Agrochemical use on banana plantations in Latin America: Perspectives on ecological risk

Authors

  • William Henriques,

    1. The Institute of Wildlife and Environmental Toxicology (TIWET) and Department of Environmental Toxicology, P.O. Box 709, TIWET Drive, Pendleton, South Carolina 29670, USA
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  • Russel D. Jeffers,

    1. The Institute of Wildlife and Environmental Toxicology (TIWET) and Department of Environmental Toxicology, P.O. Box 709, TIWET Drive, Pendleton, South Carolina 29670, USA
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  • Thomas E. Lacher Jr.,

    Corresponding author
    1. The Institute of Wildlife and Environmental Toxicology (TIWET) and Department of Environmental Toxicology, P.O. Box 709, TIWET Drive, Pendleton, South Carolina 29670, USA
    Current affiliation:
    1. Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX 77843–2258, USA
    • The Institute of Wildlife and Environmental Toxicology (TIWET) and Department of Environmental Toxicology, P.O. Box 709, TIWET Drive, Pendleton, South Carolina 29670, USA
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  • Ronald J. Kendall

    1. The Institute of Wildlife and Environmental Toxicology (TIWET) and Department of Environmental Toxicology, P.O. Box 709, TIWET Drive, Pendleton, South Carolina 29670, USA
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Abstract

Developing tropical nations have greatly expanded their agricultural production during the past decade. Substantial areas of tropical ecosystems have been altered to accommodate agriculture. Banana cultivation is responsible for much of this habitat alteration. Substantial use of agricultural chemicals is required to successfully cultivate bananas, and this has raised concern over the effects of these chemicals on workers, wildlife, and tropical environments in general. We review the practice of banana cultivation and address the major chemical inputs to plantations. Numerous cases of pesticide-related health problems in Latin American plantation workers have been documented, and most were attributable to incorrect use and handling. A review of known wildlife-related impacts of agricultural chemicals commonly used in banana plantations raises substantial concerns about the large-scale environmental impacts in tropical terrestrial and aquatic environments. We recommend the application of an environmental risk assessment process to the use of agricultural chemicals on banana plantations. The process should follow the paradigm as outlined by the U.S. Environmental Protection Agency. Such a study would create a precedent for the assessment of environmental risk in the tropics.

INTRODUCTION

Large-scale agricultural plantations occupy between 100 and 135 million ha of the Earth [1]. Approximately 31% of this area is located in tropical and subtropical regions that lie between 27°N and 27°S latitude [2]. Much of this area is occupied by banana plantations because of the conditions necessary for proper banana cultivation and the high demand for bananas throughout the world. On the global scale, banana production ranks behind only citrus and grapes, with more than 41 million tons of bananas produced in 1984; however, banana cultivation has steadily increased in the world since then [3]. In Costa Rica alone, there are currently more than 50,000 ha in cultivation (C. Wille, personal communication). Bananas are Costa Rica's top source of foreign exchange, with more than $441 million in export earnings and 32,000 employees in 1991 [4]. Costa Rica is the leading exporter of bananas in Central America and is second only to Ecuador in total banana exportation in the world [5]. With banana production rapidly increasing in Latin America, assessment of the hazards to humans and wildlife from banana cultivation is needed.

The use of pesticides to control agriculture pests is a common practice on most tropical plantations. Because frequent heavy rains wash pesticides from target areas and because banana cultivars grown in large monoculture are vulnerable, banana plantations use pesticides extensively [6]. Banana plantations managed in an environmentally conscientious manner contribute large amounts of bananas to the global economy while minimizing adverse effects on the environment. When plantations are improperly managed, environmental contamination of wildlife, plants, water, air, and soil can occur. This contamination can result in injury to nontarget organisms, which in turn can lead to indirect effects at the ecosystem level [1,7]. Other mismanagement leads to soil erosion, soil nutrient depletion, and deforestation for banana cultivation [6]. Poor transport and improper storage of agricultural chemicals in developing countries are believed to result in a loss of pesticides of as much as 10% before application compared with 0.2% in developed countries [8].

BANANA PRODUCTION

Banana production for export dominates the economy of many tropical nations; banana cultivation in some Caribbean countries is so extensive that plantations cover almost entire islands [9]. Extensive commercial banana cultivation is also found throughout Central and South America, and plantations are common in Ecuador, Costa Rica, Colombia, Honduras, Guatemala, and Panama [10]. The economic importance of this crop and the specific conditions required for its commercial production have led to the development of several criteria for optimizing plantation productivity. Many of these criteria have the potential to affect humans and the environment either directly or indirectly.

