Content uploaded by Wiratno Wiratno
Author content
All content in this area was uploaded by Wiratno Wiratno on Aug 29, 2022
Content may be subject to copyright.
A Case Study on Bangka Island, Indonesia on the
Habits and Consequences of Pesticide Use in
Pepper Plantations
Wiratno,
1,2
Darmono Taniwiryono,
3
Paul J. Van den Brink,
4,5
Ivonne M. C. M. Rietjens,
2
Albertinka J. Murk
2
1
Indonesian Medicinal and Aromatic Crops Research Institute, Jl. Tentara Pelajar No 3,
Bogor 16114, Indonesia
2
Section of Toxicology, Wageningen University, P.O. Box 8000, 6700 EA Wageningen,
The Netherlands
3
Indonesian Biotechnology Research Institute for Estate Crops, Jl. Salak No. 1,
Bogor, Indonesia
4
Alterra, Wageningen University and Research Centre, P.O. Box 47, 6700 AA Wageningen,
The Netherlands
5
Department of Aquatic Ecology and Water Quality Management, Wageningen University,
P.O. Box 8080, 6700 DD Wageningen, The Netherlands
Received 2 December 2006; revised 6 March 2007; accepted 10 March 2007
ABSTRACT: Habits and consequences of pesticide use in pepper plantations were studied in Indonesia.
The first study was conducted by questioning 117 farmers about their habits in pesticide use and determin-
ing pesticide residues on pepper berries on Bangka Island. Meanwhile, the second study was completed
by analyzing exposure levels of pesticide in farmers’ bodies before and after pesticide application to pepper
plantations at Sukamulya, West Java. Risks of pesticide exposure to below ground terrestrial invertebrates
and aquatic ecosystems adjacent to the treated fields were evaluated using scenarios and a decision sup-
port system. Results showed that five respondents (4.3%) were agricultural workers without their own plan-
tations and the others were plantation owners. About 112 respondents (95.7%) used pesticides regularly,
while 21 respondents (17.9%) had experienced pesticide poisoning. About 54 respondents (46.2%) tended
to apply the same pesticide on all occasions, and 104 respondents (88.9%) indicated to always apply a sin-
gle compound. About 91 respondents (77.8%) were not aware of the possible impact of pesticides on their
health, and 102 respondents (87.2%) were not aware of the possible effects on the environment. In addition
while spraying pesticides 17 respondents (14.5%) were smoking, 81 respondents (69.2%) were wearing
daily clothes, and 84 respondents (71.8%) were throwing empty bottles into the forest. Exposure study
revealed that the residues in the urine and blood increased 6.5–10 and 1.1–1.5 folds, respectively indicating
actual and direct exposures. The environmental risk assessment indicated low risks for the terrestrial below
ground invertebrates but high potential risks for the aquatic ecosystem. The residues of the major pesti-
cides were below the maximum residue limits. This study indicated that the farmers and their workers, and
probably also the environment, were at risk of high exposure to the pesticides applied, but that the risks for
the consumers were negligible, if present at all. #2007 Wiley Periodicals, Inc. Environ Toxicol 22: 405–414, 2007.
Keywords: pesticide use; black pepper; developing country; Indonesia
Correspondence to: Wiratno; e-mail: wiratno02@yahoo.com
Published online in Wiley InterScience (www.interscience.wiley.com).
DOI 10.1002/tox.20277
C2007 Wiley Periodicals, Inc.
405
INTRODUCTION
Black pepper (Piper nigrum L.) known as the ‘‘King’’ of
spices is economically the most important and worldwide
the most widely used spice crop. This leading position
among spices results in increasing commercial value in the
world trade and it is predicted that the global demand for
pepper will increase from 230,000 metric tons in 2010 to
about 280,000 metric tons by the year 2020, possibly fur-
ther increasing to 360,000 metric tons by 2050 (Nair, 2004).
In Indonesia, pepper was originally introduced by Hindu
colonists between 100 BC and AD 600. The most important
growing areas for pepper are Lampung (producing Lamp-
ong black pepper), Bangka (producing Munthok white
pepper), and West Kalimantan (producing black and white
pepper). Nowadays, pepper economically is one of the most
important commodities in those areas also because, being a
labor intensive crop, it provides jobs for the local popula-
tion. In addition to being a source of national revenues,
pepper can be exploited as a source of raw materials for
some industrial products, such as food, medicines, and cos-
metics (Deciyanto et al., 1998).
Because nowadays farmers cultivate pepper intensively,
pesticides are applied in high dosages and frequencies,
especially to control the most important pests in the planta-
tions, which according to Kalshoven (1981) are tinged bug
(Dasynus piperis China.), stem borer (Lophobaris piperis
Marsh.), bug (Diconocoris hewetti Dist.) and root-knot
nematode, (Meloidogyne incognita Kofoid and White.).
Departemen Pertanian (2005) provides the synthetic pesti-
cides which until now are recommended by the Indonesian
government to fight those pests. Most of the pesticides used
are insecticides, namely pyrethroids (Pyr) or organophos-
phates (OP) or carbamates (Carb), and two herbicides i.e.,
paraquat and glyphosate.
This intensive use of synthetic pesticides could, how-
ever, have serious implications for the health of the farmers
and their families, consumers, live stock, and the environ-
ment. Jeyaratnam (1990) estimated there were 30,000 cases
of pesticide poisoning annually in Indonesia, of which
2400 required hospitalization. Currently both the Indone-
sian government and consumers increasingly demand
healthier and environmentally friendlier products. There-
fore a study was performed on the current farmers’ habits
and consequences of the use of synthetic pesticides in
pepper plantations, especially on Bangka Island.
