MERCURY BIOACCUMULATION IN ORGANISMS FROM THREE PUERTO RICAN ESTUARIES J O A N N A B U R G E R 1,2, K E I T H C O O P E R 2'3 , J O R G E S A L I V A 1, D. G O C H F E L D 4, D. L I P S K Y 5 and M I C H A E L G O C H F E L D 2,6

1 Department of Biological Sciences, Rutgers University, Piscataway, New Jersey 08855, U.S,A. 2 Environmental and Occupational Health Science Institute, Piscataway, New Jersey 08855, U.S.A. 3 Toxicology, School of Pharmacy, Rutgers University, Piscataway, New Jersey 08854, U.S,A. 4 Department of Zoology, University of Hawaii, Honolulu, Hawaii 96822, U.S.A. 5 Dynamac Inc., FT Lee, New Jersey 07024, U.S.A. 6 Environmental and Community Medicine, UMDNJ-Robert Wood Johnson Medical School, Piscataway, New Jersey, U.S,4. (Received: February 1991)

Abstract. We analyzed mercury levels in shrimp (Palaemonetes sp.), Blue Crabs (Callinectes sp.), fish (Tarpon Megalops atlantica and Tilapia Tilapia mossambica), lizards (Ameiva exsul), Cattle Egret (Bubulcus ibis) and Moorhen (Gallinula chloropus) in three estuaries in Puerto Rico in 1988. There were no quantifiable concentrations greater than the method detection limit of mercury in shrimp, crabs and lizards from any site. Mercury levels were also below detection limits in Tilapia, except for specimens collected at Frontera Creek, allegedly contaminated with mercury. However, mercury levels ranged from 92-238 #g/kg (wet weight) in Tarpon, a predaceous fish that feeds on smaller fish. Few of the birds had detectable levels of mercury. Our results indicate relatively low concentrations of mercury in biota collected in all of the three estuaries at most trophic levels, although 10 of 12 Tarpon fillet samples from Frontera had detectable mercury compared to 3 of 12 fillet samples for the other two lagoons.

1. Introduction Mercury is distributed throughout the environment, and is derived from industrial processes, agricultural activities, burning of fossil fuels and natural weathering of geologic formations (Nelson, 1971). Naturally-occurring mercury, released to the environment through leaching and volatilization, is uncontrollable, but many of the man-made sources can be (and some have been) eliminated or at least curtailed by increased environmental controls. Mercurial compounds are toxic to many organisms, and the spectrum of toxicity depends on whether the mercury is present as an organometallic compound or in inorganic form. Organic mercury, particularly methylmercury, is a severe problem Environmental Monitoring and Assessment 22: 181-197, 1992. @ 1992 Kluwer Academic Publishers. Printed in the Netherlands.

182

JOANNA BURGER ET AL.

because of its propensity to attack the nervous-system, its long retention in the body, and its effect on developing organs through transplacental passage (Nelson, 1971; Goldwater, 1972; Clarkson, 1990). Much of the mercury in aquatic organisms and ecosystems is present in the organic form due to biomethylation in partially anaerobic sediments (Windom and Kendall, 1979). In birds, methylmercury reduces egg hatchability, accumulates in the brain causing neurotoxicity, and is often lethal (Nelson, 1971). In addition to causing death and decreased reproductive success of a variety of organisms (see Sunda et al., 1978), mercury also decreases growth (Roderer, 1983; Thorn, 1984) and causes behavioral abnormalities (Erdem and Meadows, 1980). High levels of mercury were reported worldwide from shellfish (Freeman et al., 1974), fish (Bache, 1971; Fimreite, 1973; Matsunaga, 1975), and birds (Fimreite et al., 1974; Hoffman and Currow, 1979; Gochfeld, 1980a,b; Parslow et al., 1982; Braune, 1987; Ohlendorf et al., 1988). As the pattem of mercury bioaccumulation and amplification became apparent, fewer descriptive papers appeared, although experimental studies continued (refer to Tables V and VII). Aquatic ecosystems and their organisms are particularly vulnerable to mercury contamination because of runoff and accumulation in water, soil, and sediments (Nelson, 1971; May et al., 1987). Mercury and other heavy metals can reach high concentrations in lakes and estuaries (Bopp and Biggs, 1981; Howard et al., 1988) as well as in the sea (Brugmann, 1981). Studies of metal levels and bioaccumulation have examined a wide range of metals in one system, in a wide number of locations for one organism, or on a wide spectrum of metals from many organisms in one system. Rarely do we examine many trophic levels from several systems. In this paper we examine mercury levels in shrimp (Palaemonetes spp.), Blue Crabs (Callinectes spp.), Tarpon (Tarpon megaIops), Tilapia (Tilapia mossambica), lizards (Ameiva exsul), Cattle Egrets (Bubulcus ibis), and Moorhens (Gallinula chloropus) in three estuaries in Puerto Rico. We were interested in whether mercury levels were increased in the higher trophic level organisms, and whether there were differences among the three estuaries.