Climate

Temperature and rainfall determine how well suited an area is for banana production [6]. Areas that are characterized by warm temperatures and extensive rainfall are optimal, and as a result, most production occurs between 27°N and 27°S latitude [11]. Optimal temperatures for foliar and fruit growth range from 26 to 30°C, and water requirements for proper growth are high. On average, banana plants require between 25 and 50 mm of water per week depending on evapotrans-piration rates. Most areas where bananas are cultivated receive more than 75 mm of rainfall monthly throughout the year. However, many areas occasionally experience dry seasons when less than 75 mm of rainfall per month occurs. In these situations irrigation is needed and is usually used two or three times per week. Irrigation usually delivers 25 to 44 mm of water per week [3], and overhead and undertree sprinkler systems are generally used [6].

Soil and drainage

Banana plants are fragile and highly susceptible to fungal infestations. Roots must be grown in soils that are well aerated and moist but that do not retain stagnant water [3]. Soils must therefore have good drainage capacity so that excess water is removed from the base of the growing plants. In general, soils should be at least 60 cm deep and should remove water from the root zone within 24 h. Flat porous soils are best for transport, irrigation, and erosion control in commercial banana production; however, some cultivation also occurs on sloped terrain [3]. Extensive drainage systems are coupled with the flat porous soils to promote runoff into local river systems. Properly designed drainage systems remove all standing surface water under the banana plants within 2 h and consist of principal canals and primary, secondary, and tertiary drains [6].

Soils must also have high nutrient content to maintain proper yields [11]. Nitrogen, potassium, and phosphorous are essential components of banana plantation soils, as are calcium, sulfur, magnesium, iron, manganese, zinc, and copper [3]. Manuring or fertilization of soils for proper nutrient content is necessary in all but very exceptional soils [3]. The best soils are usually deep, well-drained loams with a high humus content [11]. In tropical countries ideal soil conditions are most often found in forested areas, which generally have high nutrient content. Once these areas are cleared, little maintenance for desired fruit production is required [6].

Land preparation

Land for banana cultivation is classified either as virgin or rehabilitated from an existing plantation [6]. In tropical countries bananas are often cultivated on virgin land where forests have recently been cleared [12]. After the area is cleared of all underbrush, herbicides are applied to eliminate weeds. Road and drainage system infrastructure is then installed, and the area is planted [6]. Large trees are removed, and the remaining forest overstory is cut back [6,11]. Irrigation and cable ways are then installed on the new plantation during the first few months of growth [6]. When rehabilitating an established plantation, mechanical cultivation is often used to remove the adult banana plants [6,11,12]. Rather than removing the plants by hand, herbicides, such as 2,4-D (2,4-dichlorophenoxyacetic acid), are used to eliminate established plants [11] and the suckers that sprout from them [6]. Drainage and irrigation systems are then restored, and the plantation is replanted [6].

Fertilization

Continuous harvesting, leaching, and erosion remove considerable amounts of mineral nutrients from the soil and prompt the use of fertilizers on the plantation [12]. Fertilization programs vary from region to region and are established on the basis of soil and foliar analysis and on the yield potential of the area [6]. For example, fertilizer application in Central America ranges from 290 to 1,070 kg/ha per year [6]. All banana plants have high nitrogen and potassium requirements, and all plantations apply these two elements at the general rates of 300 to 600 kg N/ha four or more times a year and 400 to 800 kg K/ha once or twice a year [6]. Sources of nitrogen used on plantations include urea, ammonium nitrate, and ammonium sulfate [6]. The primary source of potassium is potassium sulfate [12]. The nitrogen and potassium fertilizers are generally applied to the crops through irrigation water by adding them directly to the planting hole [6,11] and by manually applying granular formulations to the base of developing plants [6,12]. In the past, aerial application was also used to deliver fertilizers to banana crops [6]. Bananas also require calcium, magnesium, sulfur, and zinc. In regions where these elements are required, they are supplied in addition to the usual nitrogen and potassium fertilizers [6].

