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BIOLOGICAL AND ECOTOXICOLOGICAL CHARACTERISTICS OF TERRESTRIAL VERTEBRATE SPECIES RESIDING IN ESTUARIES

Laughing Gull Laughing Gull photo by M. Iliff
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Biological Characteristics

Species Larus atricilla is 38-43 cm in length. With an average mass of 325 grams (Dunning, 1993). During the summer months this species displays a black hood. Its back and wings are grey, and the trailing edge of the wing is white. In winter, the black hood is absent (Bull and Farrand, 1977).
Status in Estuaries This species is a colonial breeder that may nest with other gulls or terns (Hoopes et al., 1994). It is found primarily along coastal bays, salt marshes and estuaries, though nesting also occurs near agricultural and industrial areas (White et al, 1983b; Bull and Farrand, 1977). Nests (5 cm high by 8 cm wide) are constructed of sticks and grass, and are on the ground or in tall grass. A typical clutch consists of 1-3 olive-brown eggs with dark spots (Bull and Farrand, 1977). Young are semiprecocial. (Ehrlich et al., 1988). The maximum age of a laughing gull recorded in nature is 15 years (Clapp et al., 1983).
Abundance and Range Laughing gulls breed along the eastern seaboard of the U.S. from the Gulf of Mexico to Connecticut with breeding areas also found in Massachusetts and Maine. In the winter, the species can be found nesting south of Virginia. Approximately 165,432 individuals were counted in the late 1970s along the Atlantic Coast and 113,212 along the Florida Coast (Spendelow and Patton, 1988).
Site Fidelity High nest site fidelity (Salvatore, 1970).
Ease of Census Simple
Feeding Habits Carnivore-scavenger. Laughing gulls feed either aerially or from the water’s surface by diving or skimming (Clapp et al., 1983). The diet is highly varied and typical items include small fish, garbage, sewage, refuse from fishing boats, and insects (Hulse et al., 1980)
 

Laughing Gull Contaminant Exposure Data

I.

Organochlorine Contaminants

A.

Concentrations in Adults

1.

Organochlorines were measured in a laughing gull collected from Florida in 1974 (Johnston, 1976). Concentrations detected in adipose tissue were 16.03 g/g wet weight DDE, 26.02 g/g total DDT, and 1.78 g/g dieldrin. In uropygial gland, values were 2.18 g/g DDE, 3.93 g/g total DDT, and 0.47 g/g dieldrin. PCB was not detected.

2.

In 1978 and 1979, laughing gull carcasses were collected from four sites in the lower Rio Grande Valley (White et al., 1983a). When examining the whole carcass, DDE was detected in all specimens and median values for the four sites ranged from 2-34 g/g wet weight, with individual values ranging from 1-81 g/g. Toxaphene was detected at three sites, with median values of 0.2, 0.2, and 0.7 g/g, with individual values up to 3 g/g. Median PCB concentrations ranged 1-4 g/g for the four sites, with individual values up to 23 g/g.

3.

In 1980 and 1981, DDE in individual laughing gull carcasses (N=20) collected from Galveston Bay ranged from 0.7 to 5.5 g/g wet weight (King and Krynitsky, 1986). Low concentrations of DDD, dieldrin, chlordane, HCB, heptachlor epoxide and polychlorinated styrene were also detected. PCB concentrations in individuals ranged from 1.5 to 11 g/g.

B.

Concentrations in Eggs

1.

Ten laughing gull eggs were collected along the Texas Coast in 1970 (King et al., 1978). Total DDT averaged 10.35 g/g wet weight. Low concentrations of dieldrin (0.52 g/g) and PCBs (3.00 g/g) were also detected.

2.

Eggs were collected from estuaries located in South Carolina near the Cape Romain National Wildlife Refuge during the 1971 and 1975 breeding seasons (Blus and Lamont, 1979). In 1971, geometric mean (range) concentration was 1.41 (0.55-3.33) g/g fresh wet weight for DDE, and 2.6 (not detectable-9.5) g/g for PCBs. In 1975, geometric mean (range) concentration was 1.14 (0.65-2.20) g/g fresh wet weight for DDE, and 1.6 (not detectable-4.8) g/g for PCBs. During both study years, concentrations of dieldrin were <1 g/g.

3.

Three laughing gull eggs collected from Floridas west coast in 1972 contained concentrations of 11.70 g/g dry weight DDE, 17.2 g/g PCB, and 0.61 g/g dieldrin (Lincer and Salkind, 1973).

4.

