SOME PARASITIC AND INFECTIOUS DISEASES IN WATERFOWL IN OKLAHOMA Author(s): A. ALAN KOCAN, MICHAEL G. SHAW and PATRICK M. MORGAN Source: Journal of Wildlife Diseases, 15(1):137-141. Published By: Wildlife Disease Association DOI: http://dx.doi.org/10.7589/0090-3558-15.1.137 URL: http://www.bioone.org/doi/full/10.7589/0090-3558-15.1.137
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal
of Wildlife
SOME
Diseases
Vol.
PARASITIC
WATERFOWL
15, January,
AND IN
1979
137
INFECTIOUS
DISEASES
IN
OKLAHOMA0
A. ALAN KOCAN, MICHAEL G. SHAW and PATRICK Microbiology and Public Health, College of Veterinary Oklahoma, 74074, USA.
M. MORGAN, Medicine,
Department Oklahoma
of Veterinary State University,
Parasitology,
Stiliwater,
Abstract: Blood films and serum samples from free-ranging waterfowl wintering in and migrating through Oklahoma were examined for hematozoa and tested for antibody responses to Newcastle disease virus (NDV) and type-A influenza. Onehundred-eleven of 728 birds (15.24%) were positive for 1 or more hematozoa. Serologic testing revealed 11 of 280 (3.93%) positive for antibody to NDV and 5 of 171 (2.95%) positive for antibody to type-A influenza.
INTRODUCTION
serologic analysis was taken from the brachial vein of all birds. Blood films were stained with Giemsa stain and examined at l5OX and under oil immersion (l000X). Sera were screened for Newcastle disease virus (NDV) antibody by the hemagglutination-inhibition (HI) test. All HI reactants (titers of 1:2 or higher) were retested before being considered positive. Sera were screened for antibody to type-A Influenza using the agar gel precipitin test (AGP).’ Serologic testing was done only on selected samples and, as a result, the number of birds screened varied for each test.
Prevalence data on serologic activity to selected pathogens and on hematozoan parasites of migratory waterfowl are available from many locations in North America. 1,2,6,7,8,10,11,14,15,16,17,8 Little information is available, however, on these parameters from wintering populations or waterfowl from the Central Flyway. The purpose of this study was to determine the antibody response to selected infectious diseases and the prevalence of hematozoa in waterfowl migrating through and wintering in Oklahoma.
MATERIALS
AND
METHODS
RESULTS
Free-ranging waterfowl wintering in and migrating through Oklahoma were examined for hematozoa and for serologic activity to Newcastle disease virus (NDV) and type-A influenza. Samples were taken between the months of October and April, 1974-77. All birds were live trapped of a rocket net at Salt Plains Wildlife Refuge (NWR), Jet, Washita NWR, Hammond, and Ham’s Lake, Stillwater, Blood used for thin films 0] Supported University.
in
part
The results of the examination of 728 blood films from free-ranging waterfowl are shown in Table 1, One-hundred-eleven birds of 5 species harbored one or more species of blood parasite, a prevalence of 15.25%. Leucocytozoon simondi, Plasmodium (0.27%), Haemoproteus nettionis (7.14%) and microfilariae (1.09%) were identified. Concurrent infections of L. simondi and H. nettionis occurred in 1.2% of the cases.
the aid National Oklahoma, Oklahoma, Oklahoma. and for Institute
DISCUSSION
Hematozoa
with
by the Environmental
AND
and
the College
of Veterinary
Medicine,
Oklahoma
State
Journal
138
TABLE
1. Hematozoa
fro m wild
Species
*Due
to mixed
number
of positive
Vol.
15. January.
1979
1 in Oklahoma Number Positive
Percent Positive
402
75
18.7
42 35
1
6
104
15
14.4
4 11
1
0
58
5
8.6
2
3 0
0
49
14
28.6
4
9 0
1
11
0
0.0
0
0 0
0
5
0
0.0
0
0 0
0
98
2
2.0
0
1 0
1
1
0
0.0
0
0 0
0
728
H = L = P = M = infections,
Diseases
Number Examined
Mallard (Anas platyrhynchos) American widgeon (Anas americana) Blue-winged teal (Anas discors) Green-winged teal (Anas crecca) Pintail (Anas acuta) Wood duck (Aix sponsa) Canada goose (Branta canadensis) Snow goose (Anser c. caerulescens) TOTALS Abbreviations:
waterfow
of Wildlife
Haemoproteus Leucocytozoon Plasmodium Microfilaria the sum
111
H
L
52 60
P M
2
8
nettionis simondi sp. of the individual
infections
may
be greater
than
the
birds.