Weed control

Weeds must be continually controlled on the plantation, especially before the banana plants develop a canopy, which naturally destroys shade-intolerant weed species [3]. Growth of grass weeds can be considerable in bright sunlight, and the amount of herbicide needed to control these weeds can be extensive [6]. Herbicides are first applied where grass growth is abundant 2 to 3 weeks before planting and again once the banana plants reach a height of 1 to 1.5 m [6]. Once a canopy is established, grasses can still be a major problem anywhere sunlight can enter, especially around the edges of the plantation and along roads and drainage ditches. Herbicides are again used to control the grasses and may occasionally be applied directly into the drainage ditches to rid them of plant material that could impede runoff water [6]. Shade-tolerant weed species must also be controlled once the canopy has developed because they may harbor pathogens that could damage the crop. Herbicides such as 2,4-D and paraquat (1,11-dimethyl-4,41 bipyridinium) are often applied to the understory to eradicate the weeds that emerge at the base of the growing plants [3].

Nonchemical forms of weed control are also used on banana plantations. Mechanical cultivation, for example, is used in rehabilitating old plantations but is not recommended once planting has occurred. Because banana root system is superficial, any mechanical cultivation could damage the root and possibly kill the plant [11,12]. Chopping weeds off just above soil level using a machete is another form of weed control that is recommended before or after planting. Hand slashing is done every 6 to 8 weeks until the weeds are shaded out by the banana plants [3]. This method, however, may promote a grass-dominant weed cover that can lead to nitrogen deficiency in the crop [12]. Hand slashing is also labor intensive and is considered more costly than herbicide use. This has led to an increasing tendency to use chemical methods for weed control instead of hand slashing [3,12]. However, herbicide use has often led to increased soil erosion in high-rainfall areas [6].

Pest control and fruit protection

Banana plants are attacked by over 200 insect pests that either directly damage plants or act as pathogen vectors [11]. Chemical control of insects on plantations is mainly directed toward the control of boring insects and certain thrips because other insect pests cause only minimal damage to the crop [6]. Use of insecticides to control these pests, however, has caused decreased numbers of insect predators and parasites and has led to outbreaks of insect pests that were previously of little importance on banana plantations [13]. Banana growers, therefore, rely heavily on integrated pest management for insect pest control [6]. Control methods include using clean planting material, keeping the base of plants clear of weeds, trapping pests, bagging fruit, dipping vulnerable plant parts in insecticides, and treating fields with insecticides [3]. Field treatment is performed by both aerial application and manual spraying of infested plants [6].

Nematodes also damage crops by burrowing into the base of plants and promoting fungal and bacterial infestations. Unlike the elective use of insecticides, however, nematocide must be used on the plantation to control nematode pests [6]. Before planting, banana corms are soaked in warm water and coated with mud containing nematocides. Soils may also be disinfected by treatment with nematocides [3]. Nematocides are then applied manually in granular and liquid formulations and are sometimes applied in irrigation water [6]. Applications are generally made every 6 months, at the beginning and end of the rainy season [6].

Fungal diseases are one of the main problems on banana plantations. Fungicides are applied to the plantations extensively by aerial spraying [6]. Fungicide formulations are mainly petroleum oil or oil mixed with fungicides and are applied in 1- to 2-week cycles [3]. Fungicide application is suspected to be responsible for the copper contamination of some Costa Rican soils, and these soils may be unsuitable for most agricultural production [4]. Herbicides are also applied to fungus-infected plants to destroy the plant and reduce spread of the disease [6].

Fruit protection is crucial for all bananas destined for export. The fruit is bagged to reduce scarring by insects, nectar-feeding bats, and fungal pathogens. Bags are saturated with pesticides and are placed on banana bunches as soon as their flowers emerge from the plant and are fertilized. Bags are replaced twice a week, and the used bags are discarded [6]. Bags sometimes fall from the bunches and end up in drainage ditches, eventually winding up in the river systems adjacent to the plantation [14]. The ECO-OK program, sponsored by the Rainforest Alliance, has encouraged plantations to collect and recycle all plastic bags [4]. Fruits are also sprayed with fungicides and alum before shipping to reduce postharvest rot and discoloration due to latex contacting the banana fingers during transport [6,11].