The aim of this study was (i) to obtain information on
the consequences of the crop protecting practices using syn-
thetic pesticides for local people, on the awareness of peo-
ple working with pesticide about health and environmental
risks and actual poisoning cases, on residual levels of major
insecticides on pepper berries, on exposure of farmers to
pesticides during application, and (ii) to perform an esti-
mated environmental risk assessment of some recom-
mended pesticides. It is expected that this information can
be used by the local government to improve the quality of
life of the farmers and support the necessity to look for al-
ternative methods for crop protection.
MATERIALS AND METHODS
Selection of the Study Areas
and Respondents
The study was conducted from June until August 2004 on
Bangka Island, one of the central pepper productions in
Indonesia. General information related to the production
volume and area of all commodities was collected and com-
piled from data from districts and provincial offices.
Detailed information concerning farmers’ behavior in man-
aging their plantations was gathered through a field survey.
The selection of the locations to interview farmers was
based on purpose sampling to obtain convenience samples,
in which districts, subdistricts, and villages would not be
chosen if only a few black pepper plants were grown there.
Moreover, farmers only were chosen if they applied
pesticides by themselves. If they worked e.g., as tin miners,
fisherman, officers, or shopkeepers they were excluded as
respondents. Out of five districts of Bangka Island, four
districts (80%) were selected and in each of them 2–3 sub-
districts were selected (40.5%). From each subdistrict four
villages were selected (34.8%) and from each village 3–5
farmers were interviewed, depending on the number of
farmers that was available during the study. In total 117
respondents were questioned. The questionnaires focused
on the farmers’ understanding of the possible risks for man
and environment when using pesticides reflecting the way
they worked with those toxic compounds. Detailed ques-
tions of the questionnaires were related to major pesticides
used by farmers, dosages or concentrations of pesticides
being applied, time and method of pesticide application,
poisoning cases of workers, and behavior of local farmers
when using pesticides with respect to the use of protective
clothing while spraying, the moment of smoking cigarettes
related to spraying activities, and the way of disposal of
emptied pesticide containers.
Farmer Exposure Study
This study was conducted on August 18th, 2004 at the
Research Installation of the Indonesian Spice and Industrial
Crops Research Institute (RIISICRI), Sukamulya. During
the study, two officers who also often used to spray pesti-
cides to control pepper pests in the experimental garden of
this institute were requested as our volunteers to spray
chlorpyrifos onto 100 pepper plants according to common
practices of the interviewed farmers. Before commencing
the application, the volunteers were informed about the risk
and possible effects of the pesticide to their health in
406 WIRATNO ET AL.
Environmental Toxicology DOI 10.1002/tox
accordance with the ethical concerns and rules of the Indo-
nesian Medicinal and Aromatic Crops Research Institute
for involving people in working with toxic compounds.
Spraying was carried out in clear weather with 298C and
67% humidity. The first farmer who sprayed 3 mL/L con-
centration was wearing long sleeves and covered his head
with a t-shirt. The other farmer who sprayed 1 mL/L con-
centration was wearing a casual t-shirt and covered his
head with a cap. Application was completed using 15 L
Solo knapsack sprayers. Application began at 9 a.m. and
lasted for 2 h, with a short break for 15 min at 10 a.m.
About 50 mL of urine and 5 cc of blood were sampled
before (8.00 a.m.) and after application (2.30 p.m.) from
the volunteers at the Medika Laboratory, Cibadak, Suka-
bumi. To avoid blood coagulation 650 mg of ethylene dia-
mine tetra-acetic acid (EDTA) was added. To estimate the
pesticide residue on the farmers’ clothes, a piece of 20
20 cm tissue paper was attached on the chest of each vol-
unteer before spraying commenced. All samples were put
in glass bottles and cooled until they could be transferred to
a freezer at 48C in the laboratory. Two days later the resi-
due levels of major pesticides were analyzed using gas
chromatography as described above.
Extraction procedures of tissue papers, urine, and blood
samples for gas chromatography analysis were almost simi-
lar. However, the organic solvent for tissue paper was ace-
tone absolute, while that for urine and blood was a mixture
of n-hexane and dichloromethane (60:40). Details of the
extraction procedures were as follows; firstly, 50 mL urine
or a tissue paper was mixed with 100 mL organic solvent
and shaken using a mechanic shaker at 40 rpm for 20 min,
while 5 cc blood was dissolved in 10 mL solvent then was
mixed on a vortex for about 2 min. After that the solvent,
containing the extracted pesticide, was collected. The
remaining sample was then re-extracted twice using the
same solvent and procedure. The samples of the three
extraction steps were mixed and homogenized. After that
the solvent was evaporated using a rotary evaporator until
about 1 mL was left. The sample was then purified in a
chromatography column filled with 30 g florisil and sodium
sulfate anhydrate and wetted with 50 mL solvent. After that
the sample was re-evaporated using a rotary evaporator
until the volume of the solution was about 1 mL then the
solution was transferred into a trial tube. Lastly, the inner
part of the evaporating glass was washed step by step using
9 mL solvent to make sure that the pesticide residue was
completely dissolved, then the solution was poured into the
above trial tube. Of the 10 mL of the final product, 2 Lof
the solution was used for the GC analysis.
Chemical Analyses
The residue levels of the major insecticides used by the
farmers were determined on pepper berries obtained from
both the local market in Belinyu and two large exporters
in Pangkalpinang, the Capital City of Bangka Island. The
residues were analyzed in the Indonesian Centre for Agri-
cultural Biotechnology and Genetic Resources Research
and Development. The details of the gas chromatographic
conditions used were as follows.
A gas chromatograph (Shimadzu 4 CM) equipped with
Electron Capture Detector (ECD) and glass capillary col-
umn (2 m length, 3 mm diameter containing chromosorb
waw) was used. The injected volume was 2 L and nitro-
gen ultra high pure (N2UHP) gas was used as carrier at a
flow rate of 40 mL/min. The injector and detector tempera-
tures were 220 and 2308C, respectively. The sensitivity of
the GC was set manually to 10
2
MOand the pulse was
10(H) kHz. The detection limits for chlorpyrifos, -cyhalo-
thrin, and BPMC (2-s-butylphenyl methylcarbamate) were
0.0002, 0.0038, and 0.0012 g/g of samples, respectively.