Studies conducted in other regions of North America have, with a few exceptions, shown a higher overall prevalence of hematozoa.6’7”#{176}”2”” In the only other study of hematozoa from waterfowl in the Central flyway, however, Stabler et al.’7 reported a 27% infection in birds they examined. Although the prevalence of hematozoa in waterfowl in Colorado is higher than that observed in Oklahoma, the difference is not appreciable and may be the result of a slightly different period at sampling. In a discussion of the frequency and distribution of avian hematozoa by host family, Greiner’ determined that Haemoproteus is the most frequent hematozoan parasitizing the Anatidae. In the present study, however, Leucocytozoon occurred with the
greatest frequency (8.24%). Stabler et al.2#{176} reported similar findings in waterfowl in Colorado. It appears that Leucocytozoon is more prevalent than Haemoproteus in the Central Flyway, however these data represent only 3 years of observation and prevalence of various species of hematozoa may fluctuate from year to year or be influenced by the time of year that the samples are taken. Green-winged teal was the species most frequently infected with one or more hematozoa (28.6%). Mallards and American widgeons followed in order of prevalence with 18.7% and 14.47%, respectively. Among the ducks, the bluewinged teal was least frequently infected (8.6%), while the Canada goose showed the lowest overall percentage of infection
Journal
of Wildlife
Diseases
Vol. 15, January,
1979
139
(2.0%). Although many factors could account for differences in prevalence among the species examined, one of the most likely is nest site selection. Bennett5 found that Simulium rugglesi, an important vector of Leucocytozoon, prefers to feed within 13 m of the shoreline and that feeding activities rapidly decrease beyond that point. Ducks selecting nest sites nearer the water would, therefore, be selectively exposed to the vector. Mallards and American widgeons are known to nest closer to the water than pintails and blue-winged teal.4 Differences in the prevalence of L. simondi in the species of ducks examined in the present study appears to correlate with nest site selection and apparent accessibility of the host to the vector. The low prevalence of hematozoa in Canada geese examined during this study suggests that they occupy a habitat unfavorable for contact with large vector populations. The nesting range for many of the Canada geese in central Oklahoma is largely confined to coastal habitat in the eastern Canadian Arctic.4 Greiner et al.’ refers to this area as the Arctic barrens, and found that a low overall prevalence of infection occurred in this region, a finding they attributed to a lack of vector activity.
Bennett et al.7 suggested that the epizootiology of hematozoa in anatids appears to be a complex interaction involving host behavior, habitat and vector activity. As a result, interpretations of findings at any point within the life of the birds must include an analysis of the total biology of both the host species and parasites involved.
Antibody Influenza
to NDV
Newcastle
Mallard (Anas
Type-A
Eleven of 280 serum samples tested by HI were positive for antibody to NDV (Table 2). Five of 156 mallards (3.21%), 5 of 87 Canada geese (5.75%) and 1 of 37 American widgeons (2.70%) were serologically positive. These findings differ from studies conducted in other flyways which report a higher percentage of serum samples containing antibody to NDV and a higher percentage of isolations of NDV. ,8,14,l5,16 The differences in the findings of this study might be explained by the absence of large poultry flocks in Oklahoma and much of the Central Flyway, such as are found in California, Michigan, Minnesota, Arkansas, and other poultry producing states in the Atlantic, Mississippi and Pacific flyways. Since domestic fowl are known to be more
TABLE 2. Prevalence of Antibody to Newcastle Disease enza in Sera from Wintering Waterfowl in Oklahoma.
Species
and
Disease Virus
Virus
and
Type-A
Influ-
Type-A Influenza
platyrhynchos)
5/156 (3.21%)
3/122 (2.45%)
American widgeon (Anas americana)
1/37 (2.70%)
1/37 (2.70%)
Pintail (Anas
(tL0%)
0/5 (0.0%)
5/87 (5.75%)
1/7 (14.28%)
Canada (Branta TOTALS
0/’5
acuta) goose
canadensis)
11/280 (3,93i)
5/171 (2.92%)
Journal
140
susceptible to Newcastle disease virus than are wild waterfowl,’ the lower number of positive serologic reactors may thus be explained by the lack of opportunity for exposure to a domestic source. Antibody to type-A influenza was detected in 5 of 171 birds examined. Three of 122 mallards (2.45%), 1 of 37 American widgeons (2.70%) and 1 of 7 Canada geese (14.28%) had antibody. The detection of antibody to influenza in serum samples collected from migratory waterfowl in Oklahoma is consistent with findings of other investigators in the Pacific, Mississippi and Atlantic flywnys.2”7”2#{176} Since all samples for
of Wildlife
Diseases
Vol.