2. Study Area We conducted our study on two coastal marshes on the East Coast (Humacao Marshes and Roosevelt Roads) and one on the Southwest coast (Boqueron) of Puerto Rico (see Pico, 1974) in February and March 1988 (Figure 1). Since sampling scale is always a problem (Livingston, 1987), we sampled two to four sites at each of the three estuaries. Boqueron Refuge is located in the southwest comer of Puerto Rico and is operated by the Department of Natural Resources. It is bordered on the west by Boqueron Bay and on the remaining sides by agricultural land, particularly pasturage. Most of the refuge consists of mangroves (including red mangrove (Rhizophora mangle), black mangrove (Avicennia nitida), and white mangrove

183

MERCURY BIOACCUMULATION IN PUERTO RICO

)

J

[__~.,,.~,./.._~~

BOQUERON

#

~

ROOSEVELT

i "o'os

FRONTERA

(~ 116 312 Fig. 1. Map of Puerto Rico showing locations of estuaries studied.

(LaguncuIaria) and extensive, essentially fresh water lagoons, separated on the west from the bay by a narrow strip of mangrove. A road through the mangroves provides acess to most of the refuge. A flood gate retains water in the lagoon, or releases it to flow into the bay. The marsh contains extensive stands of Juncus and other emergents as well as submerged vegetation. Roosevelt Roads is a U.S. Naval Air Station in northeastern Puerto Rico with restricted access. We used two collecting sites: a lagoon in a mangrove area (red and black mangroves), and a creek about 10 m wide that was similar in physiognomy (i.e., vegetation structure and density) to Frontera Creek at Humacao. The military base juts into the Caribbean Sea and has several bays and estuaries on its perimeter. Although probably the coast was originally entirely mangroves and tidal wetland, it has been extensively altered by dredging and tilling. Currently about half of the shoreline is fringed with mangrove, the remainder having been developed for military purposes. The Humacao Refuge is located 18 km southwest of Roosevelt Roads. It lies along Highway 3, about 5 km east of Humacao and is bordered on the east by the Caribbean Sea. The Humacao system contains extensive lagoons and mangrove stands, tabonuco Pterocarpus officinalis swamps, grasslands, coconut groves, estuaries and salt water marshes. The entire lagoon system covers an area of 1237 hectares (Division of Coastal Resources, 1981). The lagoon ecosystem (including the Mandri lagoons as well as Frontera lagoons) is interconnected by a canal which drains into Frontera Creek and thence into the ocean north of the E1 Morillo hill (see Colon et al., 1980). All lagoons were drained in the 1920s for sugar cane and coconut production. However, in the late 1970s drainage pumps malfunctioned, allowing the land to be submerged and the lagoons to reform. Tidal changes canbe observed at times in the lagoons. The Mandri lagoons also connect with the Caribbean via the Anto Ruiz and the Boca Prieta Stream. The freshwater marshes of the system are dominated by cattail (Typha dominguensis), and other plants such as Eleocharis spp., Alisma cordifolia, and Cyperus sp. Adjacent grassland has been subject to grazing and has

184

JOANNA BURGER ET AL.

a wide array of grasses and herbs. Panicum sp. and Paspalum vigatum were among the dominants. The aquatic system we sampled comprises three interconnected lagoons. The Front Lagoon nearest to Highway 3 has extensive cattail stands separating it from pasture. Heavily vegetated dikes separated it from Mandri Creek, Frontera Creek, and grassland. The smaller Palmas Lagoon, containing many dead coconut palm stumps, is particularly rich in wildlife and is a nesting ground for the endangered West Indian Whistling Duck (Dendrocygna arborea, Raffaele, 1983). Palmas Lagoon is connected to the large South Lagoon by a narrow overgrown channel. A densely vegetated hill partially separates the two lagoons. All three lagoons are ecologically similar, being shallow (mostly less than 2 m deep), and bordered by cattails, sedges (Cyperus spp.), and Panicum. Where salinity is low, there are some patches of water hyacinth (Eichornia crassipes), but for the most part the surface of the lagoon is open. Frontera Creek is a small stream draining the hill country north and east of Humacao. The creek is 6.4 km long and drains a 1000 hectare watershed into the Caribbean. It is also important to note that the creek has been dredged in the last ten years for flood control and drainage. Mandri Creek runs from the Mandri Lagoons west of Highway 3 to the Santa Theresa pumphouse. It is a deep water (more than 6 m deep) channel bordered along part of its length by red and black mangroves and also by hardwood forest and scrub land.