Environmental Risk Assessment
The risks of the pesticide use to the environment were
assessed using hypothetical scenarios applying the risk
assessment model PRIMET (Pesticides Risks in the Tropics
to Man, Environment, and Trade) (Van den Brink et al.,
2005). To perform a risk assessment in PRIMET, a scenario
describing the physical properties of the environmental
compartment must be provided. This scenario was com-
bined with usage data and some pesticide properties to cal-
culate a Predicted Environmental Concentration (PEC).
This PEC was then compared to a No Effect Concentration
(NEC) to calculate the Exposure Toxicity Ratio (ETR). The
NEC was calculated from EC
50
values based on laboratory
toxicity tests performed with standard test species and
safety factors to account for between species variability and
the extrapolation from 50% effect to no effect. The proce-
dure to calculate the PEC and NEC was in accordance to
the EU regulations (European Union, 1997) and was
described in detail in (Van den Brink et al., 2005). An ETR
lower than 1 indicates that no serious effects could be
expected, one of between 1 and 100 that effects were uncer-
tain, while an ETR of higher than 100 indicated that effects
were likely to occur. The risks were evaluated for an adja-
cent aquatic ecosystem and in-crop below ground terrestrial
invertebrates.
The aquatic scenario assumed an aquatic waterway of
1 m wide at the bottom, a slope of 0.5 and 50 cm of water
depth. The length from which the ditch received spray drift
following the applications as provided in Table I was
100 m with a flow velocity of 100 m/day. The water phase
was assumed to contain 1 g/L of suspended solids with an
organic matter content of 50%, while the water temperature
was assumed to be 308C. It was assumed that 10% of the
amount applied on the soil surface would reach the water
surface by spray drift. All these values seem to be realistic
for a tropical scenario, see e.g., (Van den Bosch et al.,
2006).
407
HABITS AND CONSEQUENCES OF PESTICIDE USE IN PEPPER PLANTATIONS
Environmental Toxicology DOI 10.1002/tox
The soil scenario assumed a soil with a bulk density of
1100 kg/m
3
and the top 5 cm would contain the inverte-
brates at risk.
The toxicity values for the aquatic and terrestrial stand-
ard test organisms were obtained from the National Institute
of Public Health and the Environment, The Netherlands
(RIVM) database (De Zwart, 2002; Frampton et al., 2006),
respectively. For the application scenario the usage data as
provided in Table I were taken to calculate grams of active
ingredients applied per hectare.
The PRIMET DSS (Decision Support System) is freely
available on www.primet.wur.nl and incorporated in a
Graphical User Interface.
RESULTS
Results of the secondary data collections from provincial
and district offices showed that pepper was the most com-
mon plant grown by farmers on Bangka Island, followed by
rubber, coconut, oil palm, cacao, and clove, respectively
(Table II). Although pepper was cultivated intensively in
most districts of the study areas except in Pangkalpinang,
wide areas of pepper plantations within the sub districts and
villages were still diverse (Dinas Perkebunan Propinsi
Bangka Belitung, 2004). Therefore, sub districts and vil-
lages would be selected only if they had the widest areas of
pepper plantation.
The baseline study revealed that 23 respondents (19.7%)
cultivated less than 500 plants, while 56 respondents
(47.9%) had 500 to 1000 plants and 38 respondents
(32.5%) even grew more than 1000 black pepper plants.
The study also revealed that 112 respondents (95.7%) regu-
larly applied synthetic pesticides to control main insect
pests of black pepper, i.e., the stem borer (L. piperis), the
tinged bug (D. piperis), and the bug (D. hewetti), and in
addition to control weeds. Although carbofuran had been
recommended by the ministry of agriculture to control the
root-knot nematode, M. incognita (Departemen Pertanian,
2005), only few respondents used this pesticide because
based on their experiences there were no pesticides effec-
tive enough to control this pest.
TABLE I. Synthetic pesticides recommended by the government of Indonesia to fight the most important pests in
black pepper plantations (Departemen Pertanian, 2005), including their active ingredients, purity and dosage
Pesticides Active Ingredients Groups
Dosages/
Concentration
a
Vol. of
Application (l/ha)
Max Dose
Applied (g/ha)
Insecticides
Ambush 2 EC Permethrin 20 g/L Pyr 0.5–l.0 L/ha nd 10
Arrivo 30 EC Cypermethrin 30.36 g/L Pyr 0.5–1.0 mL/L 1200–1500 46
Bassa 500 EC BPMC 500 % Carb na na na
Buldok 25 EC Beta-cyfluthrin 25 g/L Pyr 0.5–1.0 L/ha nd 25
Decis 2.5 EC Deltamethrin 25 g/L Pyr 0.1–0.2 mL/L nd na
Dharmacin 50 WP MIPC 50% Carb na na na
Dharmasan 600 EC Fenthoate 600 g/L OP na na na
Dursban 20 EC Chlorpyrifos 200 g/L OP 1.0–2.0 mL/L 1000 400
Elsan 60 EC Fenthoate 60 g/L Carb 2.0 mL/L 500–800 96
Lebaycid 500 EC Fenthion 500 g/L OP 2.0 mL/L nd na
Matador 25 EC Lambda-Cyhalothrin 25 g/L Pyr 0.5–1.0 L/ha nd 25
Marshal 200 EC Carbosulfan 200 g/L Carb 1.5–3.0 mL/L 1200–1500 900
Mipcin 50 WP Isoprocarb 50% Carb 1.0–2.0 kg/ha nd 1000
Meothrin 50 EC Fenpropathrine 50 g/L Pyr 0.5–1.0 mL/L nd na
Orthene 75 SP Acephate 75% OP na na na
Padan 50 SP Cartap hydrochloride 50% Carb 2.0 kg/ha 600– 800 1000
Pounce 20 EC Permethrin 20.04 g/L Pyr 1.0–2.0 mL/L nd na
Sevin 85 AS Carbaryl 85% Carb 2.5 kg/ha 500–1000 2125
Sumithion 50 EC Fenitrothion 500 g/L OP na na na
Sumicidin 5 EC Fenvalerate 44.5 g/L Pyr na na na
Nematicide na
Furadan 3G Carbofuran 3% Carb 30.0 gr/plant nd na
Herbicides na
Gramoxone Paraquat dichloride 276 g/L Bipiridillium 2.0–3.0 L/ha nd 828
Sunup 480 AS Glyphosate 480 g/L Gly na na na
The pesticides used are insecticides, namely pyrethroids (Pyr) or organophosphates (OP) or carbamates (Carb), nematicide, namely carbofuran and
herbicides, namely paraquat dichloride (bipiridillium) and glyphosate.