15, January,
1979
this study were taken in the winter and early spring the serologic titers, if they reflect ongoing infection, indicate that waterfowl migrating through Oklahoma carry influenza infections throughout their migratory route or that transmission occurs during migration and/or on the wintering grounds. Although considerable insight into the epizootiology of infectious diseases can be gained by serologic studies, definitive statements concerned with the acquisition and perpetuation of these infections must await detailed studies designed to isolate and characterize the agents involved.
Ackhowledgements We wish to thank Dr. E.C. Greiner, International Reference Centre for Avian Haematozoa for his aid in parasite identification; Ms. Pat Franks for her technical assistance; and Mr. Howard Jarrell for his encouragement and support. We would also like to thank the personnel of Salt Plains NWR and Washita NWR for their assistance.
LITERATURE
CITED
1.
ASPLIN,
F.D.
2.
BAHL, AK., B.S. POMEROY, B.C. EASTERDAY and S. MANGUNDIMEDJO. 1975. Isolation of type-A influenza viruses from the migratory waterfowl along the Mississippi Flyway. J. WildI. Dis. 11: 360-363.
1947.
Newcastle
3.
BEARD, C.W. 1975. Avian influenza. In: Isolation pathogens. S.B. Hitchner, C.H. Domermuth, Williams, eds. Arnold Printing Co., New York.
4.
BELLROSE, Books,
5.
BENNETT, quin
F.C. 1976. Harrisburg, G.F. Park,
1960. Ontario,
disease
Ducks, geese, Pa. 543 pp. On some Canada.
in ducks
and
and
swans
geese.
of North
ornithophilic Can. J. Zool.
blood-sucking 38: 377-389.
HEUSMANN of the Atlantic
and A.G. Flyway.
, W. BLANDIN, H.W. Hematozoa of the Anatidae Wildl. Dis. 10: 442-451.
7.
, A.D. SMITH, W. WHITMAN and M. CAMERON. Anatidae of the Atlantic Flyway. II. The Maritime Wildl. Dis. 11: 280-289.
BRADSHAW, waterfowl
J.E. and D.O. in the Mississippi
9.
GREINER, E.C., G.F. Distribution of the 1762-1787.
TRAINER. Flyway.
Rec.
and Identification G.H. Purchase
6.
8.
Vet.
America. diptera
59:621-624.
of avian and J.E. Stackpole in Algon-
CAMPBELL. I. Massachusetts.
1975. Hematozoa of the Provinces of Canada. J.
1966. Some infectious diseases J. Wildl. Manage. 30: 570-576.
BENNETT, E.M. WHITE avian hematozoa of North
1974. J.
and F. America.
of
COOMBS. 197-5. Can. J. Zool, 53:
Journal
10. 11.
of Wildlife
HERMAN, Am. .
Diseases
Vol.
15, January,
1979
C.M. 1968. Blood Wildl. Nat. Resour.
1951.
Blood
parasites
141
parasites of North Conf. 33: 348-359. from
California
American
ducks
and
waterfowl. geese.
Trans.
J. Parasit.
N.
37:280-
282. 12.
NELSON, E.C. and J.S. GASHWILER. waterfowl. J. Wildl. Manage. 3: 119-205.
13.
O’MEARA, 207-209.
D.C.
14.
PALMER, disease
S.F. and D.O. virus in Canada
15.
ROSENBERGER, J.K., W.C. KRAUSS and RD. SLEMONS. 1974. Newcastle disease and type-A influenza viruses from migratory in the Atlantic Flyway. Avian Dis. 18: 610-613.
16.
, S. disease Avian
1956.
Blood
parasites
1941.
of some
Maine
Blood
parasites
waterfowl.
of
J. Wildl.
TRAINER. 1970. Serologic evidence geese. Avian Dis. 14: 494-502.
Maine Dis. 20:
of Newcastle Isolation waterfowl
of
KLOOP and W.C. KRAUSS. 1975. Characterization of Newcastle viruses isolated from migratory waterfowl in the Atlantic Flyway. Dis. 19: 142-149.
17.
STABLER, Colorado
R.M., N.J. KITZMILLER birds. V. Anseriformes.