Agrochemical use and storage

Pesticide imports in Costa Rica are extensive, with approx. 700 pesticide formulations containing about 200 different active ingredients registered [15,16]. These include several different types of insecticides, herbicides, fungicides, nematocides, organic chemical-based solvents used for mixing toxicants, and petroleum-based dispersion agents [15]. Of the agro-chemicals imported to Costa Rica in 1989, approx. 35% were herbicides, 33% insecticides and nematocides, 28% fungicides, and 4% other pesticides and growth regulators [15]. Efforts to centralize agrochemical distribution in Central America has resulted in the shipment of technical-grade active ingredients that are mixed in Costa Rican processing plants [15]. Appendix 1 lists the names of agrochemicals that are used in the banana cultivation industry in Latin America (Ecuador Trade Center, personal communication; Embassy of Costa Rica, personal communication).

The techniques used to apply agrochemicals in banana cultivation depend on plantation size and pesticide type. Both small and large plantations utilize workers that spray pesticides by hand, while larger plantations also use aerial application by small planes [6]. Workers applying pesticides by hand most commonly use lever-operated knapsack sprayers that are worn on their backs [17]. Damaged or poorly maintained sprayers that leak are considered to be major sources of pesticide exposure and contamination [17]. Soil fumigants for nematode and fungus reduction are typically applied using knapsack sprayers, which pump pesticides into the soil to minimize release into the air [18]. Pressure inside soil trenches, however, can sometimes cause the pesticide to splash back on workers [19] Fungicides are also commonly aerially applied on both large and small plantations [6]. Herbicides are commonly applied aerially after trees are removed during land preparation and by workers that target active growing weeds and tree saplings.

Developing countries have also been characterized as having poor agrochemical storage and management practices [8]. Problems that have been most frequently observed in agro-chemical stores include poor pesticide labeling, permeable floors and walls, no feature for retaining spills, and inadequate ventilation and lighting. Also, between 25 and 50% of stores were located near drainage channels where spills could enter the water. Inadequate training on pesticide use can also lead to unnecessary pesticide exposure and contamination [7,8,15]. The majority of workers in pesticide stores were considered to be only superficially trained on pesticide use, while between 25 and 50% of the workers were considered to be either virtually untrained or unable to advise on proper pesticide use [7]. The ECO-OK project has also developed a program to improve handling and storage of chemicals [4].

Potential for adverse environmental and health effects

Evidence indicates that pesticides can cause acute toxicity and may also act as molecular inducers of cellular activity responsible for neuroendocrine functions that regulate hormonal control of reproduction, sex differentiation, cell proliferation, and immune system competence [20–22]. In the past, compounds such as DDT, 1,1′-(2,2,2-trichloroethylidene)bis(4-chlorobenzene), and other organochlorine (OC) compounds were characterized as having relatively low acute toxicity to mammals [23]. However, in response to phenomena such as egg shell thinning and the bioaccumulation of OCs in fatty tissues in long-lived organisms, less persistent compounds, such as organophosphate (OP) and carbamate pesticides, were developed [23]. Although these chemicals are less persistent in the environment than OCs, they are much more acutely toxic [24]. As a result, many occupational pesticide poisonings are attributed to the increased use of new pesticide formulations [25]. The World Health Organization estimated in 1985 that pesticide poisonings affected approx. 3 million people per year and resulted in 220,000 deaths annually. Approximately 99% of these poisonings are estimated to occur in developing countries, where training on proper pesticide use is limited and proper safety equipment is infrequently used [26]. Poor application techniques are suspected to cause such poisonings in Central America, and a number of adverse effects in workers and their families have been recorded [19,26,27]. Costa Rica alone has hundreds of cases of poisonings registered annually [15]. Approximately 33% of these poisonings occur in the banana sector of the country, which comprises only 5% of the rural population [27].

Humans and wildlife can be exposed to pesticides through aerial applications, food items, and contaminated drinking water. Aerial application is a rapid technique for delivering pesticides to large areas, but runoff from pesticide storage sites and landing strips and drift of agrochemicals from target sites may contaminate neighboring terrestrial and aquatic ecosystems [8]. Rainfall causes pesticide residues to leach into the soil, making them available to subterranean organisms, and runoff carries residues from the site of application into aquatic systems [28,29]. Contamination of water from washing bananas prior to shipping may provide another direct source of entry into aquatic ecosystems and into drinking water supplies.