a
Recommended dosages or concentrations found on the packages. na, Pesticide is not available on local markets; nd, data are not available on
the packages.
408 WIRATNO ET AL.
Environmental Toxicology DOI 10.1002/tox
The amount of pesticides used by the respondents
depended on the price of the pepper berries and the popula-
tion density of pests or weeds. Generally, most respondents
(98.3%) used the cap of pesticides’ containers (8 mL) to
measure the amount of pesticide to be used. Most of the
respondents (91.5%) used two or three caps of pesticide per
15 L of water, which was equivalent to 1.1 or 1.6 mL/L,
while the rest used four caps (equivalent to 2.1 mL/L). The
recommended concentrations of pesticides varied between
0.1 and 3 mL/L. In very extreme conditions in which price
of the berries or density of the pest population was quite
high, respondents would use four or even five caps pesti-
cide, which was equivalent to 2–2.5 mL/L. Based on this
information, some pesticides were applied in higher con-
centrations than that of the recommended concentrations,
especially those belonging to pyrethroid group, i.e., cyper-
methrin, -cyfluthrin, deltamethrin, -cyhalothrin, and fen-
propathrine (Table II). The richer farmers tended to use
more pesticides than the underprivileged farmers who only
could apply 1–2 caps per 15 L of water equivalent to 0.5–
1.1 mL/L.
The most popular pesticides were fenthion, -cyhalo-
thrin, and BPMC (2-s-butylphenyl methylcarbamate), while
only two respondents still used tuba root (Derris elliptica
Benth.) (Fig. 1). About 40 respondents (45.8%) tended to
apply the same insecticide all the time, while 104 respond-
ents (89%) preferred to apply single compounds. The rest
would mix pesticide with fertilizers or other compounds
such as fungicides or cajuput oil, the oil which was
extracted from Melaleuca leucadendron L. was believed
able to repel pests in plantations.
Of the respondents, 92.3% (108 respondents) preferred
to only spray pesticides directly onto their plants while the
rest immersed the pesticide into the rooting areas especially
to control the plant parasitic nematode M. incognita. Appli-
cation would start around 7.00 a.m. and continue until
12.00 a.m. and would be continued from 1.00 p.m. until
5.00 p.m. However, the period of application of pesticides
differed among the respondents. About 69 respondents
(58.9%) sprayed both in the morning and in the afternoon,
while 46 respondents (39.3%) only sprayed in the morning
and two respondents (1.7%) only sprayed in the afternoon.
There were 113 respondents (96.6%) who immediately
took a bath and washed their sprayer tanks and clothes in
the river after application of the pesticides. However nine
respondents (7.7%) just hung up their clothes and would
use them again the following day. They would wash those
Fig. 1. Percentage of farmers using the pesticides speci-
fied in black pepper plantation on Bangka Island based on
interviews with 117 respondents.
TABLE II. Overview per crop of the surface area and production of smallholder plantations in 4 districts of
Bangka Island (Dinas Perkebunan Propinsi Bangka Belitung, 2004)
Commodities
Districts
TotalMain Bangka Central Bangka South Bangka West Bangka
Wide
Area (ha)
Prod.
(tons)
Wide
Area (ha)
Prod.
(tons)
Wide
Area (ha)
Prod.
(tons)
Wide
Area (ha)
Prod.
(tons)
Wide
Area (ha)
Prod.
(tons)
Pepper 13,725.00 5,388.58 5,940.08 1,907.36 1,8621.58 12,830.63 10,229.90 3,440.03 48,516.56 23,566.60
Rubber 18,314.35 7,327.50 2,733.00 1,001.00 4,448.40 1,910.35 13,157.00 4,017.00 38,625.75 14,255.85
Coconut 5,956.50 3,064.40 2,497.30 1,234.29 1177.53 468.82 2,416.15 975.30 12,047.48 102.81
Oil palm 815.00 237.65 152.00 79.16 24.00 15.00 407.00 237.00 1,398.00 568.81
Cacao 140.00 43.20 51.00 – 730.00 43.20 25.50 0.10 289.50 86.50
Clove 71.00 0.64 49.00 4.18 33.25 0.78 102.50 0.85 256.21 6.45
Sugar palm 77.00 24.15 53.00 17.31 38.50 0.83 39.00 14.25 207.50 66.54
Cashew 63.00 22.16 20.00 8.80 100.00 7.24 13.40 1.89 196.40 40.09
Betel palm 27.27 1.21 75.82 3.83 37.30 1.27 26.31 8.64 166.70 14.95
Candle nut 10.50 – 46.00 7.03 9.00 6.01 6.00 – 71.50 13.04
Coffee – 4.02 32.00 0.20 18.00 – 9.00 3.66 59.00 7.88
Gambier 32.25 – – – – – 7.00 – 39.25 0.00
Patchouli 15.00 0.93 – – 11.00 – 4.00 1.25 30.00 2.18
Ginger – – – – – – – 0.15 0.00 0.15
Tee – – – – – – 1.00 – 1.00 0.00
– Data are not available.