18.
TRAINER, DO., CS. SCHILDT, of Leucocytozoon simondi Manage. 26: 137-143.
19,
WILLIAMS, of mallard Northwest
and O.W. J. Parasit. R.A. HUNT among some
OLSEN. 1975. 41: 148-149.
and L.R. JAHN. 1962. Wisconsin waterfowl.
NA., B.K. CALVERLEY and J.L. MAHRT. and pintail ducks from central Alberta and Teritories. J, Wildl. 1)is, 13: 226-229.
Received
for publication
Hematozoa
12 May
1978
from
Prevalence J, Wildl.
1977. Blood parasites the MacKenzie Delta,
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal
of Wildlife
SOME
Diseases
Vol.
PARASITIC
WATERFOWL
15, January,
AND IN
1979
137
INFECTIOUS
DISEASES
IN
OKLAHOMA0
A. ALAN KOCAN, MICHAEL G. SHAW and PATRICK Microbiology and Public Health, College of Veterinary Oklahoma, 74074, USA.
M. MORGAN, Medicine,
Department Oklahoma
of Veterinary State University,
Parasitology,
Stiliwater,
Abstract: Blood films and serum samples from free-ranging waterfowl wintering in and migrating through Oklahoma were examined for hematozoa and tested for antibody responses to Newcastle disease virus (NDV) and type-A influenza. Onehundred-eleven of 728 birds (15.24%) were positive for 1 or more hematozoa. Serologic testing revealed 11 of 280 (3.93%) positive for antibody to NDV and 5 of 171 (2.95%) positive for antibody to type-A influenza.
INTRODUCTION
serologic analysis was taken from the brachial vein of all birds. Blood films were stained with Giemsa stain and examined at l5OX and under oil immersion (l000X). Sera were screened for Newcastle disease virus (NDV) antibody by the hemagglutination-inhibition (HI) test. All HI reactants (titers of 1:2 or higher) were retested before being considered positive. Sera were screened for antibody to type-A Influenza using the agar gel precipitin test (AGP).’ Serologic testing was done only on selected samples and, as a result, the number of birds screened varied for each test.
Prevalence data on serologic activity to selected pathogens and on hematozoan parasites of migratory waterfowl are available from many locations in North America. 1,2,6,7,8,10,11,14,15,16,17,8 Little information is available, however, on these parameters from wintering populations or waterfowl from the Central Flyway. The purpose of this study was to determine the antibody response to selected infectious diseases and the prevalence of hematozoa in waterfowl migrating through and wintering in Oklahoma.
MATERIALS
AND
METHODS
RESULTS
Free-ranging waterfowl wintering in and migrating through Oklahoma were examined for hematozoa and for serologic activity to Newcastle disease virus (NDV) and type-A influenza. Samples were taken between the months of October and April, 1974-77. All birds were live trapped of a rocket net at Salt Plains Wildlife Refuge (NWR), Jet, Washita NWR, Hammond, and Ham’s Lake, Stillwater, Blood used for thin films 0] Supported University.
in
part
The results of the examination of 728 blood films from free-ranging waterfowl are shown in Table 1, One-hundred-eleven birds of 5 species harbored one or more species of blood parasite, a prevalence of 15.25%. Leucocytozoon simondi, Plasmodium (0.27%), Haemoproteus nettionis (7.14%) and microfilariae (1.09%) were identified. Concurrent infections of L. simondi and H. nettionis occurred in 1.2% of the cases.
the aid National Oklahoma, Oklahoma, Oklahoma. and for Institute
DISCUSSION
Hematozoa
with
by the Environmental
AND
and
the College
of Veterinary
Medicine,
Oklahoma
State
Journal
138
TABLE
1. Hematozoa
fro m wild
Species
*Due
to mixed
number
of positive
Vol.
15. January.
1979
1 in Oklahoma Number Positive
Percent Positive
402
75
18.7
42 35
1
6
104
15
14.4
4 11
1
0
58
5
8.6
2
3 0
0
49
14
28.6
4
9 0
1
11
0
0.0
0
0 0
0
5
0
0.0
0
0 0
0
98
2
2.0
0
1 0
1
1
0
0.0
0
0 0
0
728
H = L = P = M = infections,
Diseases
Number Examined
Mallard (Anas platyrhynchos) American widgeon (Anas americana) Blue-winged teal (Anas discors) Green-winged teal (Anas crecca) Pintail (Anas acuta) Wood duck (Aix sponsa) Canada goose (Branta canadensis) Snow goose (Anser c. caerulescens) TOTALS Abbreviations:
waterfow
of Wildlife
Haemoproteus Leucocytozoon Plasmodium Microfilaria the sum
111
H
L
52 60
P M
2
8
nettionis simondi sp. of the individual
infections
may
be greater
than
the
birds.