Eggs were collected from Corpus Christi (N=92), Port Mansfield (N=56), and Laguna Vista (N=53) along Texas' southern coast (White et al., 1983b). DDE was highest at the Port Mansfield location at a geometric mean concentration of 3.7 g/g wet weight (range 0.8-63). The highest concentration of DDE in an individual egg was 91 g/g from Corpus Christi. Concentration of dieldrin, heptachlor epoxide, and toxaphene were low (<1 g/g). The geometric mean for PCBs was highest at Laguna Vista and Corpus Christi at 2.0 g/g.

5.

Laughing gull eggs were collected along Galveston Bay in 1980 (N=20) and 1981 (N=20) (King and Krynitsky, 1986). DDE in individual samples ranged from 0.3 to 4.5 g/g wet weight, PCBs from 0.7 to 8.5 g/g, and levels of dieldrin, chlordane, HCB, heptachlor epoxide, and PCS were low.

6.

A summary of data collected from Corpus Christi, Port Mansfield, Languna Vista, and Galveston Bay, Texas found that between 1970 and 1981, DDE concentrations in laughing gull eggs decreased from 10 g/g wet weight to <1 g/g, and PCBs declined from 3.0 g/g to 1.5 g/g (Mora, 1995).

II.

Cholinesterase-Inhibiting Pesticides

1.

In 1978, a die-off of adults and chicks occurred after a cotton field in Corpus Christi, Texas was sprayed with parathion (White et al., 1979a). Of 9 gastrointestinal tracts analyzed from birds found dead, 7 contained parathion in concentrations ranging from <0.02-10 g/g wet weight.

2.

In July 1993, a live laughing gull was found lying on its side 36 hours following application of bendiocarb to a turfgrass nursery (Rainwater et al., 1995). A footwash sample from this bird was found to contain 50.33 g bendiocarb.

III.

Trace Elements, Metals, and Metalloids

A.

Concentrations in Adults, Juveniles, and Nestlings

1.

In 1974, Pb in the brain, heart, liver, and muscle were analyzed in adult and prefledgling carcasses collected from South Deer Island, Galveston Bay, Texas (Munoz et al., 1976). In male and female adults, mean Pb concentrations were highest in the liver, 5.04 and 3.74 g/g wet weight, respectively. Lead concentrations were lowest in the muscle at 1.74 g/g for males and 1.24 g/g for females. In prefledgling males and females, Pb levels were again highest in the liver at 4.20 g/g and 5.43 g/g, respectively. The values were lowest in the muscle at a mean concentration of <1.0 g/g for males and 1.13 g/g for females.

2.

Between 1974 and 1976, one laughing gull was collected from Brunswick, Georgia (Gardner et al., 1978). Mercury concentrations of 7.4 mg/g dry weight in the muscle, of which 66% was MeHg, and 29 mg/g in the liver, of which 77% was MeHg, were found.

3.

In 1977, male and female laughing gulls from various age groups were again collected from South Deer Island in Galveston Bay (Hulse et al., 1980). The data indicated that no sex related differences existed in uptake of metals. In the downy young, Pb was highest in the liver at 1.84 g/g wet weight and was detected at <1 g/g in the brain, bone, heart, kidney, and muscle. In prefledglings, Pb was highest in the bone at 3.85 g/g, followed by the liver at 3.13 g/g. In adults, Pb was highest in the bone at 6.93 g/g followed by the liver at 5.31 g/g. Cadmium in downy young was highest in the kidney at 0.116 g/g. In prefledglings, Cd was highest in the liver at 0.116 g/g and in adults Cd was highest in the kidney at 1.509 g/g. Manganese was highest in the brain of the downy young at 2.4 g/g with similar levels in the liver at 2.3 g/g. In prefledglings, Mn was highest in the kidney at 1.8 g/g followed by the bone at 1.7 g/g, and the kidney at 1.6 g/g. In adults, Mn was highest in the liver at 2.3 g/g.

4.

In 1977, a laughing gull collected from the Savannah Estuary in Georgia contained 0.80 g/g Hg in the breast muscle (Odom, 1978).

5.

In 1978, a laughing gull collected from the Savannah Estuary in Georgia contained 1.20 g/g Hg in the liver and 0.51 g/g in the breast muscle (Odom, 1981).

6.

Thirteen downy young, 18 prefledglings, and 12 adults were collected from Galveston and Matagorda Bay from 1977 to 1980 and Pb and Cd was measured in the bone, liver, and kidney (Reid and Hacker, 1982). 