409HABITS AND CONSEQUENCES OF PESTICIDE USE IN PEPPER PLANTATIONS
Environmental Toxicology DOI 10.1002/tox
clothes after the second application or occasionally after
finishing spraying all their plants.
Unfortunately, 90 respondents (76.9%) did not really re-
alize the possible impact of pesticides on their health. As a
result about 21 respondents (17.9%) felt pesticide poisoning
though they did not visit physicians for further clinical
investigation. Because of the generally limited awareness
of possible health risks during application of pesticides, 81
respondents (69.2%) just wore their ordinary clothes with-
out considering any protection against contamination with
pesticides [Fig. 2(a)]. Only one respondent (0.9%) fully
protected himself. During spraying pesticides about 18
respondents (15.4%) even smoked a cigarette, and 77
respondents (65.8) smoked during the break before washing
or changing clothes [Fig. 2(b)]. Most of the respondents
would take a bath before having lunch. This habit, however,
was due to the hot weather causing strong sweating and not
because of awareness of the risk of using pesticides.
The awareness of the importance of safe disposal of the
empty pesticide containers seems to be very limited as 82
respondents (70.1%) just threw empty pesticide containers
away into the forest and one respondent (0.8%) even used
them for other purposes such as to make lamps [Fig. 2(c)].
In addition, of the respondents, 102 respondents (87.2%)
did not really realize the existence of natural enemies and
their important role in controlling pests in their plantations.
The two volunteers in the exposure study sprayed the
pesticide in the common way of the interviewed farmers.
They walked around the plant trying to spray the canopy of
pepper plants evenly. They used one hand to pump the tank
while the other hand was used to spray the pesticide. While
spraying the highest part of the plant, they looked up to the
end of the canopy to make sure that this part was really
sprayed (Fig. 3). The average spraying period per plant was
16.5 62.5 s.
After completing the application the two volunteers did
not experience any symptoms of pesticide poisoning. How-
ever, chemical analysis of the urine, blood, and tissue
papers indicated strong exposures upon application of the
pesticide. Results of the exposure study also revealed that
higher concentration used by the volunteer resulted in
higher residue levels of the pesticide on the analyzed
samples. The residues of pesticide in urine and blood of the
volunteer applying 1 mL increased 6.5 and 1.1 times,
respectively while those of that 3 mL increased 10.3 and
1.5 times, respectively (Table III).
Fig. 2. Percentage of local farmers on Bangka Island, Indo-
nesia displaying specific behavior when using pesticides in
black pepper plantations with respect to (a) the use of pro-
tective clothing while spraying, (b) the moment of smoking
cigarettes related to spraying activities and (c) the way of
disposal of empty pesticide containers.
Fig. 3. Common way of spraying pesticides in on black
pepper plants by farmers on Bangka Island, Indonesia.
[Color figure can be viewed in the online issue, which is
available at www.interscience.wiley.com.]
410 WIRATNO ET AL.
Environmental Toxicology DOI 10.1002/tox
The difference in chlorpyrifos level between the tissue
papers on the farmers spraying 1 and 3 mL/L was only
small, i.e., 1.08 times. It gave the impression that the slight
different levels of protective clothing worn by the volun-
teers might not influence the actual exposure to pesticide
since the volunteers might be exposed mainly through inha-
lation. The presprayed residues detected in their bodies
probably resulted from earlier regular exposures since they
used to spray pesticides to control pests in botanical gar-
dens of the RIISICRI, where this farmer exposure study
was also conducted.
Gas chromatographic analysis on the pepper berries
obtained from a local market and two exporters showed
that the residual levels were below the standard maximum
residue limit (MRL) on food as generally defined (Pesticide
Residue Committee, 2006); (The Japan Food Chemical
Research Foundation, 2007). In all cases and often the resi-
dues bellowed the limit of detection (Table IV).
Table V provides the results of the Environmental Risk
Assessment in terms of ETRs for the aquatic and terrestrial
compartments. Although realistic worst case assumptions
were chosen, large potential risks were calculated for the
aquatic ecosystem, while risks were absent for the terres-
trial below ground invertebrates. For the aquatic environ-
ment the highest potential risks were indicated for the
insecticides cartap hydrochloride, chlorpyrifos, and carba-
ryl, while lower ones were calculated for the insecticides
carbosulfan and -cyhalothrin and the herbicide paraquat
dichloride.
DISCUSSION
This study reveals that problems on the usage of pesti-
cides in pepper plantations on Bangka Island seem to
arise predominantly from unwise use of pesticides rather
than from the toxic nature of the pesticides itself. This
includes too high concentrations being applied, using sin-
gle brand of synthetic pesticide continuously, poor appli-
cation technology, and rarely using standard protective
equipments.
The study indicated that farmers were severely exposed
to pesticides since 21 respondents (17.9%) had experienced
acute pesticide poisoning with the common symptoms
TABLE IV. Residues of three synthetic insecticides frequently used by Indonesian
farmers on pepper berries
Source of
samples
Lambda-cyhalothrin
(g/g)
Fenthion
(g/g)
BPMC
(2-sec-butylphenyl
methylcarbamate) (g/g)
MRL* Residue MRL* Residue MRL* Residue
Exporter 1 0.02 0.0192 0.02 0.0043 0.3 0.0110
Exporter 2 <dl 0.0046 <dl
Local market <dl 0.0041 <dl
<dl ¼below limit of detection.
The berries were sampled from a local market at Belinyu and two big local exporters at Pangkalpinang.
MRL stands for Maximum Residue Limit as defined by the Pesticide Residue Committee (2006) and Staats-
courant (2002).