EFFECTS ON HUMANS OF AGROCHEMICALS USED ON BANANA PLANTATIONS

Organochlorines

Most OC pesticides have been banned in the United States, but many developing countries buy these compounds from U.S. chemical companies for agricultural uses [21]. In Costa Rica, for example, some OCs were banned in the late 1980s, but Mirex (1,1a,2,2,3,3a,4,5,5,5a,5b,6-dodecachlorooctahydro-1,3,4-methen-1H-cyclobuta[cd]pentalene), pentachloronitro-benzene, endosulfan (6,7,8,9,10,10-hexachloro-1,5,5a, 6,9,9a-hexahydro-6,9-methano-2,4,3-benzodioxathiepin 3-oxide), heptachlor (1H-1,4,5,6,7,8,8-heptachloro-3a,4,7,7a-tetrahydro-4,7-methanoindene), lindane (1,2,3,4,5,6-hexachloro-cy-chlohexane), and dienochlor (1,1′,2,2′,3,3′,4,4′,5,5′-decachlorobi-2,4-cyclopentadiene-1-yl) were still being used in 1991 [15]. The problem with OC pesticides is that they tend to persist in the environment, increasing exposure to wildlife and humans [16]. They are also highly lipophilic and are stored in the fat tissues of exposed individuals and accumulate over time [22]. Organochlorines have also been documented to affect normal endocrine function, causing a variety of adverse physiological effects that are now being intensely studied [30].

Humans are not exempt from the phenomenon of bioac-cumulation of OC pesticides. Human tissue samples taken from Costa Rican hospitals contained alarmingly high concentrations of OC compounds [15]. Also, DDT and its metabolite DDE (2,2-bis(4chlorophenyl)-1,1 dichloroethylene) were found in 100% of the adipose tissue samples collected. Hex-achlorobenzene was found in 98% of the samples, and heptachlor was found in 90%. The mean DDT concentration in adipose samples was 33.2 μg/g. Concentrations in tissues of agricultural workers were significantly higher than in non-agricultural workers. Agricultural workers had a mean DDT concentration of 59.3 μg/g in their tissues, while nonagricul-tural workers had a mean DDT concentration of only 13.7 μg/g. Because of its high lipid content, human breast milk also accumulates high concentrations of OCs [15]. The World Health Organization considers concentrations of DDT greater than 0.05 μg/g in cow's milk to exceed the maximum residue limit. Breast milk samples taken from Costa Rican hospitals and separated by regions from which the samples were collected all had mean DDT concentrations that exceeded the maximum residue limit [15].

Sterility also occurred in Costa Rican banana plantation workers after exposure to the nematocide dibromochloropro-pane (DBCP) [27]. Men were exposed to DBCP while mixing and applying the compound without using appropriate protection devices to prevent exposure. Lawsuits filed by these workers resulted in the payment of $2,000 to $3,000 to each man by the chemical manufacturers in the United States because the chemical containers were improperly labeled and/or were labeled only in English. The potential adverse effects of DBCP were known in the United States because of tests in laboratory animals and in workers exposed to this chemical during production [27]. Use of DBCP in the United States was discontinued, but the chemical companies that produced this compound continued to sell it to countries where its use was still not prohibited [27]. Under current U.S. laws, the export of toxic chemicals is not limited, even if the chemicals have been determined to be hazardous to health [31]. In 1981 a government order known as Executive Order 12264 was enacted to restrict export of toxic chemicals whose sale had been banned in the United States. This order, however, was revoked in 1981 by President Ronald Reagan in one of his first acts [31]. Currently, many of the chemicals being used in banana cultivation have been or are in the process of being discontinued in the United States because of concerns about their toxicity [15].

Organophosphates and carbamates

Organophosphate and carbamate pesticides are designed to be acutely toxic and to degrade rapidly in the environment. Since their development, physicians have been called to diagnose and manage a growing number of pesticide-related poisonings [25]. Because of the acute toxic nature of these compounds, improper use and handling could easily lead to workers being exposed to concentrations that could produce adverse effects. One study, conducted to determine the risk of crop duster aviation mechanics in Nicaragua to pesticide exposure, found that 61% of the workers sampled had depressed erythrocyte cholinesterase levels, strongly suggesting pesticide exposure [32]. In 1988 in Pitahaya, Costa Rica, several workers were treated for symptoms ranging from headache and dizziness to vomiting blood after applying the OP pesticide terbufos, phosphorodithiocic acid S-([(1,1-dimethylethyl)thio] methyl)O,O-diethyl ester, to sugarcane crops [26]. These workers had not been properly trained and failed to use protective gear to limit their exposure. Human exposure to trichlorfon, (2,2,2-trichloro-1-hydroxyethyl)-phosphonic acid dimethyl ester, an OP currently used in Costa Rica, resulted in congenital malformations in 73% of births in a small Hungarian village [33]. It was determined that these malformations resulted when the insecticide was used to kill mosquito larvae in nearby fish ponds.