3. Collecting Methods Shrimp, crabs, fish and lizards were collected at all three study sites. Because of the sensitivity of endangered avian species at Roosevelt Roads, birds were collected only at Humacao and Boqueron. All specimens were collected in February and March 1988. Shrimp were located from grass beds at the edges of lagoons and creeks with a 5 m long, fine mesh, two-person seine and with a 15 x 10 cm dip net. Shrimp were removed from the net with polyethylene gloved hands, and counted. Crabs were collected using bait and hooks, folding star crab traps, and gill nets. The former two methods, using chicken as bait, were also used extensively by local crabbers. Fish were caught with 40 m long gill nets which were set during the day and at night, and left f o r 4 to 12 h. Fish identifications were based on Erdman (1967). Lizards were collected using drift fences and baited rat traps on land adjacent to the estuaries (often on dikes between ponds). Drift fences of plastic sheeting held by wooden slats were configured in a V with 30 m wings, and several people herded the lizards which were funneled into a mesh trap. Birds were collected from several locations within each estuary using a 12-gauge shotgun with steel shot.

MERCURY BIOACCUMULATION IN PUERTO RICO

185

4. Handling and Analysis Methods In the field, animals (except shrimp) were assigned individuals numbers and were weighed, measured, and double-wrapped in aluminum foil that had been triplerinsed with analytical grade n-hexane. Each package contained a waterproof label between the aluminium layers, as well as an external label with a chain of custody. Shrimp samples were composites of 100 grams (wet weight). All specimens were placed on ice and later transported to a field freezer until they were transported on dry ice in sealed ice chests to our laboratory. Dissection and homogenization of specimens in the laboratory were performed according to EPA specifications (EPA, 1981). All equipment was triple-rinsed with ultra pure analytical grade n-hexane and nitric acid followed by a triple rinse with glassdistilled deionized water. Specimens (except shrimp and birds from all sites, and Tilapia from Fronters Creek) were pooled into groups of five individuals of similar size from the same collection day and place. Birds and the six fish from Frontera Creek were individually analyzed. Shrimp pools represented 100 g or about 1000 individuals. For whole body analysis the frozen organisms were chopped into cubes and ground in a blender. Equal portions from each of the five organisms were then blended to provide the composite sample. For fish, edible portions comprised a fillet of lateral muscles. For crabs, the edible portions (with the green gland) were prepared, and for birds only the edible pectoral muscles were used. Fillets (fish) and livers (fish, birds) were prepared in a similar manner. Mercury levels were analyzed by Environmental Testing and Certification Laboratories, Edison, New Jersey, using EPA approved procedures for digestion, analysis, and quality control (EPA, 1981). Mercury was analyzed by cold vapor atomic adsorption with a 80 #g/kg detection limit. Each run included calibration standards and spiked samples. Only runs with recoveries between 85 and 115% were accepted, and samples were not corrected for recovery. All values are presented as arithmetic means on a wet weight basis.

5. Results Shrimp, crabs, fish and lizards were abundant at all three sample sites, but catch per hour of effort varied among and within sites (Table I). In general, capture rates were higher for crabs, Tilapia and total fish at Frontera compared to the other sites, and for lizards at Boqueron compared to the other sites. There was no detectable mercury in any of the shrimp samples, including nine from Humacao and three each from Roosevelt Roads and Boqueron. Each shrimp sample weighed 75-100 gm, depending on shrimp size. The average mass of an individual shrimp was 107-4-20 mg at Humacao, 112-4-8 mg at Roosevelt Roads and 177 4- 10 mg at Boqueron. Similarly, there were no detectable levels of mercury in the Blue Crab samples, including six whole and 12 edible samples from Humacao,

186

JOANNA BURGER ET AL.