For each site, Pb concentrations were highest in adults in all three tissues. In the bone, mean values for Galveston and Matagorda were 8.51 and 2.30 g/g wet weight in adults, 0.94 and 0.23 g/g in prefledglings, and 0.0056 and 0.13 g/g in downy young. In the liver, mean Pb values were 1.06 and 0.37 g/g in adults, 0.26 and 0.071 g/g in prefledglings, and 0.036 and 0.025 g/g in downy young. In the kidney, mean Pb values were 1.39 and 0.35 g/g in adults, 0.11 and 0.13 g/g in prefledglings, and 0.048 and 0.026 g/g in downy young.

Cadmium concentrations were similar among age-groups in the bone, and highest in adults for the liver and kidneys. In the bone, means ranged between 0.61-0.86 g/g for all ages at both sites. In the liver, mean Cd values for Galveston and Matagorda were 0.35 and 0.49 g/g, respectively, in adults, and 0.041-0.055 g/g for prefledglings and downy young. In the kidney, Cd values were 2.35 and 3.16 g/g in adults, 0.097 and 0.041 g/g in prefledglings, and 0.044 and 0.069 g/g in downy young.

7.

Ten laughing gulls from Galveston Bay were collected in 1980 and again in 1981 (King and Cromartie, 1986). Geometric mean concentrations of Hg in the liver were 0.88 g/g wet weight in 1980 and 0.75 g/g in 1981. Lead was detected in the liver of five gulls, with individual values ranging from 0.1-0.5 g/g. In the kidney, the geometric mean for Cd was 2.43 g/g in 1980 and 2.52 g/g in 1981. The geometric mean for Se in the kidney was 3.13 g/g in 1980 and 8.88 g/g in 1981.

8.

In 1992, laughing gulls were collected from J.F.K. Airport in New York from May thru August (Gochfeld et al., 1996). The goal of the study was to look for gender, age, and tissue differences in Pb, Hg, Cd, Mn, Se, and Cr. Lead levels were highest in the liver (0.4 g/g wet weight), in the kidney (1.5 g/g wet weight) and in feathers (2.65 g/g dry weight). Hg decreased with age in the feathers and the heart and Se decreased with age for all tissues studied. Cadmium and Cr increased with age. Specifically, Cd was higher in the feathers, hear, liver, and muscle of older birds, and Cr was higher in the liver and heart of older birds.

B.

Concentrations in Eggs

1.

In 1974, ten eggs collected from South Deer Island located in Galveston Bay contained Pb concentrations <1 g/g (Munoz et al., 1976).

2.

From 1977 to 1980, eggs were collected from South Deer Island in Galveston Bay and from an unnamed island in Matagorda Bay (Reid and Hacker, 1982). In Galveston Bay the mean Pb concentration of the total egg in 1977 was 0.15 g/g wet weight. By 1980, the mean Pb concentration had dropped to 0.037 g/g. In 1977, Cd was detected at a concentration of <0.025 g/g in Galveston Bay, and had risen to 0.17 g/g by 1980. Metal concentrations were reported for Matagorda Bay for 1980 and were similar to those outlined above for Galveston Bay.

3.

Mean Hg concentration was approximately 0.4 g/g dry weight in eggs of laughing gull nestlings from Long Point, New Jersey in the New York Bight (Burger and Gochfeld, 1997).

IV.

Petroleum

 

No residue data available 

 
Laughing Gull Contaminant Response Data

I.

Organochlorine Contaminants

1.

DDT concentration and shell thickness were measured in eggs collected along the coast of Texas in 1970 (King et al., 1978). Prior to 1943, the thickness of laughing gull eggs (N=27) was approximately 0.270 mm. In 1970 (N=65), thickness was measured to be approximately 0.263 mm, representing a significant decrease of 3%.

2.

The thickness of 15 eggs collected in 1971 and 11 eggs collected in 1975 near Cape Romain NWR in South Carolina was compared to pre-1947 values (Blus and Lamont, 1979). Mean thickness values were 0.280 mm (N=4) prior to 1947, 0.271 mm in 1971, and 0.268 mm. Differences were not statistically significant.

3.

Egg shell thinning (7-14%) was detected in eggs collected from Corpus Christi, Port Mansfield and Languna Vista, Texas (White et al., 1983b). No relationship was found between DDE concentratoin and shell thinning.

4.

No change in eggshell thickness was detected when eggs collected in 1980, 1981, and 1982 in Galveston Bay, Texas were compared to pre-1947 measurements (King and Krynitsky, 1986).