The first phase of OP poisoning involves a cholinergic crisis resulting in miosis, salivation, and sweating [25]. An intermediate syndrome is then observed 24 to 96 h after exposure and is characterized by muscle weakness without other cholinergic manifestations [34]. Weakness of muscles responsible for respiration often leads to respiratory failure that cannot be treated with typical treatment for OP poisoning, and mechanical ventilatory support is required [25]. Patients can also develop a delayed peripheral neuropathy affecting the distal muscles of the extremities [25]. Delayed neuropathy occurs 2 to 3 weeks after exposure and is characterized as distinct from the early onset of the intermediate syndrome [34].

EFFECTS OF AGROCHEMICALS USED ON BANANA PLANTATIONS ON WILDLIFE AND POTENTIAL RISKS IN THE TROPICS

Organochlorine

Wildlife can experience acute toxicity from OC exposure either through direct exposure to the compound or through secondary exposure after ingesting contaminated food items [35]. Fish are highly susceptible to direct exposure to OC pesticides, and even modest treatments (e.g., 0.5 to 1.0 lb/acre) can produce concentrations in aquatic systems that are lethal to fish [22]. For example, significant fish kills were recorded after a 0.22 kg/ha application of DDT [35]. Birds tend to be less sensitive to most OC pesticides than fish but are highly sensitive to the OCs aldrin (1,2,3,4,10,10-hexachloro-1,4,4a,5,8,8a-hexahydro-1,4:5,8-dimethanonaphthalene), dieldrin (1,2,3,4,10,10-hexachloro-6,7-epoxy-1,4,4a,5,6,7,8, 8a-octah-ydro-endo,exo-1,45:5,8-dimethanonaphthalene), and heptachlor [35]. These compounds caused die-offs of granivorous birds in Great Britain where chemicals had been used as seed dressings. Mortality was also recorded in predatory bird species exposed to high concentrations of DDT [36]. Foxes that preyed on dead and dying birds that were exposed to aldrin, dieldrin, and heptachlor also obtained sufficient levels of these chemicals to result in mortality [35]. In general, however, wild mammals appear to be rather resistant to the acute toxic effects of OC pesticides [22].

Organochlorine compounds have also been documented to have severe effects on reproduction by altering normal endocrine functions that regulate sex differentiation and reproduction [30,37]and by targeting reproductive organs [27]. For example, some OCs possibly mimic the female hormone estrogen and block the effects of the male hormone androgen. In Lake Apopka, Florida, USA, the DDT metabolite p,p′-DDE appears to be primarily respon sible for blocking androgen in alligators (Alligator mississippiensis), resulting in feminization of male juveniles. Egg shell thinning associated with exposure to OC contamination has also resulted in reproductive failure in numerous bird species [38]. In Anacoba, Santa Barbara, California, USA, for example, there was a large reduction in hatchling brown pelicans (Pelecanus occidentalis) because of OC-induced egg shell thinning. In one nesting season, only five nestlings successfully hatched out of a minimum of 1,272 nesting attempts because thin egg shells collapsed during incubation [39]. Continued use of these pesticides for agriculture in developing countries will likely increase OC concentrations in the environment because of the persistence of these compounds.

Studies suggest that some OCs also have carcinogenic potential [16]. Mice dosed with 10 ppm of dietary dieldrin showed a significant increase in the formation of benign liver tumors, and the OC Mirex has also been reported to be carcinogenic in mice [22]. Another study performed on mice has shown that exposure to the OC lindane (gamma benzene hex-achloride) causes reduced humoral immune response, resulting in increased susceptibility to infection [40]. Reduced immune response could result in epidemics and reduced survivability of exposed populations. Caterpillars (Pieris rapae) exposed to DDT showed signs of reduced immune response, and individuals on treated plots were more vulnerable to the granulosis virus than individuals on untreated plots [35].