TABLE I Comparative summary of biota collections at Humacao, Boqueron and Roosevelt Roads. Given are mean number of specimens collected per hour, per person, per net or trap. Crabs Hook and Star Trap Gill Net Tilapia Bay or Creek Lagoons Total Fish (net) Bay or Creek Lagoon Lizards (trap)

Humacao

Boqueron

Roosevelt Roads

0.40 0.76

0.22 0.43

0.31 0.28

3.31 1.58

0.32 0.91

0.37 1.46

4.65 2.42 0.10

0.64 1.04 0.49

0.62 1.70 0.04

and three whole and six edible samples from Roosevelt Roads and Boqueron. Each sample was a composite of five individuals. Mercury levels in Tilapia were generally low (Table II). There was no detectable mercury in fillets from Boqueron, Roosevelt Roads, or Humacao, although five of six fish from Frontera Creek had mercury that ranged from 92-460 #g/kg. All pooled Tilapia liver samples from Humacao had mercury levels > 80 #g/kg (Table II). There were detectable mercury levels from Tarpon fillets at Roosevelt Roads and Humacao (Table III). Both the range and mean values were slightly higher at Roosevelt Roads. There were no detectable mercury levels in the lizards. The birds were analyzed individually. One of the Cattle Egrets at Boqueron and one of the five Moorhens at Humacao had detectable mercury in the muscle, and only one whole Moorhen from Humacao showed mercury (Table IV). Mercury was detected in the liver composite (from five birds) Cattle Egrets at both sites and Moorhens at Humacao. The levels of mercury ranged from 44 to 160 #g/kg (Table IV).

6. Discussion

In the following discussion one must take into account several problems with the heavy metal literature. In some published studies authors did not specify whether wet or dry weight was used and it is not always possible to determine whether arithmetic or geometric means were reported. Moreover, changes in analytic methodologies have lowered detection limits and different authors have handled non-detectable values differently (some omitting them, others calling them zero, and others using 1/2 the detection limit). Both inter- and intra-laboratory vari-

MERCURYBIOACCUMULATIONIN PUERTORICO

187

TABLE II Mercury Levels (#g/kg wet weight) in Tilapia. Except where noted each sample (except liver) included five individuals. Number of Number of Mercury Levels Mean 4- SD Range Samples Samples Analyzed with mercury > 80/zg/kg Humacao (whole) Frontera Creek 0 Mandri Creek 3 0 Lagoons 3 0 Humacao (fillet) 176 4- 144 92--460 Frontera Creek" 6 5 Mandri Creek 6 0 Lagoons 6 0 Humacao (liver) Frontera Creekb 1 1 Mandri Creekb 1 1 8O Lagoonsb 1 1 133 Boqueron - whole 3 0 fillet 6 0 liver 1 0 Roosevelt Roads - whole 3 0 fillet 6 0 liver 1 0 "Individual fish; we also prepared a pooled sample from all fix fish (Hg = 108 ppm). b 20 livers per sample. c Only inorganic mercury available, value = 480 #g/kg. c

ability confound comparisons. Finally, s o m e studies (perhaps m a n y ) that discover low levels o f contamination are n e v e r published, hence causing confusion about ambient levels. We did not find any detectable levels o f m e r c u r y in shrimp, crab or lizards. T h e f o r m e r two are relatively low in the food chain, and the lack o f m e r c u r y is not unusual. Lizards, however, feed primarily on insects although they eat m a n y invertebrates and vegetation (Rivero 1978). Thus they m i g h t be expected to accumulate h e a v y metals if they were present. M e r c u r y levels in Tilapia generally were in the non-detectable range, except for the six fish from Frontera Creek. Frontera Creek itself has b e e n the subject o f extensive study because o f concern regarding alleged m e r c u r y contamination. Although detectable, the level in these fish was low. H i g h e r levels were found in the tarpon and birds, and these will be discussed below. In general m e r c u r y levels in fish v a r y with the size and age o f the fish (Bache

18 8

JOANNABURGERET AL. TABLE HI Mercury levels (#g/kg wet weight) in Tarpon in Puerto Rico Number of Number of Mercury Levelsa Samples Samples Mean 4- SD Range with mercury > 80 tzg/kg Humacao - whole Frontera Lagoons 3 0 Humacao - fillet Mandri Creek 5b 4 130 4- 19 112-156 Lagoons 6 6 113 4- 20 92-144 Humacao - liver Mandri Creek 1 0 Lagoons 5 0 Boqueron - whole 3 0 fillet 6 0 liver 3 0 Roosevelt Roads - whole 3 0 fillet 6 3 198 4- 43 152 4- 238 liver 3 0 a Of samples with detectable levels. b Each sample had only two fish.