*Based on category seeds – others.
TABLE III. Chlorpyrifos residue levels in urine, blood and tissue paper attached to
the clothes of volunteers before and after spraying 100 pepper plants with
chlorpyrifos according to common practices
Volunteers
Concentration of
Chlorpyrifos Sample
Insecticide Residue (g/g)
Before
Application
After
Application
Volunteer A 1 mL/L Urine 0.0002 0.0013
Blood 0.0015 0.0016
Paper nd 0.2044
Volunteer B 3 mL/L Urine 0.0003 0.0031
Blood 0.0015 0.0023
Paper nd 0.2219
nd, not determined.
411HABITS AND CONSEQUENCES OF PESTICIDE USE IN PEPPER PLANTATIONS
Environmental Toxicology DOI 10.1002/tox
headache, fatigue, dizziness, or diarrhea. This condition
may happen since during spraying pesticides, farmers are
rarely wearing standard protective equipments as they are
extremely inconvenient and uncomfortable to use, espe-
cially under high temperature field conditions. According
to Rainbird and O’Neill (1995), these senses are exacer-
bated by the higher human energy expenditure associated
with carrying and operating a knapsack sprayer which
heated their bodies causing sweating during pesticide appli-
cation. Moreover, the equipments are sometimes not com-
pletely available on the market, costly, poorly maintained,
as well as not designed for tropical climates. Therefore, the
workers themselves probably are at the greatest risk of pes-
ticide poisoning because of their close contact with concen-
trated forms of the toxic substances.
Wilson and Tisdell (2001) pointed out that too high ex-
posure to pesticides was common in developing countries
with each year tens of thousands of farmers being affected
by exposure to pesticides. Little et al. (2003) performed a
farmer survey in Thailand indicating significant health
problems related to pesticide use which were perceived by
farmers. Headaches, dizziness, and vomiting are also the
most common symptoms thought to be linked to pesticide
exposure. Konradsen et al. (2003) estimated that 3 million
cases of pesticide poisoning occur worldwide annually with
220,000 deaths.
The volunteers in this study only sprayed 100 plants at
3 mL/L, but still the residue levels of chlorpyrifos increased
up to 10 times in urine (0.0003–0.0031 g/g) and 1.5 times
in blood (0.0015–0.0023 g/g). In the real situation the
exposure to pesticides would be higher than that of in these
volunteers, since 32% of the farmers had more than 1000
plants. The highest exposure is to be expected for the
workers, i.e., 5 respondents (4%) without own plantation,
who are applying pesticides intensively. Exposure may be
via inhalation of spray drift, from dermal exposure, either
directly (during spraying or preparation of the formulation)
or via wetted clothes and/or from ingestion during smoking
or eating before washing (Murphy et al., 1999). This can
result in acute or chronic illnesses (Kishi et al., 1995) such
as dermatitis (Koh and Jeyaratnam, 1996), as well as in
physical and mental problems including anxiety, irritability,
loss of memory and depression, which can lead to suicide
(Harris, 2000). Interviewing of the volunteers revealed no
symptoms experienced after pesticide application indicat-
ing that the exposure levels would be still relatively low.
Studies of the World Health Organization (1978) demon-
strated that 28 single daily doses of chlorpyrifos adminis-
tered at 0.3 g/g/day produced no measurable cholinester-
ase changes or adverse clinical symptoms.
Chemical analysis on the berries demonstrated that con-
sumers were not at risk from pesticide residues since the
levels of the analyzed synthetic pesticides on the berries
were below Maximum Residue Limit (MRL) values for
food in general as defined by (Staatscourant, 2002; Pesti-
cide Residue Committee, 2006). Moreover, since this spice
is used in relatively small quantities a relevant exposure via
this product is not likely to occur especially compared to
the risk of pesticide residues on daily food items that are
consumed in larger quantities. Carcinogenic or reprotoxic
effects are likely not occur as residue levels of the major
pesticides tested were below the MRL values.
The sampling procedures of the study were based on
data collected from provincial and district offices. Mean-
while, respondents were directly chosen in their fields
located in the forests without considering economic status,
age or size of pepper plantation. This limitation however
could bias the finding since these factors might influence
attitude of farmers in using pesticides. However, since the
island was isolated, the education level of the workers was
low (graduated only from elementary to high schools), and
pest control strategies were inherited from their parents, the
bias would not be so high.
In this study, applying at theoretical model for calculat-
ing environmental impact of pesticide use, it could be dem-
onstrated that pesticide use poses serious potential risks to
the aquatic environment, if aquatic ecosystems are present
adjacent to the treated fields (Table V). Satapornvanit et al.
(2004) reach the same conclusion for the use of pesticides
in Thailand, while Van den Bosch et al. (2006) provide
similar results for China and Vietnam. This indicates that
the environmental side-effects of pesticide use receive too
little attention in South-East Asia. This contamination of
the aquatic ecosystem might not only harm the ecological
integrity of the water, but also the livelihoods of local peo-
ple in terms of reduced (drinking) water quality, reduced
productivity (e.g., fish kills, effects on cattle that uses sur-
face water as drinking water). Poor people are expected to
TABLE V. Exposure toxicity ratios (ETRs) as calculated
by the PRIMET model for the aquatic ecosystem and
terrestrial below ground invertebrates
Active Ingredient
Application
(g/ha) ETR soil ETR water
Permethrin 10 nd 260
a
Cypermethrin 46 0.0084 360
a
Beta-cyfluthrin 25 0.0300 170
a
Fenthoate 96 nd nd
Lambda-cyhalothrin 25 0.0580 3
Chlorpyrifos 400 0.0068 1900
a
Carbosulfan 900 nd 20
Isoprocarb 1000 nd nd
Cartap hydrochloride 1000 nd 2400
a
Carbaryl 2125 0.4500 900
a
Paraquat dichloride 828 0.0340 0.015
ETR values below 1 indicate absence of risks, between 1 and 100 small
potential risks and above 100 large risks.
nd indicates that the ETR was not determined because toxicity data
were not available.
a
Represents a large risk.
