Trophic accumulation of DDT in a terrestrial food web

Enlirtmmenta/Polhltion (St'rie~ A) 25 (1981) 219 228

TROPHIC A C C U M U L A T I O N OF D D T IN A TERRESTRIAL F O O D WEB

R. L. RUDD,R. B. CRAIG* t~LW. S. WILLIAMSt

Department of Zoology, Universityof CaliJbrnia, Davis, California 95616, USA

ABSTRACT DDT was aerially applied to a 13-ha plot adjacent to croplands at the low rate of 0.22kg/ha (0.21bs/acre). Modular food-web relationships in this simplified agroecosystem were linked with DDT residues. Soils, vegetation and tissues of resident biota were analysed for total residues at regular intervals (up to 2 years) subsequent to application. Herbivores ( orthopterans, homopterans, coleopterans and lepidopterans) showed an immediate uptake of DDT-R in tissue, jollowed by a precipitous decline and then stabilisation or slight long-term incline in concentrations. Carnivorous arthropods (arachnids" and coleopterans) and birds (loggerhead shrikes) initially showed a similar pattern followed by unexpected trophic increase. However, the time-span of uptake was greatly extended. Results indicate a two compartment mode of uptake--one fast, one very slow--the latter dependent on trophic concentration alone. Time delay in carnivores must be related to both trophic factors and individual life histories within the feeding guild. Ecological hazard was exhibited in only one feeding group (shrews) after experimental treatment. Shrews were totally absent from the area after DDT application.

INTRODUCTION

T h e i m m e d i a t e effects o f the i n t r u s i o n o f toxic chemicals into the e n v i r o n m e n t have been described for m a n y decades ( R u d d & Genelly, 1956; R u d d , 1964) a n d were early c o n s i d e r e d as the m o s t h a z a r d o u s aspect o f their presence. L a t e r studies m a d e clear that not only were longer term effects o f persistent chemicals a n d their altered * Present address: Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37830, USA. 5" Present address: Tacoma Family Medicine, 19th & Union Sts, Tacoma, Washington 98405, USA. 219 Environ. Pollut.Ser. A. 0143-1471/81/0025-0219/$02.50 ~' Applied Science Publishers Ltd, England, 1981 Printed in Great Britain

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R . L . RUDD, R. B. CRAIG, W. S. WILLIAMS

residues more biologically hazardous, but that their effects were less predictable and analysis of such effects more difficult. A retrospective view indeed reveals that early intuitive suspicions of both degrees of hazard and complexities of analysis were only the tips of icebergs. The difficulties of ecological analysis and prediction were particularly underestimated. Chemical applications, irrespective of target or of chemical nature, impose stresses on entire ecological communities (Odum, 1969; Barrett et al., 1976). Normally, however, research studies have been autecological or centred on single physiological phenomena such as reproductive inhibition. Our earlier work on the intentionally contaminated Clear Lake, California, ecosystem, for example, focused on the reproductive failure, for more than 15 years, of a population of western grebes, all of which accumulated and stored high levels of chlorinated hydrocarbon residues in fatty tissues (Rudd, 1964; Herman et al., 1969; Rudd & Herman, 1972). Such a focus diverts attention from community-wide effects and emphasises simpler descriptions (e.g. food-chain transfers). Important as many of these descriptions are (e.g. studies of egg-shell thinning), they rarely lead to ecological generalisations essential to proper comprehension of the degree of environmental contamination, particularly at such a level as to frame appropriate controlling legislation (Kenaga, 1972). The 'Odum School' has placed emphasis on community responses to induced stresses (chemical and other) in man-altered ecosystems (Barrett, 1968; Woodwell, 1970). Our studies at Clear Lake resulted in descriptions of food webs to include levels of pesticide residues in living components in this well-studied, semi-enclosed aquatic ecosystem. Particular features of these efforts were the construction of predictive models describing the ecokinetics of residues in restricted ecological and physiological pathways and more generalised graphic and mathematical compartmental models describing food-webs and energy pathways within the ecosystem (Rudd & Herman, 1972; Craig & Rudd, 1974; Rudd, 1975). The Clear Lake graphic model was reduced to twelve functional compartments. We also applied this type of analysis to a terrestrial environment (Craig & Rudd, 1974). An eight-compartmental graphic model was proposed to describe the foodweb in a simplified agroecosystem near Davis, California. Subsequent community analyses focused on feeding guilds and consumer levels. Comparable methods of analysis are suggested in Harrison et al. (1970) and Schoener (1974). Compartments were studied with an underlying consideration of community energetics. Particular attention was accorded to a resident passeriform predator, the common loggerhead shrike Lanius ludovicianus gambeli Ridgway. Publications derived from this study to date are those of Craig & Rudd (1974), Craig (1978) and Craig et al. (1979). DDT application to the study area was made after completion of the model. The low level of pesticide applied was intended to mark trophic pathways, to assess sites of concentration and to uncover long-term ecological effects of residue presence in a simplified agricultural environment. It was prejudged to have little or no immediate