II.

Cholinesterase-Inhibiting Pesticides

1.

In 1978, a die-off of adults and chicks occurred after a cotton field in Corpus Christi, Texas was sprayed with parathion (White et al., 1979a). Acetylcholinesterase (ChE) in the brains of dead adults was inhibited by 57-89%. The brains of nine chicks were analyzed, four which exhibited ChE inhibition of 75-90%. Acetylcholinesterase activity in the remaining five chicks was similar to control values. The cause of death in these birds was suspected to be parathion exposure resulting from insect consumption.

2.

In 1979, organophosphorous poisoning was the suspected cause of death in chicks from a Corpus Christi colony (White et al., 1983b). Low productivity (0.5 fledgling/nest) occurred as a result of these deaths.

3.

In July 1993, a laughing gull was found displaying signs of anticholinesterase poisoning (profuse salivation, respiration with rapid pants, and paralysis) about 36 hours after a turfgrass nursery was sprayed with bendiocarb (Rainwater et al., 1995). Blood samples were drawn, and ChE in this bird was found to be inhibited by 87%. The authors noted that this bird recovered from its exposure rather quickly.

4.

A controlled dosing study found that a dose of parathion at 6 mg/kg body weight depressed ChE activity by approximately 50% but no obvious signs of intoxication were exhibited (White et al., 1983c). Based on this data, the same dose was given orally to laughing gulls to determine the effect on nest attentiveness. Gulls were observed to spend less time incubating on day 2 and 3, yet by noon on day 3 incubation time for the treated birds was similar to the controls.

5.

One sublethal dose of parathion (5 mg/kg) was found to have no effect on either nest defense behavior or hatching success (King et al., 1984).

III.

Trace Elements, Metals, and Metalloids

 

No response data available

IV.

Petroleum

1.

The breast feathers of laughing gulls were treated with 2.5 ml of no. 2 fuel oil and the gulls were allowed to incubate (King and Lefever, 1979). Within five days, 41% of embryos in the oil-treated group had died compared to only 2% of embryos in the control group. There was no significant difference in the number of infertile eggs between groups.

2.

When 20 l of oil was applied to the air cell end of laughing gull eggs, 83% embryo mortality occurred after five days (White et al., 1979b).

3.

No significant increase in embryo mortality was seen when 10 l of oil was applied to the eggshell surface about half way through incubation (Macko and King, 1980). 


References for Laughing Gulls

Blus, L.J. and T.G. Lamont. 1979. Organochlorine residues in 6 species of estuarine birds South Carolina USA 1971-1975. Pestic. Monit. J. 13:56-60

Bull, J. and J. Farrand, Jr. 1977. The Audubon Society Field Guide to North American Birds. Alfred A. Knopf, New York. 784 pp.

Burger, J., and M. Gochfeld. 1997. Risk, mercury levels, and birds: Relating adverse laboratory effects to field biomonitoring. Environ. Res. 75:160-172.

Clapp, R.B., D. Morgan-Jacobs, and R.C. Banks. 1983. Marine birds of the southeastern United States and Gulf of Mexico. Part III: Charadriiformes. U.S. Fish and Wildlife Service, Office of Biological Services, Washington, D.C. FWS/OBS-83/30. 853 pp.

Dunning, Jr., J.B., ed. 1993. CRC Handbook of Avian Body Masses. CRC Press, Ann Arbor. 371 pp.

Ehrlich, P.R., D.S. Dobkin, and D. Wheye. 1988. The Birder's Handbook. Simon & Schuster, New York. 785 pp.

Gardner, W.S., D.R. Kendall, R.R. Odom, H.L. Windom, and J.A. Stephens. 1978. The distribution of methyl mercury in a contaminated salt marsh ecosystem. Environ. Pollut. 15:243-251.

Gochfeld, M., J.L. Belant, T. Shukla, T. Benson, and J. Burger. 1996. Heavy metals in laughing gulls: Gender, age and tissue differences. Environ. Toxicol. Chem. 15:2275-2283.

Hoopes, E.M., P.M. Cavanagh, C.R. Griffin, and J.T. Finn. 1994. Synthesis of information on marine and coastal birds of the Atlantic Coast: Abundance, distribution, and potential risks from oil and gas activities. Volume II: Species accounts, abundance, distribution, and status. Massachusetts Cooperative Fish and Wildlife Research Unit, Amherst, Massachusetts. 178 pp.