Studies conducted in other regions of North America have, with a few exceptions, shown a higher overall prevalence of hematozoa.6’7”#{176}”2”” In the only other study of hematozoa from waterfowl in the Central flyway, however, Stabler et al.’7 reported a 27% infection in birds they examined. Although the prevalence of hematozoa in waterfowl in Colorado is higher than that observed in Oklahoma, the difference is not appreciable and may be the result of a slightly different period at sampling. In a discussion of the frequency and distribution of avian hematozoa by host family, Greiner’ determined that Haemoproteus is the most frequent hematozoan parasitizing the Anatidae. In the present study, however, Leucocytozoon occurred with the
greatest frequency (8.24%). Stabler et al.2#{176} reported similar findings in waterfowl in Colorado. It appears that Leucocytozoon is more prevalent than Haemoproteus in the Central Flyway, however these data represent only 3 years of observation and prevalence of various species of hematozoa may fluctuate from year to year or be influenced by the time of year that the samples are taken. Green-winged teal was the species most frequently infected with one or more hematozoa (28.6%). Mallards and American widgeons followed in order of prevalence with 18.7% and 14.47%, respectively. Among the ducks, the bluewinged teal was least frequently infected (8.6%), while the Canada goose showed the lowest overall percentage of infection
Journal
of Wildlife
Diseases
Vol. 15, January,
1979
139
(2.0%). Although many factors could account for differences in prevalence among the species examined, one of the most likely is nest site selection. Bennett5 found that Simulium rugglesi, an important vector of Leucocytozoon, prefers to feed within 13 m of the shoreline and that feeding activities rapidly decrease beyond that point. Ducks selecting nest sites nearer the water would, therefore, be selectively exposed to the vector. Mallards and American widgeons are known to nest closer to the water than pintails and blue-winged teal.4 Differences in the prevalence of L. simondi in the species of ducks examined in the present study appears to correlate with nest site selection and apparent accessibility of the host to the vector. The low prevalence of hematozoa in Canada geese examined during this study suggests that they occupy a habitat unfavorable for contact with large vector populations. The nesting range for many of the Canada geese in central Oklahoma is largely confined to coastal habitat in the eastern Canadian Arctic.4 Greiner et al.’ refers to this area as the Arctic barrens, and found that a low overall prevalence of infection occurred in this region, a finding they attributed to a lack of vector activity.
Bennett et al.7 suggested that the epizootiology of hematozoa in anatids appears to be a complex interaction involving host behavior, habitat and vector activity. As a result, interpretations of findings at any point within the life of the birds must include an analysis of the total biology of both the host species and parasites involved.
Antibody Influenza
to NDV
Newcastle
Mallard (Anas
Type-A
Eleven of 280 serum samples tested by HI were positive for antibody to NDV (Table 2). Five of 156 mallards (3.21%), 5 of 87 Canada geese (5.75%) and 1 of 37 American widgeons (2.70%) were serologically positive. These findings differ from studies conducted in other flyways which report a higher percentage of serum samples containing antibody to NDV and a higher percentage of isolations of NDV. ,8,14,l5,16 The differences in the findings of this study might be explained by the absence of large poultry flocks in Oklahoma and much of the Central Flyway, such as are found in California, Michigan, Minnesota, Arkansas, and other poultry producing states in the Atlantic, Mississippi and Pacific flyways. Since domestic fowl are known to be more
TABLE 2. Prevalence of Antibody to Newcastle Disease enza in Sera from Wintering Waterfowl in Oklahoma.
Species
and
Disease Virus
Virus
and
Type-A
Influ-
Type-A Influenza
platyrhynchos)
5/156 (3.21%)
3/122 (2.45%)
American widgeon (Anas americana)
1/37 (2.70%)
1/37 (2.70%)
Pintail (Anas
(tL0%)
0/5 (0.0%)
5/87 (5.75%)
1/7 (14.28%)
Canada (Branta TOTALS
0/’5
acuta) goose
canadensis)
11/280 (3,93i)
5/171 (2.92%)
Journal
140
susceptible to Newcastle disease virus than are wild waterfowl,’ the lower number of positive serologic reactors may thus be explained by the lack of opportunity for exposure to a domestic source. Antibody to type-A influenza was detected in 5 of 171 birds examined. Three of 122 mallards (2.45%), 1 of 37 American widgeons (2.70%) and 1 of 7 Canada geese (14.28%) had antibody. The detection of antibody to influenza in serum samples collected from migratory waterfowl in Oklahoma is consistent with findings of other investigators in the Pacific, Mississippi and Atlantic flywnys.2”7”2#{176} Since all samples for
of Wildlife
Diseases
Vol.