DDT

IN A TERRESTRIAL FOOD WEB

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toxic effect (although, in one instance, our prior judgement was shown to be significantly incorrect).

METHODS

The study site was a fallow area between intensively worked agricultural fields. The natural drainage (Willow Slough) was leveed and gravelled roads ran through the study area on the tops of levees. The location is 3-2 km north-east of Davis, Yolo County, California. The study area is a thin rectangle, 0.4 x 3.2 km in dimension. Most animal life is concentrated on slough and levee margins. Summer rains rarely occur but irrigation run-off from adjacent croplands ensures available surface water at all seasons. Technical D D T was aerially applied to 13 ha at the site at the rate of 0.22 kg/ha (0-21bs/acre) in May 1972. The eight graphic components of our model (soil, vegetation and major animal guilds) were sampled before and immediately after application and at regular intervals when permissible for the following year. Casual observations and collections continued for over two years. Visual observations on a regulated basis accompanied sampling activities. Soil, vegetation and insects were removed from within the area of a randomly thrown 0-5 m 2 ring. Five replications were made on each sampling day. Soil was cored to a depth of 12cm; all above-ground vegetation within the ring area was clipped and removed. All insects within the ring area were removed from surface soil and vegetation before clipping by a powerful portable gasoline-operated vacuum suction machine ('D-vac'). Supplementary insect samples were taken in standardised sweep-net transects. Small mammals were taken in both live and kill traps. Birds were shot. All animal samples were washed with hexane, sealed in aluminium foil and frozen for later segregation. Insects were hand sorted and identified to both major taxon and feeding guild. Efforts were made in each category to replicate five times per daily sample. Sufficient mass for chemical analysis was considered to be 5 7 g for each sample and was not always achieved. Insects were pooled for analysis; on occasion thousands of individuals per guild were needed for a single.pesticide analysis. Since we were interested in patterns of residue distribution--and since costs of analyses were limiting--we have shown only mean values of DDT-R concentrations in the accompanying figures (Kenaga, 1972). DDT-R in this instance represents the additive concentrations of DDT, D D D and DDE. Other pesticide residues (origins unknown) were occasionally found to be present in individual samples in small but measurable amounts. These residues were aldrin, dieldrin, heptachlor epoxide and lindane. All chemical analyses were independently made by California Analytical kaboratories~ Sacramento.

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R.L.

RUDD,

R . B. C R A I G ,

W . S. W I L L I A M S

RESULTS

Chemical residue levels in soil and vegetation were surprisingly high before application (Table 1). We are unable to identify sources for the observed levels. No direct application of DDT has been made in the areas for many years. These are 'fossil' residues and illustrate well the ubiquity and persistence of some chemical classes. TABLE 1 CONCENTRATIONS OF DDT-R IN SOIL AND VEGETATION BEFORE (DAY 0) AND AFTER SPRAYING WITH DDT AT 0 . 2 2 k g / h a ADJACENT TO CROPLANDS NEAR DAVIS, CALIFORNIA. VALUES ARE MEANS OF FIVE SAMPLES FOR EACH SAMPLING DAY (FRESH WEIGHT BASIS)

DDT-R (ppm)

0

1

9.0

---

28.67

4790

Day 30

60

100

--

71.3

130

--

Soil :~

Vegetation :?