Hulse, M., J.S. Mahoney, G.D. Schroder, C.S. Hacker and S.M. Pier. 1980. Environmentally acquired lead, cadmium, and manganese in the cattle egret, Bubulcus ibis, and the laughing gull, Larus atricilla. Arch. Environ. Contam. Toxicol. 9:65-78

Johnston, D.W. 1976. Organochlorine pesticide residues in uropygial glands and adipose tissue of wild birds. Bull. Environ. Contam. Toxicol. 16:149-155.

King, K.A. and E. Cromartie. 1986. Mercury, cadmium, lead, and selenium in three waterbird species nesting in Galveston Bay, Texas, USA. Colon. Waterbirds 9:90-94

King, K.A. and A.J. Krynitsky. 1986. Population trends, reproductive success, and organochlorine chemical contaminants in waterbirds nesting in Galveston Bay, Texas. Arch. Environ. Contam. Toxicol. 15:367-376.

King, K.A. and C.A. Lefever. 1979. Effects of oil transferred from incubating gulls to their eggs. Proc. Conf. Colonial Waterbird Group 3:258.

King, K.A., E.L. Flickinger., and H.H. Hildebrand. 1978. Shell thinning and pesticide residues in Texas aquatic bird eggs, 1970. Pestic. Monit. J. 12:16-21.

King, K.A., D.H. White and C.A. Mitchell. 1984. Nest defense behavior and reproductive success of laughing gulls sublethally dosed with parathion. Bull. Environ. Contam. Toxicol. 33:499-504.

Lincer, J.L., and D. Salkind. 1973. A preliminary note on organochlorine residues in the eggs of fish-eating birds of the west coast of Florida. Florida Field-Nat. 1: 19-22.

Macko, S.A. and S.M. King. 1980. Weathered oil: effect on hatchability of heron and gull eggs. Bull. Environ. Contam. Toxicol. 25:316

Mora, M.A. 1995. Residues and trends of organochlorine pesticide and polychlorinated biphenyls in birds from Texas, 1965-88. Fish Wildl. Res. No. 14. Technical Report. U.S. National Biological Service, Washington, D.C.

Munoz, R.V. Jr., C.S. Hacker, and T.F. Gesell. 1976. Environmentally acquired lead in the laughing gull, Larus atricilla. J. Wildl. Dis. 12:139-142

Odom, R.R. 1978. Statewide wildlife investigations.: Mercury contamination studies. Georgia Game and Fish Division. 17 pp.

Odom, R.R. 1981. Statewide wildlife investigations: Mercury contamination studies. Georgia Game and Fish Div. 15 pp.

Rainwater, T.R., V.A. Leopold, M.J. Hooper, and R.J. Kendall. 1995. Avian exposure to organophosphorous and carbamate pesticides on a coastal South Carolina golf course. Environ. Toxicol. Chem. 14:2155-2161.

Reid, M. and C.S. Hacker. 1982. Spatial and temporal variation in lead and cadmium in the laughing gull, Larus atricilla. Mar. Pollut. Bull. 13:387-389

Salvatore, F. B.1970. Nest-site selection by adult laughing gull (Larus atricilla). Animal Behavior 18:434-444.

Spendelow, J.A., and S.R. Patton. 1988. National atlas of coastal waterbird colonies in the contiguous United States: 1976-82. Biological Report 88(5). U.S. Fish and Wildlife Service, Washington, D.C.

White, D.H., K.A. King, C.A. Mitchell, E.F. Hill, and T.G. Lamont 1979a. Parathion causes secondary poisoning in a laughing gull breeding colony. Bull. Environ. Contam. Toxicol. 23:281-284.

White, D.H., K.A. King, and N.C. Coon. 1979b. Effects of no. 2 fuel oil on hatchability of marine and estuarine bird eggs. Bull. Environ. Contam. Toxicol. 21:7-10.

White, D.H. C.A. Mitchell., H.D. Kennedy, A.J. Krynitsky, and M.A. Ribick. 1983a. Elevated DDE and toxaphene residues in fishes and birds reflect local contamination in the lower Rio Grande Valley, Texas. Southwest Naturalist 28:325-333.

White, D.H., C.A. Mitchell and R.M. Prouty. 1983b.  Nesting biology of laughing gulls in relation to agricultural chemicals in south Texas, 1978-81. Wilson Bull. 95:540-551.

White, D.H., C.A. Mitchell and E. F. Hill. 1983c. Parathion alters incubation behavior of laughing gulls. Bull. Environ. Contam. Toxicol. 31:93-97.

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