Because of the lipophilic nature of OC pesticides, sublethal exposure can result in accumulation of high concentrations of these compounds in the fat reserves of wildlife [35]. Wildlife that occupy higher trophic levels are at a greater risk of bioaccumulation because of the concentrations of OCs they are exposed to in food items [22]. During periods of stress such as starvation, migration, reproduction, or molting, lethal doses of OCs can be released into the bloodstream when fat reserves are utilized, causing acute poisoning of the individual [41]. Therefore, individuals subjected to the stresses involved with the tropical dry season may in turn be more vulnerable to the acute toxic effects of OC compounds. Also, migratory species, such as Neotropical migratory birds, may be exposed repeatedly to sublethal concentrations of OCs on their migratory routes. Declines in the numbers of Neotropical migrants have recently been recorded, although no direct correlation between these declines and the use of agrochemicals in the tropics has been documented [42].

Organophosphates and carbamates

Direct mortality of wildlife has been frequently reported following the use of OP pesticides [43]. In Essex, UK, a spill of the OP chlorpyrifos caused a die-off of all the arthropods and 90% of the fish in a 23-mile (36.8 km) stretch of the River Roading [44]. Certain OP compounds under the proper exposure/reexposure conditions can cause peripheral neuropathy in animals that is permanent with minimal recovery. Organo-phosphate-induced delayed neuropathy has developed in humans exposed to OP compounds through accidental poisonings and suicide attempts, even from a single nonlethal dose [34].

Effects of carbamate insecticides are very similar to those of OP compounds. Carbamate pesticides, however, do not bind as tightly to acetylcholinesterase, and recovery is often more rapid. Wild rabbits (Sylvilagus floridanus) exposed to a granular form of the carbamate aldicarb, 2-methyl-2-(methyl-thio)propanal O-[(methylamino)carbonyl]oxime, experienced acute toxicity after feeding on a mint bush to which the pesticide had been applied. A single mint leaf produced severe muscle twitching, but the animal recovered after 3 h. Three grams of mint leaves killed one rabbit within 2 h [45].

Direct effects of OPs on the reproductive system of wildlife have also been reported. The OP parathion, phosphorothioic acid O,O-diethyl O-4(4-nitrophenyl)ester, has been shown to affect breeding success and hormone levels in bobwhite quail (Colinus virginianus) [46]. Acetylcholinesterase (AChE) activity in birds dosed with 400 ppm was 30% less than that of control birds. Decreased food intake and loss of body weight were also observed. Ovarian weight was 12% lower in dosed birds than in controls, and egg production was 30% lower. These effects were traced to a decrease in luteinizing hormone and steroid hormones in the exposed birds [47]. Other OPs, such as diazinon, phosphorothioic acid O,O-diethyl O-[6-methyl-2-(1-methylethyl)-4-pyrimidinyl]ester affect mice and fathead minnows in the developmental stage, resulting in deformities and reduced numbers of live young. Diazinon also inhibits chicken embryo kynurenine foramidase, which results in a decreased concentration of nicotine adenine dinucleotide in the embryo and abnormal feathering and micromeli [48]. Lannate 20, N-[(methylcarbamoyl)oxy] thioacetimidic acid methyl ester, an experimental carbamate nematocide used in Central America, also induced abnormal sperm in mice after 35 d of exposure [49]. The direct reproductive effects of OP pesticides may occur as a result of inadequate synthesis of the neurotransmitter norepinephrine due to inhibition of dopamine beta hydroxylase [50]. Norepinephrine plays an important role in pituitary function and therefore has an indirect affect on reproductive hormones.

Indirect reproductive effects can be attributed to OP-induced aberrant behavior. Care of nestlings by female starlings (Sturnus vulgaris) treated with the OP dicrotophos (phosphoric acid 3-(dimethylamino)-1-methyl-3-oxo-1 propenyl dimethyl ester) at a dose that reduced brain AChE to 50% resulted in significantly fewer returns to the nest to feed young and longer time duration away from the nest. Nestlings of treated parents also lost significantly more weight than controls [51]. A similar study involving male starlings dosed with dicrotophos at the same 50% AChE depression level showed behavior of male starlings to be markedly altered within 2 to 4 h of dosing [52]. Treated birds spent significantly more time perching and less time flying, singing, and displaying. Similar aberrant reproductive behavior was also recorded in zebra finches (Poephila guttata) exposed to fenitrothion (phosphorothioic acid O,O-dimethyl O-(3-methyl-4-nitrophenyl)ester) [53]. During gestation carbofuran can cross the rat placenta and inhibit AChE in fetal tissues to a greater extent than in maternal tissues, causing behavioral and neurologic effects in newborns [54]. Also, experiments with embryos and tadpoles of the frog Microhyla ornata at near-lethal doses (28 μg/L for 96 h) caused blisters on the body, distension of body cavities, curvature of the body axis, poor blood circulation, poor pigmentation, growth retardation, loss of balance, and listless behavior [55].