121

We were interested in both 'disappearance' rates from basic ecological compartments of soil and vegetation and the portion available for incorporation into animal food webs. DDT-R levels were very high on vegetation immediately after application, but within one month had markedly declined, as expected, to a low 'steady-state' level confirmed by the sample value at 60 days post-application. Survival values of residues in both soil and vegetation indicate a continuing source of input into the animal community. There is ample evidence of a rapid uptake capability in all higher trophic levels (Tables 2 and 3; Figs 1,2 and 3). A 5-40 fold increase in residue levels occurs in all insects within 8 days of application, irrespective of feeding guild. Surface adsorption and spiracle uptake must be important routes of entry for herbivorous insects, in addition to ingestion, and are lesser factors for predatory insects. Coccinellid beetles have a greater increase in residue levels than herbivorous forms, presumably because of the additive contamination of both the surfaces and the bodies of prey insects whose tissues are contaminated. Arachnids and shrikes delay uptake slightly but magnify concentrations more than insects (200-400 fold). These are predatory animal groups normally less likely to contact contaminated surfaces than herbivorous insects and whose sole source of contamination shortly after application must be considered to be ingested food. Levels in shrikes (Fig. 3) are much higher than are noted in whole body analysis. Skin, subcutaneous fat and brain have high lipid fractions and are normally sites of concentration.

DDT

IN A TERRESTRIAL

FOOD

WEB

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TABLE 2 CONCENTRATIONS OF DDT AND DDE IN INSECT GROUPS NOT ILLUSTRATED IN THE FIGURES BEFORE AND AFTER SPRAYING WITH DDT AT 0"22 k g / h a ADJACENT TO CROPLANDS ]qEAR DAVIS, CALIFORNIA. INDIVIDUAL VALUES REPRESENT SINGLE POOLED SAMPLES (LIPID WEIGHT BASIS). DASHES INDICATE THAT NO SAMPLE WAS TAKEN. DAY 0 REPRESENTS SAMPLES TAKEN IMMEDIATELY PRIOR TO APPLICATION

Taxon

Lepidoptera Adult

Larvae

Coleoptera (herbivore)

Chemical (ppm)

DDT DDE DDT-R DDT DDE DDT-R DDT DDE DDT-R

Day 0

1

2

4

8

16

32

96

0.00 0-36 0.36 0.00 0.407 0.407 2.7 1.12 3.82

---2.47 4.9 7.47 4.3 19.85 24.19

---18.52 51.85 70.37 9.8 14.23 23-03

5-40 10.80 16-20 ---3.0 17.0 20-0

---3.6 7.2 10.8 2.2 14.6 16.8

----12.1 12.1 ----

---12.88 9.14 22.02 ----

0.64 8.16 8.80 ------

Mice, which both ingest accumulated residues and inevitably contact contaminated surfaces, showed relatively low values initially. Absorption through feet and fur must be a minor route of entry. Moreover, house mice prefer to eat fruiting, rather than vegetative, plant parts. Interest in this trophic group lies in its pattern of long-term residue accumulation. Carnivorous mammals (shrews) simply 'disappeared'. Pre-application residue levels were inordinately high, indicating their known unusual ability to concentrate chlorinated hydrocarbon residues and their susceptibility to nervous system toxicants (Nash & Woolson, 1967). We do not believe that our inability to capture shrews after application is due to the vagaries of trapping techniques or to the animals' relative scarcity. Rapid, continuous declines in residue levels characterise all groups within 2-3 weeks following the first week of initial high uptake. This period was followed by a slow decline or stable levels for extended periods. At no time, however, did residue levels reach--or closely approach--the pre-application baseline. TABLE 3 MEAN CONCENTRATIONS (LIPID WEIGHT BASIS) OF DDT-R IN WHOLE BODIES OF MICE Mus musculus AND SHREWS Sorex ornatus BEFORE (DAY 0) AND AFTER SPRAYING WITH DDT AT 0 ' 2 2 k g / h a ADJACENT TO CROPLANDS NEAR DAVIS, CALIFORNIA. FIVE MICE ARE REPRESENTED IN EACH DAILY SAMPLE; THE SHREWS REPRESENT FOUR INDIVIDUALS

D D T- R (ppm) Mice (herbivores) Shrews (carnivores)

Day 0

5

34

70

100

+_365

2.15

4.61

1.79

1.16

2.84

5.27

17.51

No shrews caught after application

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R . L . RUDD, R. B. CRAIG, W. S. WILLIAMS 50

20

E=

40 5

\/ ~/

'1 5O

D D T - R IN ORTHOPTERA (HERBIVOROUS)

I

I

....

