurred in all samples (~70 ng/g) and dieldrin was found in seven samples (~40 ng/g). Five samples contained traces (~3.5 ng/g) of both hexachlorocyclohexane and HCB. Endrin was found in one egg at 1.9 ng/g. No other OC pesticides were detected in egg contents. Total PCBs in samples also were low, ranging from 10-132 ng/g; the toxic coplanar congeners (according to IUPAC) averaged <5% of the totals. In general, PCDD and PCDF residues in samples were low. The highly toxic isomer, 2,3,7,8-TCDD, occurred in six samples, but residues were ~ 0.6 pg/g in all instances. The highest dioxin/furan residues detected in an egg were 216 pg/g penta-CDD, 76 pg/g octa-CDD and 75 pg/g penta-CDF, resulting in a toxicity equivalent (TEQ), based on 2,3,7,8-TCDD, of 146 pg/g.

Air samples: There was no difference (P < 0.05) in air residue concentrations between sites, so we combined chemical analytical results from both monitoring stations. Mean monthly PCDD/PCDF residues were low overall (0.29 - 1.04 pg/m3) and were highest during the second half of August (1.04 pg/m3) and the first half of September (0.55 pg/m3). Neither 2,3,7,8-TCCD, penta-CDD, nor 2,3,7,8-TCDF was detected in air samples at the limits of quantification. Meteorological parameters, with the exception of precipitation, were fairly consistent throughout the study, and there was no significant correlation between PCDD/PCDF levels in ambient air and weather factors. Four of the seven coplanar PCB compounds analyzed occurred in air samples at background concentrations, averaging 1.41-2.45 pg/m3. There was no difference (P < 0.05) in mean total coplanar PCB residues over time, and there was no correlation of residues with weather parameters. Seventeen PAH compounds were detected at low concentrations in air samples, ranging from 2-3 ng/m3 . Consistently, the highest PAH residues were of phenanthrene, fluoranthene, and pyrene, but there was no difference in mean total PAH concentrations over time, nor were they correlated with meteorological phenomena. Moreover, there were no discernible trends in ambient air contamination for any of the four major chemical groups analyzed during the five-month sampling period. .

SUMMARY

The remaining wild population of endangered Mississippi sandhill cranes (Grus canadensis pulla) numbers about 102 individuals, of which about 76% is captive-reared stock. The cranes' sanctuary is bisected by I-10 and is located <16 km from an industrial complex. Historically, reproduction in the wild flock has been poor. During 1982-1993, hatching success averaged just 36% and only 12 chicks reached fledgling size. Also, 67% of adult cranes found dead during this period exhibited air-sac related cancerous tumors that probably killed them. Because the nature of the adversity suggests contaminants exposure, we surveyed pollutants in nonviable crane eggs and in ambient air at the Mississippi Sandhill Crane National Wildlife Refuge where the cranes live as a first step in assessing potential impacts. Ten nonviable crane eggs collected over two nesting seasons contained only background levels of organochlorine pesticides (<0.07 ppm) and coplanar PCBs (<0.005 ppm). Three eggs contained potentially harmful levels of PCDDs and PCDFs (23, 39, and 146, pg/g), based on 2,3,7,8-TCDD toxicity equivalents (TEQ). However, TEQs were not the aggregate cause of egg failure, because six failed eggs contained no PCDDs/PCDFs . Composite bimonthly air samples from two sites on the Refuge collected during spring and summer contained only background levels of PCDDs, PCDFs, coplanar PCBs, and PAHs. There were no discernible trends in air pollutants over time nor were pollutants correlated with meteorological parameters.

It is unlikely that the contaminants we surveyed in nonviable eggs and ambient air are responsible for poor reproduction or air-sac tumors in wild Mississippi sandhill cranes.

DISCUSSION AND CONCLUSIONS

All nonviable crane eggs analyzed contained residues of chlordane, mirex, and DDE, but concentrations were far below those thought to influence reproduction in other avian species (Hyde et al. 1973, Longcore et al. 1977, Stickel et al. 1979, Henny et al. 1984, White et al. 1988). Concentrations of PCBs in eggs also were probably below harmful levels. None contained the toxic coplanar congeners in sufficient amounts to cause reproductive problems reported for other avian species (Kubiak et al. 1989). Three crane eggs had TEQs (representing cumulative toxicity of PCDD/PCDF isomers) of 23, 39, and 146 pg/g. These levels were within the range (> 20-50 pg/g) where reproductive impairment was evident in wood ducks (White and Seginak 1994), but wood ducks may be more sensitive to PCDD/PCDF contamination than other species. Moreover, six crane eggs had TEQs <1 pg/g; thus PCDDs/PCDFs may have influenced egg failure in some instances, but was not the aggregate cause. Mississippi sandhill crane eggs suitable for laboratory examinations are rare. Because of the scarcity of material and the crane's endangered status, nonviable eggs when available in the future should be monitored for toxic pollutants.

It is unlikely that any of the compounds we monitored in ambient air during the five-month period were responsible for air-sac tumors in wild cranes, even though the prevailing winds blow from the direction of I-10 and the industrialized city of Pascagoula. In fact, most of the concentrations we detected were far below levels in ambient air reported for other studies (Eisler 1987, Rogers et al. 1988, Edgerton et al. 1989, Steer et al. 1990). Also, some of the more toxic carcinogens found in air (e.g., 2,3,7,8-TCDD) were either absent or were detected infrequently in minute concentrations. Meteorological factors were not correlated with air pollutants, probably because of the relatively stable weather conditions we encountered during summer.

REFERENCES

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Hyde, K.M., J.B. Graves, and F.L. Bonner. 1973. Reproductive success of mallard ducks fed mirex. J. Wildl. Manage. 37:479-484.

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Stickel, L.F., W.H. Stickel, R.D. McArthur, and D.L. Hughes. 1979. Chlordane in birds: a study of lethal residues and loss rates. In: Deichmann, W.B. (Ed.), Toxicology and Occupational Medicine, Elsevier/North-Holland, New York, pp 387-396.

White, D.H. and J.W. Hardy. 1994. Ambient air concentrations of PCDDs, PCDFs, coplanar PCBs, and PAHs at the Mississippi Sandhill Crane National Wildlife Refuge, Jackson County, Mississippi. Environ. Monit. Assess. 33:247-256.

White, D.H. and J.T. Seginak. 1994. Dioxins and furans linked to reproductive impairment in wood ducks. J. Wildl. Manage. 58:100-106.

White, D.H., W.J. Fleming, and K.L. Ensor. 1988. Pesticide contamination and hatching success of waterbirds in Mississippi. J. Wildl. Manage. 52:724-729.

White, D.H., C.P. Rice, D.J. Hoffman, and G.F. Gee. 1994. Environmental contaminants in nonviable eggs of the endangered Mississippi sandhill crane. Environ. Monit. Assess. 31:225-232.