Persistence, phytotoxicity, and management of arsenic, lead and mercury residues in old orchard soils of New York State

Chemosphere,Vol. 29, No. 6, pp. 1361-1367, 1994

Pergamon

Copyright O 1994 Elsevier Science Ltd Printed in Great Britain. All fights reserved 13045-6535/94 $7.130+0.00

0045-6535(94)00218-5

PERSISTENCE,

PHYTOTOXICITY, AND MANAGEMENT OF ARSENIC, LEAD AND MERCURY RESIDUES IN OLD ORCHARD SOILS OF NEW YORK STATE

Ian Merwin, l Patrick T. Pruyne, I Joseph G. Ebel, Jr., 2 Kerry L. Manzell, 2 and Donald J. Lisk I" IDepartment of Fruit and Vegetable Science New York State College of Agriculture and Life Sciences ~ e t e r i n a r y Diagnostic Laboratory, Division of Toxicology New York State College of Veterinary Medicine Cornell University, Ithaca New York 14853

(Received in USA 15 June 1994; accepted 11 July 1994)

ABS~I&CT Load arsenate was used for pest control in fruit orchards for many years in the United States, and its rooldues remain in most of those soils. Since arsenic and load are toxic and only slightly mobile in soils, an analytical survey was conducted in 1993 to determine the concentrations of those elements persisting in sell samples from 13 older and newer orchards in Now York State. Concentrations of arsenic and load ranged, respectively, from 1.60 to 141 and from 1.48 to 720 (ppe, dry wt). Significant (P < 0.01, n - 13) pairwlee corrolatlons wore observed among concentrations of these olomentsz As vs. Pb (r - 0.97), As vs. Hg (r - 0.79), and Pb vs. Hg (r - 0.83). Despite previous reports of phytotoxicity to fruit trees, elevated arsenic concentrations did not significantly reduce the dry weights of apple (Nalus domescica) soodllngs grown in pasteurized soil from these orchards. The general environmental effects and best management strategies for arsenic and lead in orchard soils are discussed including phytotoxlclty of arsenic and its uptake and accumulation in plants, ingestion by small man,hal herbivores and their predators in orchards, and ways to minimize potential adverse effects on humans. II~ODUCTIOM

Lead arsenate was often used for pest control in apple and other fruit orchards in New York State from the 1930e to 1960s.

To a lesser extent, fungicides containing organic mercury were

also used for control of diseases such as apple scab (Venturia inaequalis). Very high application rates of lead arsenate, common in many orchards.

some exceeding 3300 ks/ha (Jones and Hatch 1937), were

Since arsenic and lead are relatively immobile in soils, the

accumulation and persistence of residues in the upper soil profile are to be expected.

There

have been past reports of phytotoxlcity to newly planted fruit trees and other crops from arsenic residues in such soils

(Sheppard 1992), and this may be a factor in tree replant

problems at some old orchard sites (Peryea, 1991a; Benson st al. 1978).

Possible adverse

health effects in humans, pets, grazing animals and wildlife are also of concern where houses, gardens or forage crops now occupy old orchards.

It wa~ therefore of interest to determine

the magnitude of residues of these elements remaining in old orchard York State, and posslble mammalian or phytotoxlc impacts.

soils throughout New

In the work reported here, soils

were collected from 13 sites with recent or historical tree-fruit plantings. concentrations of arsenic,

The total

lead and mercury were determined, and phytotoxlcity to apple

seedlings was assayed under controlled environment conditions. EXPERIMENTAL

Thirteen orchards in the major fruit growing regions of New York State were selected to provide a representative

sample of various sell types and pH, organic matter content,

and

cropping histories (Table 1). Except where crops other than tree-frults had been grown, the *Address all correspondence

1361

1362 Table 1. Soil textural classifications, pH, organic matter (loss-on-ignition dry wt), and previous cropping history at 13 orchard sites sampled in New York State during 1992 and 1993. Soil Type

pH

Organic matter

Arkport (coaree-loauny mixed, mesic psammentic hapludalfs)

6.7

1.9

Old apple orchard

Chenango (loamy-skeletal mixed, mesic typic dyetochrepts}

6.3

6.3

old apple orchard

Lackawanna (coarse-loamy, mixed, mesic t[sic fragiochre~ts)

6.4

4.4

old apple orchard

Hoosic (sandy-skeletal mixed, mesic typic dystrochrepts)