I

D D T - R IN HOMOPTERA ANO HEMIPTERA (HERBIVOROUS) 20 '10 o. 5 lq 2 '1 BASELINE

16

52

4.8

64

80

96

'1'12

DAYS

Fig. 1. Concentrationsof DDT-R(Ijpidweight basis) in herbivorousinsects(orthopterans--tOl~-and hemipterans and homopteranscombined--bottom---chewingand sucking insects, respectively)before and after sprayingwithDDT at 0.22kg/ha adjacentto croplandsnear Davis,California.Valuesare from pooled samples representing total biomass.

To this point we recognise three patterns of residue level in all groups: rapid uptake, rapid decline and slow decline with stabilisation at greater than preapplication values. In addition, we recognise a long-term compartment of slowly increasing uptake in four groups of animals dependent on ingested food for residue entry. Orthopteran and arachnid residues turned upward in the third month. Shrikes, from a winter low point, rapidly increased their residue levels in the breeding season one year following application. Mice at 100 days show only slight evidence of the long-term increase that becomes apparent in the residue level at one year. At the latter time, residue levels in mice exceeded those in the period of rapid uptake immediately following D D T application. Casual collections and analyses one and two years later add substance to our suggestion of long-term uptake and increase in residue levels following stabilisation at 2-4 months. A sample taken from a clutch of ring-necked pheasant eggs in the area one year after application had a mean DDT-R value of 3.76ppm. Graminivorous birds normally do not accumulate high residues and galliform birds particularly seem to be resistant to levels considered hazardous to birds that are

D D T IN A TERRESTRIAL FOOD WEB BO

225

____~_

DDT-R INCOCCN IE~LB LD IEETLES (CARNIVOROUS)

`10 E

g

i

s

I i

!

z

[

`1 soo

200

~""*

F

I

]

•i 1

O D T - R IN ARACHNIDS (CARNIVOROUS)

1oo

50

~.

Ii I

2o

J

1o

I BASELINE

'16

32

48 DAYS

64

80

96

Fig. 2. Concentrations of DDT-R (lipid weight basis) in carnivorous arthropods before and after spraying with DDT at 0-22 kg/ha adjacent to croplands near Davis, California. Values are from pooled samples representing entire biomass. Wavy arrow indicates normal outward migration of adults from the area.

omnivores or carnivores. Nevertheless, an entire clutch of starling eggs from the area, taken in the species of the year following application, had a mean DDT-R value of 113.4 ppm. Starlings are common omnivorous birds in the region. Most strikingly, analysis of skin and brain of two shrikes, taken more than two years after application, showed individual DDT-R values much higher than those in Fig. 3. These values were 820.93 and 293.43 ppm. Residues present were almost entirely DDE, indicating long-term accumulation and storage.

226

R. L. RUDD, R. B. CRAIG, W. S. WILLIAMS 240

so/l._

200

I

. . . .

DDT-R IN SHRIKES LIPID WEIGHT

,

460

E

~20

/

/

40

0 BASELINE

50

I00

't50

7'00 DAYS

250

300

350

Fig. 3. Concentrations of DDT-R (lipid weight basis) in a predatory passeriform bird, the loggerhead shrike Lanius ludovicianus before and after spraying with DDT at 0.22 kg/ha adjacent to croplands near Davis, California. Each dot represents mean residue levels in skin and brain tissue from four birds, except the last three, for a total of 27 birds. Values from two additional birds are given in the text.