et al., 1971; Scott, 1974; Potter et al., 1975; Linko and Terko, 1977; Phillips et al., 1980), and its position in the food chain (its trophic level: Phillips et al., 1980; Potter et aI., 1975). However, some studies found no relation between mercury levels and sex or weight (Freeman et al., 1974), or age (Westoo, 1973). Mercury levels also vary with distance from point sources (Fimreite and Reynolds, 1973), sediment levels o f mercury, pH, water hardness (Hakarison et al., 1988), and acidification (acidity sometimes enhances uptake: Jenson, 1988). Since fish growth is indeterminate, size can be used to some extent as a surrogate measure for age. Generally older fish have had a longer period to accumulate mercury, but more importantly they are larger and therefore eat larger prey which m a y be more likely to have higher mercury levels. Another generalization is that piscivorous (fish-eating) fish have higher levels than planktivorous or herbivorous species. Table V summarizes world-wide studies o f mercury levels in fish species favored for sport and human consumption. The highest level detected was 47 000 ~g/kg (47 ppm) in Northern Pike from a mercury contaminated site in Ontario. Fish higher on the food chain tend to have about an order o f magnitude higher levels than those lower on the food chain. There is also substantial geographic variation with lower values in England than in

MERCURY BIOACCUMULATION IN PUERTO RICO

189

TABLE IV Mercury levels (#g/kg wet weight) in Cattle Egrets and Moorhen Number of Samples

Number of with Mercury > 80/zg/kg

Cattle Egret Humacao muscle 5 whole 1 fiver 1 Boqueron muscle 5 whole 1 fiver 1 Moorhen Humacao muscle 5 whole 1 fiver 1 Boqueron muscle 5 whole 1 fiver 1 a Of samples with detectable limits of

0 0 1

Mercury Mean Level #g/kg a

44

1 0 1

132

1 1 1

120 84 160

0 0 1 80 #g/kg.

98

0

North America. Levels in fish may show temporal declines as more environmental controls are placed on industry. The large majority of reported values are in the range of 1000 to 10 000 #g/kg, or 1-10 ppm, with most below 2000 #g/kg. The lowest values (~ 20 #g/kg) were recorded in three species of herbivorous marine fish from Israel. Thus the levels of mercury in the Puerto Rican estuaries we studied were generally low, particularly for a predaceous species such as Tarpon. Table VI indicates mercury levels (#g/kg, wet weight) in a variety of fish analyzed from Puerto Rico and the Virgin Islands in the early 1970s. The table gives the range of mean values for anywhere from one to five geographically separated samples. Except for two shark samples, all means were below 1000 #g/kg. The highest values encountered in our Tilapia sample, 460 #g]kg, was near the median for the entire set. The values for tarpon were all below 250/@/kg, toward the low end of the distribution, and corresponding to the single mean of 200 #g/kg for a tarpon sample from Guyanilla, Puerto Rico (Riemold, 1975). Thus the values obtained in this study were generally much lower than most values obtained from a wide variety of coastal fish. This might suggest that mercury levels have declined in the past two decades. Alternatively there may be consistent geographic variation

190

JOANNA BURGERETAL.

TABLE

V

Literature s u m m a r y of m e r c u r y levels in fish. F o r T r o p h i c level, P = plankton, D = detritus, H = plants, C = carnivore, * = predator on o t h e r fish; S i z e of letter indicates i m p o r t a n c e Speoes

American plaice (Hippoglossowles platessoldes) Arctic Claa~ (Salvelinus alpir~us) AtlanticSalmon (Salma salar) Atlantic Salmon Atlantic Salmon Afl~mtlcSalmon Atlantic Salmon Baltic Henfing (Clupea harengus) Barracuda (Sphyraena borealis) Barracuda BlackCrappie (Pomoxis nlgromaculatus) Blaaklish ( Gadopsis marmoratas) Bluefish (Pomatomus saltatrix) 81uefish BrowaTrout (Sa lmo trutta ) Brown Trout Burbot (Lota Iota) Bttrbot Cod (Gadus collarias) Cod Cod Cod Crucian carp (Carassius carassius langsdorfiO Cask (Brasme bro~'me) Daoe (Triblodon hakonensis) Fourhom sculpin (Myx~ephalus quadricornis) Fourhom Scadpm Gaspereau (alewife) (Alosa pseudohanengus) Goldeye (Hiodon alasoides) Haddock (Melanogrammus aeglefinus) Hake (Urophyci$ tenuis) Halibut (HIppoglossus hlppoglossus) Halibut Herring Lake Trout (Salvelira~ namaycush) Lake Trout LakeWl~tefish (Coregvnus clupeaformis) Longnose Sucker ( Catostomus catastomus) Lm~fish (Cyclopterus lw~pus) Mackerel (Scomber scambrus) Menhaden (Brevcortia tyrannus)