6.9

3.7

old corn and hayfield

Arkport

6.8

1.4

Old apple orchard

Arkport

6.8

1.3

Old apple orchard -> Sudan grass

Mardin (coarse-loamy mixed, mesic typic fragiochrepts)

6.8

6.3

old woodlot -> apple

Arkport

6.5

1.8

old cherry orchard

Bernardston (coarse-loamy mixed, mesic udic fra~iochre~ts)

6.9

5.7

old pasture -> a~le

10

Ark~ort

6.4

2.0

Old apple orchard

11

Bath (coarse-loamy mixed, mesic typic fragiochrepts)

6.2

5.4

old pear orchard

12

Colonie (fine-sandy mixed, mesic typic udipsamments)

6.9

4.1

Old cherry orchard

13

Oakville (fine-sandy mixed, mesic typic udipsamments)

5.9

3.2

old apple orchard

site

Cropping history

(%)

soils had presumably not been deep-plowed since the era of lead arsenate applications.

At

each site, bulked composite samples of 30 to 50 soil cores were taken during 1992 and 1993, beneath 15 to 30 randomly selected trees, to a depth of 25 cm. debris and all stones or woody roots were discarded, by tumbling.

The top 1 to 2 cm of organic

and each sample was air-dried and mixed

Samples were ground to a fine powdery consistency and again mixed prior to

elemental analysis.

For determination of arsenic and lead, a 0.5 g portion of each sample was

transferred to a Kjeldahl flask, 5 ml of concentrated nitric acid and 2 ml of 70% perchloric acid were added.

The mixture was then heated until white fumes of perchloric acid appeared,

and refluxed for 30 minutes.

Digestion with nitric and perchloric acids has been shown to

release 98% of total soil lead as compared to digestion with nitric acid, potassium perchlorate and hydrofluoric acid (Veneman et al. hydrochloric acid and mixed. solution, respectively,

1982).

The digests were diluted to 25 ml with IN

Arsenic and lead were then determined in the supernatant

by Zeeman effect electrothermal

(Eckerlin et al.

1987) and flame

atomic absorption spectrophotometry.

Mercury was determined using a 2-g portion of soil by

cold vapor atomic adsorption analysis

(Hatch and Ott 1968).

For the apple-seedling bioassays, clay pots, steam-pasteurized

soil from each sample was placed into four replicate 0.5 1

at 70°C for 30 minutes, and then ventilated for i0 days at 20°C.

Open-pollinated 'Northern Spy'

apple seeds were collected,

surface disinfected in a 10% Clorox

solution, dusted with captan fungicide and stratified at 4°C for several months in moist, sterile vermiculite.

Sprouted seedlings were later selected for uniformity of development and

transplanted to moist vermiculite trays in a walk-in growth chamber maintained at 16 hr of light (400 pE m'2s"I) and 22°C. selected for uniformity,

After ten days, seedlings with 4 to 6 leaves were again

and one seedling was transplanted into each pot of soil from the 13

1363 orchards. Seedlings were watered daily and fertilized every I0 days with a liquid formulation containing all the essential plant macro and micro nutrients.

After 70 days in the growth

chamber, seedlings were harvested, dried for 24 hours at 70*C, and weighed. RESULTs AND DISCUSSION

Concentrations of arsenic, lead and mercury in these soils varied substantially (Table 2) ranging from 1.60 to 141 ppm (dry wt) for arsenic, and 1.48 to 720 for lead.

The magnitude

and variation presumably were dependent on cumulative lead arsenate applications at each site in the past.

Apparently the soils at sites 5 and 6 had not received lead arsenate applica-

tions and represent natural background levels of these elements.

Similarly, in the case of

mercury, soils at sites 1 and 5 may represent natural soil concentrations.

Organic mercurial

fungicides were typically applied less frequently and at much lower rates than arsenic and lead on apples.

Therefore, mercury concentrations in soil would expectedly be far lower than

those of arsenic or lead.

Since the upper 25 cm of soil at each sampled site was combined

prior to analysis, no inferences can be made regarding the downward migration of these elements in the upper soil profile.

However, progressively decreasing residues of arsenic and

lead at increasing depth in lead arsenate-treated orchard soils have been reported (Aten et al. 1980; Frank et al.

1976; Veneman et al. 1983).

For example, Venemen et al.

(1982)

observed that arsenic and lead in an old orchard silt loam soil had not migrated downward below 20 cm.