DISCUSSION

Disruption of community organisation in areas of application of toxic chemicals is an immediate purpose in pest control. The desired purpose is continued suppression or permanent removal of a feeding guild. No one has been able to achieve this state by means of chemicals although it has been accomplished in restricted situations by physical means and by biological competition. Although control chemicals normally disrupt ecological communities for relatively short periods, longer term residual effects are largely beyond control and are neither anticipated nor well studied. The ultimate question has been repeatedly asked but remains unanswered. Do uncontrollable residues or their transferred ecological effects alter or reduce biological productivity in the long run ? Only in a few specific situations (e.g. egg-shell thinning) is it clear that they do. These are targets--unintended but targets nonetheless, just as a pest species is. They do not indicate a lessening of community productivity. This paper describes a food-web distribution of pesticide residues with individual chemical levels indicated within functional trophic compartments. Residue distributions are then formed into temporal patterns from static readings. A truly trophic or energy flow description must take into account the total biomass and community organisation through all seasons; we were unable to measure these aspects. No studies to date include all elements of community disruption resulting from pesticide stress on an ecosystem. Barrett (1968) and his students (Suttman & Barrett, 1979) describe reductions in biomass and differential reduction of arthropod taxa in

DDT

IN A TERRESTRIAL FOOD WEB

227

cereal grains treated with sevin. This carbamate insecticide degraded quickly (within 16 days) but its ecologically disruptive effects continued for three months in the arthropod community and for six months as measured by reproductive and demographic effects in small mammal populations. Ecokinesis of some heavy metals parallel patterns noted in the distribution of persistent insecticide residues in our study. Hughes et al. (1980), in a major review, summarise ecological distribution of heavy metals combinants in graphic compartments, much as we have previously presented (Craig & Rudd, 1974). However, Hughes et al. describe residue kinetics in linear food-chain sequences which cannot describe complex interactions in a terrestrial ecosystem. Sufficient data on the ecological distribution of some heavy metals, notably cadmium and mercury, exist to enable descriptions of contaminant relationships to food webs in aquatic ecosystems. Our own study indicates a short-term residue uptake and decline in model compartments that accords with predictions based on many published accounts. But we find no comparable published example of the longer term reversal of residue decline to levels often exceeding initial uptake in several taxonomically unrelated groups of organisms in a single ecological community. Long-term increase in residues accumulated in shrikes was detectable only in skin and brain, both depots of immobile fat. Whole body analysis does not show this pattern. The modes of physiological response to ingested residues must differ with time. We speculate that initial ingestion of residues by shrikes stimulates a DDT-ase enzyme which rapidly reduces tissue levels to tolerable thresholds. At these thresholds DDT-ase actions are removed. Continued ingestion of appropriate prey (Craig, 1978), contaminated at low levels, fails to stimulate DDT-ase production but does allow storage at organ sites with high lipid content, notably skin with subcutaneous fat and brain tissue. The same speculation would apply to fatty gonad tissue with the potential for reproductive inhibition (e.g. egg-shell thinning) when fat is mobilised during o6genesis. All feeding groups possessing the long-term pattern shown may be depositing residues in physiologically inactive fat depots, as shown in shrikes. However, only shrikes among groups showing the up-turn pattern can be expected to live as individuals for more than one year. Further study must be conducted to determine sites of residue concentration in affected arthropods and the ecological importance of those concentrations. The point must be made that only in a single instance (the total absence of shrews following application) was any disruption of community construction following low-level application of DDT apparent. The manifold increases in residue levels shown in the figures would seem to be ecologically hazardous only in shrikes but, since these are top predators in this agroecosystem, they would be rarely taken as prey themselves. The residue levels in shrikes, moreover, seem not to interfere with reproduction or with population density. Residue levels in the immobile fat of top

228

R . L . RUDD, R. B. CRAIG, W. S. WILLIAMS

predators, unaffected individually by the presence of these residues, may constitute a kind of ecological siphon or sump. This suggestion cannot, however, be viewed as a sanction for the continuing environmental presence of uncontrollable residues.

ACKNOWLEDGEMENTS

This research was supported under the 'San Joaquin Valley Project', Food Protection and Toxicology Center, University of California, Davis, USA, with funding from the National Science Foundation (NSF GB 33723-XI) and Oak Ridge National Laboratory, operated by Union Carbide Corporation for the US Department of Energy under Contract W-7405-eng-26. Publication No 1638, Environmental Science Division.

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