Tropl~c Levela

Country

P,e

Canada

C* C*

Range in Muscle Min Max (~,~b

Mean Vale

Reference

Freeman et al., 1974

140

150

Norway

140

420

Canada

100

110

C* C* C* C~ P

Sweden Canada Canada $ wedea Finland

143 I40 180 148 90

321 140 190 375 150

C*

Israel

200

700

Levita~etal.,1974

C* C

Israel Montana

210 125

1750 650

Levitanetal.,1974 Phillips et aL, 1980

C

Australia

80

640

Bycroft et al., 1982

C*

commercial

600

Wobeseret al., 1970

C* C*

LI New York Norway

500 I400

Undardaland Hastein, 1971

C* C

Australia Saskatchewan

C C C C C H,C

Ontario Canada Canada LI New York Canada Japan

90

7380

40 1200

350 5300

190

24800 340

100

310

327

140

Westoo, 1973 Freemanetal., 1974 Freemaaetal.,1974 Westoo, 1973 Linko and Terho, 1977

Byerofi et al., 1982 Wobeseretal.,1970 21950

200 150 200

Underdaland Hastem, 1971

FreemanetaL, 1Tl4

240 1700

Fimreite and Reynolds, 1973 Fmcmanetal.,1974

Freemanetal.,1974 Jenaen and Fohre~bach 1971 Freemanetal.,1974 Matsunaga, 1975 Frecmanetal., 1974

C

Canada

130

150

c,h

Japan

400

4600

Matsa~ga, 1975

C*

Baltic

80

1120

Nuo~eva and Ita~alma 1975

C* P,e

Baltic Canada

30 I20

450 290

Nuotteva and Itasalmn 1975 Frecmaaetal.,1974

C

Saskatchewan

900

7200

Wobeser et al., 1970

C

Canada

| 20

190

Freeman et al., 1974

C

Canada

120

190

Freemmaet al., 1974

C*

commercial

C* P C*

Canada Canada commefical

200 90

260 120

C* C

New Yoek Ontario

190 1329

660 3~61

Bache et aL, 1971 Scott, 1974

700

1700

Wobeser etal., 1970

Fl~.cmalletal., 1974

C

Saskatchewan

C

Canada

60

I00

C

Canada

80

160

P,h

LI New York

300

Wobeseret al., 1982

800

FleemaJaet ai., 1974 Freeman et al., 1974 Wobeseret al., 1982

Freeroanetal., 1974 90

Jensen and Fobxenbach 1971

MERCURY BIOACCUMULATION IN PUERTO RICO

191

Table V (continued) Species

Menhaden Mooneye (Hiodon teraisus) Northern Pike Northern Pike NorthernPike Northern Pike Notahem Pike Northern Pike Northern Pike No.hem Pike Northern Pike N. Redhorse (Moxostoma ~pp) Pacific Hake (Merluccius productto) Perch (Perca fluviatilis) poloek (Pollachius virens) Rainbow trout (Salmo gairdneri) Redfish (sebaaes marinus) Roach (Rutilus rutilu~) Rock Bass (Ambloplites rupearis) Sauger (Stizoaedion canadense) Sauger Sea Raven (Hemitripterus amerlcanus) Sea Trout (Sa lmo ocla ) Sea Trout Shad (Alosa sapidisaima) Silver Hake

Trophic Levela

Cotmtry

Pja C

Canada Saskatchewan

C* C* C* C* C* C* C* C* C* C

Sweden Manitoba Ontario Ontario Finland Metatana Saskatchewan Ontario England Seskatohewan

C

Pacific Coast

C

England

C

C~aaada

C* C C~a C

Range m M~sde Min Max (t~ghcg)h 90 110 1600 3600 200 5000

>2000 12000

47141

6723

200 700 3740 80 1000

1600 10600 27800 400 2400

England Ontario

Freeman et a l,, 1974 Wobe~ et aL, 1970

430

Hakamon et al., 1988 Scott and Armstrong, 1972 ~te and Reynolds, 1973 Scott, 1974 Linko and Terho, 1977 PFillipsetaL, 1980 Wobaser et aL, 1970 Famreite and Reynolds, 1973 Bull et aL, 1981 Wobeser et aL, 1970