In tests fifteen years after sludge amendments and deep plowing, Stearns and

Wheeler (1991) reported that essentially all of the detectable arsenic, lead and cadmium residues remained in the upper 40 cm of a New York orchard.

Although arsenic is considered to

be more mobile than lead in soils (Sheppard 1992), the correlation coefficients (r) among arsenic, lead and mercury concentrations in our soil samples were all significant (P < 0.01, n = 13):

As vs. Pb (r = 0.97);

As vs. Hg (r = 0.79); and Pb vs. Hg (r = 0.83}.

This indicates

that arsenic, lead and mercury have not migrated downward at different rates in these soils, and that most of the residues of these three elements were probably included in the topsoil sampled. The apple seedling soil bioassays provide a useful test of the residues (Table 2).

phytotoxicity of arsenic

Soll pasteurization eliminates soilborne plant pathogens, and the

provision of liquid nutrient solutions minimizes nutrient limitations to apple seedling growth in these tests (Hoestra 1968).

These bioassays therefore provide a useful evaluation of soil

arsenic phytotoxicity to apple trees in the absence of other biotic limitations.

Despite past

reports of reduced yields and fruit tree growth in soils with high concentrations of arsenic (Benson et al. 1978; Sheppard 1992), our linear regression of plant biomass on soil arsenic residues indicated no significant phytotoxicity in these soils (Fig. 1).

These results are

also consistent with observations of excellent apple tree growth, fruit yields, and vegetable crop production in a New York orchard soil amended with sewage sludge, and containing high soil concentrations of arsenic (61 ppm), lead (260 ppm), cadmium (44 ppm), and other toxic heavy metals (Elfving et al., 1978; Sterns and Wheler 1991; Merwin and Stiles 1994). Elevated concentrations of arsenic and lead in soils can affect many other parts of the environment, and there are several sources of error to consider in studying the concentrations of arsenic and lead in old orchard soils and in plants grown thereon.

Records of spray

history may be nonexistent or incomplete, making it impossible to reliably estimate the total quantities of arsenic or lead applied in the past.

The extent of disturbance or mixing of

soil profiles over the life of the orchard by deep cultivation may also be uncertain. Extraneous sources of lead such as vehicle exhaust or sewage sludge applications may be involved.

Lead pellets from past hunting in the area could also contaminate samples.

Finally, the accumulation of arsenic and lead in soil-dwelling animals and predators higher in the trophic hierarchy will depend upon whether they inhabited old orchard soils exclusively throughout their lifetimes.

1364

T~le 2. Soil concentrations of arsenic, lead and mercury and total dry weights of apple seedlings grown for 8 weeks in orchard soils sampled in New York State in 1992 and 1993.

Site

Parts per million tdrv wt) Lead Mercury

Arsenic

1

18.5

0.01

14.7

2

141

599

0.26

7.6

3

125

720

0.55

9.0

0.05

2.1

4

51.3

Seedling dry wt(g)

1.60

21.4

5

1.80

1.48

0.02

12.7

6

3.00

1.48

0.04

8.7

7

6.00

8

22.9

9

5.00

21.4

0.06

8.6

91.1

0.06

9.7

61.3

0.08

11.4

10

48.5

151

0.06

6.2

11

74.0

290

12

9.00

13

24.8

)5

,

,

,

I

,

,

.

I

,

,

,

I

0

,

.

,

0.52

6.6

41.3

0.05

7.3

81.2

0.11

0.11

I

I

,

,

I

,

,

•

I

•

•

•

I

•

,

,

,

•

Y = 9.923 - .019 * X; R^2 = .13

)4 13 ~= 12 O

~11 •

lO

8

7 o •

0

,

.

a

20

•

,

,

i

40

, ~ ,

,

i

60

•

,

,

i

•

,

,

i

80 100 Arsenic (ppm)

•

,

,

|

120

•

,

,

i

•

140

160

Fig. 1. Regression of apple seedling dry weights on soil arsenic concentrations in 12 old orchard soils. Arsenic was not a significant predictor of variation in seedling biomass (P=0.25 for the linear model, standardized slope coefficient = -0.36). One outlier was removed from the analysis. ~ o t a l dry plant weight.

For determination of arsenic or lead content in plants grown in contaminated soils, it is possible to analyze above-ground crops if they are thoroughly cleaned, and root crops such as carrots (Daucus carota) if they are first cleaned and peeled to remove adhering soil particles.