412 WIRATNO ET AL.
Environmental Toxicology DOI 10.1002/tox
be disproportionately affected by any deterioration in the
environment (Maxwell, 1999), and it is therefore important
for ensuring the future availability of clean water in Asia to
predict the effects of intensified agriculture on the biodiver-
sity and quality of freshwater. It is, however, essential for a
true estimation of risks that the results from this prelimi-
nary ecological risk assessment will be validated using
chemical measurements, bioassays and bio-monitoring (the
TRIAD approach (Chapman, 2000)).
Although the organophosphates and the carbamates have
a high environmental degradability and water solubility
which both strongly reduce the risk of bioaccumulation,
these chemicals still pose a threat to the local environment
(Table V). Direct spraying exposure could kill wildlife and
natural enemies of pest species living around the treated
plants. In addition using the same pesticides all the time
would stimulate the development of resistance of the pests.
Both factors might result in an outbreak of secondary pests
(Sagar, 1991). The study of Kranthi et al. (2002) provided
evidence of the development of resistance of some cotton’s
insect pests in India i.e., Helicoverpa armigera Hubner.,
Pectinophora gossypiella Saunders., Spodoptera litura
Fab., and Earias vitella Fab., to cypermethrin, chlorpyrifos,
and endosulfan while Bemisia tabaci Genn. became resist-
ant to cypermethrin after improper application of pesticides
over the past two decades. Washing tanks in the river and
throwing empty pesticide containers away in the forests are
other causes for possible health risk for people, aquatic
organisms, and other living creatures in the area.
In general, this study indicates that local workers make
unwise use of pesticides. To avoid further exposure of the
farmers and the environment, they should be trained in why
and how to use pesticides safely under tropical conditions
(Ecobichon, 2001). In addition, the current promotion of
the Integrated Pest Management (IPM) including reduction
of the application of synthetic pesticides to occasions when
such pesticide use is necessary (Pedigo et al., 1986). IPM
has successfully been applied to control the rice brown
planthopper, Nilaparvata lugens Stal. in Indonesia (Tjitro-
semito, 1993). After applying the IPM strategy this country
would save more than $100 million/year by phasing out
85% pesticide subsidy between 1986 and 1989 while rice
yields increased although average pesticide applications/
season fall from over 4 to about 2.5 times (Matesson, 2000).
IPM also promotes the use of botanical pesticide to
replace the synthetic ones. Regnault-Roger (2005) ex-
plained that the use of botanical pesticides is a strategy par-
ticularly helpful in reducing current environmental and
health concerns because botanical pesticides are generally
less persistent and therefore can be applied selectively after
which they disappear. Therefore the use of botanical pesti-
cides protects diversity and prevents the build-up of toxic
residues in food chains and ecosystems. Unfortunately,
practical information related to the use of plants to effec-
tively control pests of pepper plantation has not been avail-
able to these farmers so far. Philoge
`ne et al. (2005) point
out that the development of the pesticide needs further
studies aiming at better characterizations of their toxic
potencies, improved standardization of the quality of raw
materials, and better definition of their formulation before
their use can be implemented in industrialized and develop-
ing countries.
The authors are grateful to the head of Bangka Belitung
Assessment Institute for Agricultural Technology and that of
Sukamulya Research Installation of the Indonesian Research Insti-
tute for Spice and Medicinal Crops for providing many facilities
throughout this study. We acknowledge the help of Dr. Asep
Nugraha, Ir. Eman Sulaeman, and Mr. Aji Mohammad Tohir of
the Indonesian Centre for Agricultural Biotechnology and Genetic
Resources Research and Development with the residue analyses.
We are indebted to The Integrated Pest Management for Small-
holder and Estate Crop Project (IPMSECP) for providing a fellow-
ship to Wiratno.
REFERENCES
Chapman PM. 2000. The Sediment Quality Triad: Then, now and
tomorrow. Int J Environ Pollut 13:351–356.
De Zwart D. 2002. Observed regularities in species sensitivity
distributions for aquatic species. In: Posthuma L, Suter G, Traas
T, editors. Species Sensitivity Distributions in Ecotoxicology.
Boca Raton, FL: Lewis. pp 133–154.
Deciyanto S, Wahid P, Manohara D, Dhalimi A. 1998. July-
December 1998. Adoption of a good agricultural practice to
prevent contamination on an Indonesia experience. Int News
22:39–42.
Departemen Pertanian. 2005. Pesticides for Agriculture and Estate
Crops. Jakarta: Koperasi Ditjen Bina Sarana Pertanian. p 490
(in Indonesian).
Dinas Perkebunan Propinsi Bangka Belitung. 2004. The develop-
ment of pests, diseases and weeds. Annual Report of the prov-
ince of Bangka-Belitung (in Indonesian).
Ecobichon DJ. 2001. Pesticide use in developing countries. Toxi-
cology 160:27.
European Union. 1997. Commission proposal for a council direc-
tive establishing Annex VI to Directive 91/414/EEC concerning
the placing of plant protection products on the market. Official J
Eur Union C 240:1–23.
Frampton GK, Ja
¨nsch S, Scott-Fordsmand JJ, Ro
¨mbke J, Van
den Brink PJ. 2006. Effects of pesticides on soil inverte-
brates in laboratory studies: A review and analysis using
species sensitivity distributions. Environ Toxicol Chem 25:
2480–2489.
Harris J. 2000. Chemical Markets, Health Risks and Residues.
Biopesticides Series 1. New York: CABI. 54 p.
Jeyaratnam J. 1990. Acute pesticide poisoning; a major global
health problem. World Health Stat Q 43:139–144.