15, January,
1979
this study were taken in the winter and early spring the serologic titers, if they reflect ongoing infection, indicate that waterfowl migrating through Oklahoma carry influenza infections throughout their migratory route or that transmission occurs during migration and/or on the wintering grounds. Although considerable insight into the epizootiology of infectious diseases can be gained by serologic studies, definitive statements concerned with the acquisition and perpetuation of these infections must await detailed studies designed to isolate and characterize the agents involved.
Ackhowledgements We wish to thank Dr. E.C. Greiner, International Reference Centre for Avian Haematozoa for his aid in parasite identification; Ms. Pat Franks for her technical assistance; and Mr. Howard Jarrell for his encouragement and support. We would also like to thank the personnel of Salt Plains NWR and Washita NWR for their assistance.
LITERATURE
CITED
1.
ASPLIN,
F.D.
2.
BAHL, AK., B.S. POMEROY, B.C. EASTERDAY and S. MANGUNDIMEDJO. 1975. Isolation of type-A influenza viruses from the migratory waterfowl along the Mississippi Flyway. J. WildI. Dis. 11: 360-363.
1947.
Newcastle
3.
BEARD, C.W. 1975. Avian influenza. In: Isolation pathogens. S.B. Hitchner, C.H. Domermuth, Williams, eds. Arnold Printing Co., New York.
4.
BELLROSE, Books,
5.
BENNETT, quin
F.C. 1976. Harrisburg, G.F. Park,
1960. Ontario,
disease
Ducks, geese, Pa. 543 pp. On some Canada.
in ducks
and
and
swans
geese.
of North
ornithophilic Can. J. Zool.
blood-sucking 38: 377-389.
HEUSMANN of the Atlantic
and A.G. Flyway.
, W. BLANDIN, H.W. Hematozoa of the Anatidae Wildl. Dis. 10: 442-451.
7.
, A.D. SMITH, W. WHITMAN and M. CAMERON. Anatidae of the Atlantic Flyway. II. The Maritime Wildl. Dis. 11: 280-289.
BRADSHAW, waterfowl
J.E. and D.O. in the Mississippi
9.
GREINER, E.C., G.F. Distribution of the 1762-1787.
TRAINER. Flyway.
Rec.
and Identification G.H. Purchase
6.
8.
Vet.
America. diptera
59:621-624.
of avian and J.E. Stackpole in Algon-
CAMPBELL. I. Massachusetts.
1975. Hematozoa of the Provinces of Canada. J.
1966. Some infectious diseases J. Wildl. Manage. 30: 570-576.
BENNETT, E.M. WHITE avian hematozoa of North
1974. J.
and F. America.
of
COOMBS. 197-5. Can. J. Zool, 53:
Journal
10. 11.
of Wildlife
HERMAN, Am. .
Diseases
Vol.
15, January,
1979
C.M. 1968. Blood Wildl. Nat. Resour.
1951.
Blood
parasites
141
parasites of North Conf. 33: 348-359. from
California
American
ducks
and
waterfowl. geese.
Trans.
J. Parasit.
N.
37:280-
282. 12.
NELSON, E.C. and J.S. GASHWILER. waterfowl. J. Wildl. Manage. 3: 119-205.
13.
O’MEARA, 207-209.
D.C.
14.
PALMER, disease
S.F. and D.O. virus in Canada
15.
ROSENBERGER, J.K., W.C. KRAUSS and RD. SLEMONS. 1974. Newcastle disease and type-A influenza viruses from migratory in the Atlantic Flyway. Avian Dis. 18: 610-613.
16.
, S. disease Avian
1956.
Blood
parasites
1941.
of some
Maine
Blood
parasites
waterfowl.
of
J. Wildl.
TRAINER. 1970. Serologic evidence geese. Avian Dis. 14: 494-502.
Maine Dis. 20:
of Newcastle Isolation waterfowl
of
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Received
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Hematozoa
12 May
1978
from
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