However, it is difficult (and perhaps not desirable if human ingestion is being

estimated) to completely remove all adhering and embedded soil particles from the fibrous root systems of grasses, or convoluted leafy vegetables such as broccoli or kale (Brassica oleracea).

Nevertheless, several studies have dealt with the magnitude of arsenic and lead

uptake by vegetable and fruit crops grown on lead arsenate-treated orchard soils.

Elfving et

1365 al.

(1978) r e p o r t e d t h a t p e e l e d carrot roots and onion

b u l b s g r o w n on a silt

(Allium cepa)

loam o r c h a r d soil c o n t a i n e d 0.9 and 0.4 p p m arsenic and 7.1 and 0.8 p p m lead, respectively. R e s i d u e s of a r s e n i c and lead w e r e n e g l i g i b l e or v e r y low in the e d i b l e p o r t i o n of beans, cabbage, p o t a t o e s and tomatoes.

In another study, apple leaf, peel and p u l p as well as potato

leaf and peel g r o w n o n a r s e n i c t r e a t e d o r c h a r d soils were s i g n i f i c a n t l y h i g h e r in arsenic residues

(Maclean and L a n g i l l e 1981).

A recent study by Creger and P e r y e a

(1992) in lead

a r s e n a t e - c o n t a m i n a t e d o r c h a r d soils r e p o r t e d that arsenic content in a p r i c o t

(Prunus

and a p p l e fruit was p o s i t i v e l y correlated w i t h H C l - e x t r a c t a b l e soil arsenic, but

armeniaca)

lead was not d e t e c t a b l e

in t h e s e fruits.

It is very important to note that the concentrations

of a r s e n i c and lead d e t e c t e d in crops grown in all of the a f o r e m e n t i o n e d o r c h a r d studies r e m a i n e d s u b s t a n t i a l l y b e l o w levels c o n s i d e r e d hazardous to h u m a n health. Sheppard

(1992) c o m p r e h e n s i v e l y s u r v e y e d the literature d e a l i n g w i t h p h y t o t o x i c i t y of arsenic

in a g r i c u l t u r a l

soils.

S t u d i e s g e n e r a l l y indicate that arsenic has low m o b i l i t y in soils, and

that i n o r g a n i c s o u r c e s are less t o x i c than organic sources. more a c u t e l y p h y t o t o x i c

about 40 m g / k g soil) t h a n in clay soils Monocotyledonous phytotoxicity.

Inorganic s o u r c e s of arsenic are

in p r e d o m i n a n t l y sandy and loamy soils

(threshold t o x i c concentrations

(threshold c o n c e n t r a t i o n s about 200 m g / k g soil).

and d i c o t y l e d o n o u s plants are e v i d e n t l y e q u a l l y s u s c e p t i b l e to arsenic M a n a g e m e n t of c o n t a m i n a t e d soils appears to affect the p e r s i s t e n c e and plant

a v a i l a b i l i t y of arsenic.

Peryea

(1991a) r e p o r t e d that r e l e a s e of a r s e n i c i n c r e a s e d after

f e r t i l i z a t i o n w i t h m o n o a m m o n i u m p h o s p h a t e and m o n o c a l c i u m phosphate. that use of p h o s p h a t e

p o t e n t i a l for a r s e n i c p h y t o t o x i c i t y or c o n t a m i n a t i o n of g r o u n d w a t e r 1991).

However,

It has b e e n suggested

f e r t i l i z e r s on lead arsenate c o n t a m i n a t e d soils m a y t e m p o r a r i l y enhance (Davenport and Peryea

in a n o t h e r study w h e a t seedlings in nutrient s o l u t i o n c u l t u r e s w e r e

r e p o r t e d l y p r o t e c t e d a g a i n s t a r s e n i c p h y t o t o x i c i t y if sufficient p h o s p h o r u s was also p r o v i d e d (Hurd-Karrer 1936). R e s i d u e s in lead a r s e n a t e - t r e a t e d soils can also affect soil a n i m a l s and t h e i r predators. E a r t h w o r m s h a v e b e e n s h o w n to c o n c e n t r a t e lead from soils

(Ash and Lee 1980; M o r g a n and Morgan

1988; G i s h and C h r i s t e n s e n 1973; Beyer and Cromartie 1987; Ireland 1979). (1978; 1979) and H a s c h e k et al. tissues of m e a d o w v o l e s

E l f v i n g et al.