Kalshoven LGE. 1981. Pest of Crops in Indonesia. Jakarta: Pt.
Ichtiar Baru Van-Hoeve. 701 p.
413HABITS AND CONSEQUENCES OF PESTICIDE USE IN PEPPER PLANTATIONS
Environmental Toxicology DOI 10.1002/tox
Kishi M, Hirschhorn N, Djajadisastra M, Satterlee LN, Strowman
S, Dilts R. 1995. Relationship of pesticide spraying to signs and
symptoms in Indonesian farmers. Scan J Work Environ Health
21:124–133.
Koh D, Jeyaratnam J. 1996. Pesticides hazards in developing
countries. The science of the total environment 188 (Suppl 1):
S78–S85.
Konradsen F, van der Hoek W, Cole DC, Hutchinson G, Daisley
H, Singh S, Eddleston M. 2003. Reducing acute poisoning in
developing countries—options for restricting the availability of
pesticides. Toxicology 192:249–261.
Kranthi KR, Jadhav DR, Kranthi S, Wanjari RR, Ali SS, Russell
DA. 2002. Insecticide resistance in five major insect pests of
cotton in India. Crop Protect 21:449.
Little DC, Yakupitiyage A, Satapornvanit K, Kaewpaitoon K,
Ungsethaphand T, Milwain GK, Baird DJ, Van den Brink PJ,
Taylor GT, Nogueira AJA. 2003. Managing Agrochemicals in
Multi-use Aquatic Systems (MAMAS). State-of-the-system
report. Thailand: Asian Institute of Technology and Kasetsart
University, Bangkok.
Matesson PC. 2000. Insect pest management in tropical Asian irri-
gated rice. Ann Rev Entomol 45:549–574.
Maxwell S. 1999. The meaning and measurement of Poverty.
ODI. Poverty briefing, 3 edn. London, UK. Available at http://
www.odi.org.uk/publications/briefing/pov3.html. Accessed Jan-
uary 28, 2007.
Murphy H, Sanusi A, Dilts R, Djajadisastra M, Hirschhorn N,
Yuliatiningsih S. 1999. Health effects of pesticide use among
Indoncsian women farmers: Part I: Exposure and acute health
effects. J Agromedicine 6:61–85.
Nair KPP. 2004. The Agronomy and Economy of Black Pepper
(Piper nigrum L.) the ‘‘King of Spices’’. New York: Academic
Press.
Pedigo LP, Hutchins SH, Higley LB. 1986. Economic injury lev-
els in theory and practice. Ann Rev Entomol 31:341–368.
Pesticide Residue Committee. 2006. Maximum residue levels
(MRL). Available at http://www.pesticides.gov.uk/prc.asp?id¼
956#Where_can_I_obtain_more_information_on_MRLs.
Accessed April 5, 2007.
Philoge
`ne BJR, Regnault-Roger C, Vincent C. 2005. Botanicals:
Yesterday’s and today’s promises. In: Regnault-Roger C, Phil-
oge
`ne BJR, Vincent C, editors. Biopesticides of Plant Origin.
USA: Lavoisier Publishing Inc. pp 1–15.
Rainbird G, O’Neill D. 1995. Occupational disorders affecting ag-
ricultural workers in tropical developing countries: Results of a
literature review. Appl Ergon 26:187–193.
Regnault-Roger C. 2005. New insecticides of plant origin for the
third millenium? In: Regnault-Roger BJR, Philogene C, Vincent
C, editors. Biopesticides of Plant Origin. Secaucus, NJ:
Lavoisier. pp 17–35.
Sagar AD. 1991. Pest control strategies: concerns, issues and
options. Environ Impact Assess Rev 11:257–279.
Satapornvanit K, Baird DJ, Little DC, Milwain GK, Van den Brink
PJ, Beltman WHJ, Nogueira AJA, Daam MA, Domingues I,
Kodithuwakku SS, Perera MWP, Yakupitiyage A, Sureshku-
mar SN, Taylor GJ. 2004. Risks of pesticide use in aquatic
ecosystems adjacent to mixed vegetable and monocrop fruit
growing areas in Thailand. Australas J Ecotoxicol 10:85–95.
The Japan Food Chemical Research Foundation. 2007. Table of
MRLs for Agricultural Chemicals. Available at http://www.m5.
ws001.squarestart.ne.jp/foundation/agrdtl.php? a_ing=58000.
Accessed April 5, 2007.
Tjitrosemito S. 1993. Integrated management of paddy and aquatic
weed in Indonesia. Bogor: BIOTROP. p 19. Available at http://
www.agnet.org/library/eb/367b/. Accessed November 29, 2006.
Van den Bosch H, Chaowen L, Pham Van Hoi, Ter Horst MMS,
Van den Brink PJ, Yunliang P, Groenwold JG, Yibing C, Van
Dung N, Van Wijk MS, Vlaming J. 2006. Environmental risks
of pesticide use in intensive vegetable farming systems in peri-
urban Hanoi (Dong Anh) and Chengdu (Pengzhou). Wagenin-
gen, The Netherlands: Alterra report 1285, 166 p.
Van den Brink PJ, Ter Horst MMS, Beltman WHJ, Vlaming J,
Van den Bosch H. 2005. PRIMET version 1.0, manual and
technical description. A decision support system for assessing
pesticide risks in the tropics to man, environment and trade.
Wageningen, The Netherlands: Alterra report 1185, 60 p.
Wilson C, Tisdell C. 2001. Why farmers continue to use pesticides
despite environmental, health and sustainability costs. Ecol
Econ 39:449.
World Health Organization. 1978. Data sheets on pesticides
No. 33: chlorpyrifos-methyl. Available at http:www.inchem.
org/documents/pds/pds/pest33_e.htm. Accessed August 31, 2006.
414 WIRATNO ET AL.
Environmental Toxicology DOI 10.1002/tox