85

383

Oatxball et al., 1978

100

500

Bull et al., 1981

80

50

commercial Canada

Reference

Meaa Value

Freemim et a l. ,19"14 1000

Wol~seret al., 1970

130

160

Freeman et al., 1974

40

320

Bull etal., 1980

550

10900

1100

1500

Wobeser et aL, I970 Phillips et al., 1980 Fxeeman et al., 1974

Fiameiteand Reynolds, 1973

C*

Saskatchewan

C* C*

Montana Canada

190 290

1400 450

C*

Sweden

257

271

Westoo, 1973

C* p

Sweden Canada

343 90

469 110

Westoo, 1973 Freeman et al., I974

60

90

280

720

C*

Canada

C*

New Zealand

C*

LI New York

C*

Canada

240

420

C*

Ontario

1500

19600

C* C* C* C* C* C* C* C

Manitoba Ontario Momam Ontario Wis~ Michigan Saskatchewan Montana

300

500

100 6110 410 140 600 I00

1300 7748 1740 470 5300 600

Scott and Armstrong, 1972 Fixmeiteand Reynolds, 1973 Pldlips et al., 1980 Scott, 1974 Jcmen, 1988 Kelleyet al,, 1975 Wobeser et al., 1970 PbJllips et aL, 1980

h,c

Ontario

1000

4190

~ite

h,c h,c h,c C

Manitoba Ontario Saskatchewan Canada

20 1866 700 170

200 2490 11200 200

Scott and An~trong Scott, 1974 Wobescr et al., 1970 Freemala et aL, 1974

C

Saskatchewan

1400

1400

Wobeser et al., 1970

h,c

Japan

1800

2800

Matstmaga,1975

F,xeeroan et al., 1974

(Merluceius bilinea~s) Snapper

(Chrysaphrys auratus) Striped Bass (Morone ~ t i l a s ) Thorny Skate (Raja radiata) Walleye (Stizon~edion vitre~n) Walleye Walleye Walleye Walleye Walleye Walleye Walleye W~te Crappie (Pomox~s armulans) White Sucker ( Cato$tomus cormr~rsoni) Wlfite Sucker White Sucker White Sucker Whtter Flounder (Pseudopleurnectes amerieanus) Yellow Perch (Perca flavescens) (Zaccotetmninchku)

a From Bigelow and Scl~oedsr, 1953;WhJtworth et al., 1983; and tba papers re fereno~d in the table. b Cort*eted to/~g/kg wet weight where possible. Dry weight values weTed~vi&dby 3 to esttmate wet weight.

Robertson et aL, 1975 300

Jemen and FohIenbach 1971 Freeman et al., 975 Fimr~te and Reynolds, 1973

360

and Reynolds, 1973

192

JOANNA BURGERET AL.

TABLE VI Mercury in fish from Puerto Rico and the VirginIslands (range of mean values in/zg/'kg). Barbu Barracuda Blue-striped Grunt Bonefish False Pilchard Frigate Mackerel Gray Snapper Green Moray Hammerhead Shark Houndfish Ladyfish Lemon Shark Mullet Nurse Shark Ocean Surgeon Porcupine Fish Queen Triggerfish Red Drum Red Snapper Rock Hind Schoolmaster Sharpnose Shark Spadefish Spanish Mackerel Spotted Eagle Ray Spotted Goatfish Spotted Goatfish Tarpon Thread Herring Tiger Shark West Indian Sardine Whalebone Anchovy Yellow Goatfish YeUowfin Mojarra Yellowtail Snapper

824 271 - 968 70 40 - 160 590 70 - 840 700 190 440 190 730 310 80 - 220 490 25 78 75 - 822 114 736 290 - 304 155 240 - 1290 194 230 - 770 130 650 110 200 50 - 200 1160 271 40 110 87 83

s u c h that the e a r l i e r s a m p l e s do n o t a d e q u a t e l y reflect the areas w e s a m p l e d i n 1988. I n birds, m e r c u r y levels h a v e b e e n m e a s u r e d i n eggs a n d i n a v a r i e t y o f tissue i n c l u d i n g liver, m u s c l e , b l o o d heart, b r a i n , k i d n e y a n d feathers o f adults. I n g e n e r a l ,

19 3

MERCURY BIOACCUMULATION IN PUERTO RICO

TABLE VH Mercury levels in birds reported in the literature (#g/kg or ppb wet weight) shows mean -4- S.D. For trophic level H = herbivore, C = carnivores, P = plankton. Capital letter indicates the primary foods. Species

Trophic

Liver

Muscle

Source

C,h

450

70

Branne, 1987

C,h

370

40

Braune, 1987

1060 4- 600

990 4- 286

Level Bonaparte's Gull Larus philadelphia Black-legged Kittiwake Rissa tridactyla Common Tern

C

Sterna hirundo

(405b)

Gochfeld, 1980 Gochfeld, unpubl.