(1979) showed that lead content in kidney,

(Microtus

spp.) trapped in two old o r c h a r d s w a s

to 300 ppm) t h a n in c o n t r o l animals

(up to 33 ppm).

liver and bone

m a r k e d l y higher

(up

Intranuclear i n c l u s i o n b o d i e s diagnostic

of c l a s s i c a l lead p o i s o n i n g w e r e found in the renal epithelial cells of v o l e s from lead arsen a t e - t r e a t e d orchards.

W h o l e body arsenic content of voles and m i c e from c o n t a m i n a t e d

o r c h a r d s was c o r r e l a t e d w i t h the c o n c e n t r a t i o n s of arsenic in soil Since t h e s e a n i m a l s are subterranean,

(Elfving et al.

1979).

they p r o b a b l y become c o n t a m i n a t e d by i n a d v e r t e n t

ingestion of a r s e n i c - and l e a d - c o n t a i n i n g soil particles as they forage on soil insects and plant root m a t e r i a l . days,

W h e n v o l e s w i t h e l e v a t e d lead content w e r e fed to l a b o r a t o r y cats for 86

lead c o n c e n t r a t i o n s

c o m p a r e d to c o n t r o l s

i n c r e a s e d 5- to 10-fold in feline kidney,

(Gilmartin et al.

1985).

liver and b o n e tissue

O t h e r o r c h a r d p r e d a t o r s such as owls, hawks and

fox w o u l d p r o b a b l y c o n c e n t r a t e lead similarly to the cats e x p e r i m e n t a l l y fed m e a d o w voles. Similarly,

b i r d s e a t i n g e a r t h w o r m s are likely to a c c u m u l a t e and c o n c e n t r a t e lead from

c o n t a m i n a t e d sites. There is p r e s e n t l y m u c h c o n c e r n about the p o s s i b l e human health e f f e c t s of lead.

When

r e s i d e n c e s are b u i l t on old o r c h a r d soils, c o n t a m i n a t i o n of g a r d e n crops and h a n d - t o - m o u t h ingestion of soil b y y o u n g c h i l d r e n may occur. health have b e e n d o n e

(Hawley,

M a n y studies of lead in soil and children's

1985; M a d h a v e n et al. 1989; van W i j n e n et al. 1990), w i t h mixed

c o n c l u s i o n s a b o u t t h e m a g n i t u d e of actual risks from soil sources. studied p r o f e s s i o n a l

N e l s o n et al.

and o b s e r v e d no c l e a r r e l a t i o n s h i p b e t w e e n exposure times, h e a l t h e f f e c t s disease,

and cancers)

(1973)

fruit g r o w e r s who had used lead a r s e n a t e r e p e a t e d l y for u p to 21 years, or l o n g e v i t y in c o m p a r i s o n to an u n e x p o s e d group.

(cardiovascular

1366

How should lead arsenate-contaminated old orchard soils be managed?

In a recent study,

8charpenseel and Becker-Heidmann (1990) recommended soil remediation when the concentration of arsenic in soil was >2.5-fold above background levels.

Significant removal of arsenic has

been accomplished by amending soils with apple pomace as a carbon source and flooding them. Under these conditions biomethylation of arsenic and evolution of methylarsine occurred (Peryea 1991b). orchards.

The best management strategy may be to maintain contaminated sites as

If fruit trees are removed and these soils are cultivated or otherwise disturbed,

increased erosion and transport of arsenic and lead out of the site on soil particles is likely.

If forage crops are planted, grazing animals can be exposed to arsenic and lead.

Aside from uptake of these elements on consumed vegetation, livestock often tear out plants by the roots while grazing, and consume significant quantities of soil that is occluded to plant roots (McGrath et al. 1982).

As noted earlier, the risks of ingestion by humans or other

herbivores are also increased where leafy or root crop vegetables are produced in contaminated soils.

However, in most orchards there is minimal disturbance of the soil, groundcover

vegetation is not harvested for forage, and human activities are restricted for much of the year because of the routine applications of crop protectants necessary to produce marketable fruit.

Studies have shown that tree fruits grown in contaminated soils do not contain

hazardous residues of lead or arsenic (Creger and

Peryea 1992; Sheppard 1992).

Fruit trees

can apparently tolerate relatively high soil concentrations of these elements without serious phytotoxlcity.

These circumstances suggest that fruit growing is perhaps the best strategem

for productive use of old orchard sites while historical lead arsenate burdens slowly dissipate. REFERENCES

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