Common Tern

C

1250

120

Braune, 1987

Arctic Tern

C

470

90

Braune, 1987

Sterna paradigaea Laughing Gull

C,h

880 (500-1600)

King and Cromartie,

Black Skimmer

C

1420 (600-1600)

King and Cromartie,

Atlantic Puffin

C

118 4- 4.98 (98.3-151)

Larus atricilla

1986 1986

Fratercula artica Black Guillemot

46700 4- 1190

Osbom etal., 1979

(41500-53400) C

510

110

H

500 4- 60 (100-2340)

Parslow etal., 1982

900 -- 400 (140-2260)

Parslow et aL, 1982

H,c

1200 -4- 100 (50--4620)

Parslow et al., 1982

H,c

3700 4- 500 (160-12140)

Parslow et al., 1982

H,c

1500 4- 100 (150M370)

Parslow et aL, 1982

H,c

600 4- 100 (320-970)

Parslow et al., 1982

3000 4- 300 (470-6440)

Parslow etal. 1982

H,C

2600 4- 1100 (140-13990)

Parslow et al., 1982

H,C

990

Braune, 1987

Cepphus gryUe Eurasian Wigeon Anas penelope Gadwall Anas strepera Gadwall Anas platyrhynchos Pintail Anas acuta Teal Anas crecca Pochard Aythya ferina Shoveler

H,C,p

Anas clypeata Tufted Duck Aythya fuligula Common Eider Somateria mollissima a Cramp, 1977. b Maximum value detected.

150

Braune, 1987

194

JOANNA BURGER ET AL.

average mercury levels reported for avian livers range from 370 #g/kg or 370 ppb) for kittiwakes (Braune, 1987) to 188 000 #g/kg in puffins (Obsbom et al., 1979). For avian muscle, average levels ranged from 90 #g/kg in tems (Braune, 1987) to 46 000 #g/kg in puffins (Osbome et al., 1979). In general, most bird results average less than 1000 #g/kg (Table VII). In general birds that are lower in the food chain (i.e. herbivorous ducks) have considerably lower levels of contaminants than fish-eating species such as terns, skuas, fulmars and puffins. Omnivorous species tend to be intermediate. Thus bioamplification is well documented in birds (Maedgen et al., 1982; Gochfeld, 1980; Gochfeld and Burger, 1987), as well as in fish. Fumess et al. (1990) reported that Red-billed Gulls (Larus novaehollandiae) do not show increasing levels of mercury with age. Herons and egrets generally have intermediate levels. They eat a wide variety of aquatic and terrestrial food. The highest mercury level reported in a heron was 143 000 #g/kg. The few studies that report mercury in muscles of herons and egrets range from 100 to 2715 #g/kg, with most reporting average levels below 1000 #g/kg. Cattle egrets have seldom been studied, and published accounts refer to metals other than mercury (Hulse et al., 1980). Similarly, Moorhens and related marsh birds have received little attention. At the Puerto Rican study sites we detected mercury in only one sample of egret muscle from Boqueron and one sample of Moorhen muscle from Humacao. There was detectable mercury in the composite liver samples from egrets at both sites, as well as in Moorhens from Humacao. However, the maximum value detected was 160 #g/kg, well below the values reported for either liver or muscle in most studies. Thus, these species tend to indicate relatively low mercury contamination in the estuaries we studied. Finally, the results of this study demonstrate the importance of baseline data and of publishing data with relatively low levels. Overall, our study indicated that several different trophic levels had no detectable levels, and when there were detectable levels, they were relatively low compared to those reported in the literature despite concern over possible presence of mercury at Humacao. Both the percentage of samples with detectable levels and the levels in samples with mercury, were low. Yet the literature has few reports of low or non-detectable levels. This renders it extremely difficult to ascertain the true world-wide levels of contamination. We feel the trend to avoid publishing low levels or non-detectable levels (because they were not interesting?) makes us unable to adequately evaluate higher levels. And more studies are needed to allow comparisons among habitats and species.

Acknowledgements We thank M. Arciezewski, J. Collazzo, and Dynamac, Inc. for logistical support. M. Corbett, J. Rodriquez and E Mestey allowed and facilitated access to the Humacao, Boqueron and Roosvelt Roads sites respectively. B. Cintron was extremely

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