Organophosphate and carbamate pesticides can also affect immune system competence. Malathion [(dimethoxyphosphin-othioyl)thio]butanedioic acid diethyl ester), parathion, dichlorvos (phosphoric acid 2,2-dichloroethenyl dimethyl ester), and methyl parathion (phosphorothioic acid O,O-dimethyl O-(4-nitrophenyl)ester) have all been documented to suppress humoral immune response in laboratory mice [56], and other compounds produce autoimmune function changes such as hy-persensitivity and sensitization. Aldicarb has been documented to affect splenic plaque-forming response in mice injected with sheep red blood cells, indicating a depressed ability to recognize nonself from self, which is crucial for proper immune function [57]. Organophosphate compounds have also been reported to inhibit salt gland function essential for the survival of birds maintained on drinking water with an electrolyte composition equivalent to seawater [58]. Additionally, parathion has been associated with increased cold stress through a rise in corticosterone levels in quail [59] and kestrels (Falco sparverius paulus) [60].

Fungicides

Once in the soil, fungicides can strongly inhibit the normal nitrification process that occurs in soil through selective effects on soil enzyme processes and can modify the biodegredation of soil organic matter [61]. Also, the lethal effects of fungicides on soil fungal growth could affect decomposition processes, resulting in decreased soil fertility [29]. These compounds can also leach out of soil during heavy rains and contaminate streams and aquatic ecosystems [29]. Chlorothalonil (2,4,5,6-tetrachloro-1,3-benzenedicarbonitrile) is highly toxic to aquatic invertebrates and may affect their reproduction at concentrations less than 80 ppb [62]. It can also affect fish populations at concentrations less than 10 ppb [62]. Because its half-life is between 1 and 8 d, there is the potential for invertebrate populations to recover between episodes of high concentrations if daily rains during the wet season do not overwhelm the system.

The fungicide mancozeb (ethylenebis (dithiocarbamic acid) manganese zinc complex) is a mixture of maneb (a known carcinogen) and zinc. This substance is still in use in Central America. The ethylene-bis-dithio carbamates are being discontinued from registration in the United States because of concerns for mutagenicity and teratogenicity in laboratory animals [63]. Sensitization to dithiocarbamate pesticides in florists has resulted in contact dermatitis [18]. Benomyl, methyl-1-(butylcarbamoyl-2-benzimidazole carbamate), a fungicide with systemic activity that is applied to bananas prior to shipment, is a carbamate fungicide that does not inhibit cholin-esterase activity. It is, however, a teratogen and has been shown to cause reproductive impairment [64]. Teratogenic effects can result in death [45]

A soil fumigant mixture of 1,3-dichloropropene, 1,2-dich-loropropene, and chloropicrin or epichlorhydrin is applied to soil trenches and covered. It has replaced the use of ethylene dibromide as a soil fumigant in banana plantations. It is mobile in soil and can potentially contaminate groundwater supplies under conditions of very heavy rains [65]. This substance is a possible human carcinogen (U.S. Environmental Protection Agency (EPA) class B2) that has caused neoplastic lesions in the fore stomach, urinary bladder, lung, and liver of rats. Sensitization in humans resulting in dermatitis has been reported in workers that have been repeatedly exposed to epichlorhydrin [66]. Other studies suggest links to cancer in humans [67].

Herbicides

Paraquat is the most widely used postemergent herbicide on banana plantations in Latin America and the Caribbean [68]. Paraquat has extensive respiratory effects in humans and animals that are independent of the route of exposure. Teratogenicity in mice from exposure to paraquat has also been reported. Hens exposed to 40 ppm paraquat in drinking water produced eggs with concentrations of the compound as high as 0.1 ppm. Ingestion, inhalation, or dermal exposure to even small amounts may result in severe toxicity and death within 24 h. Necrosis of the lung, liver, kidneys, adrenals, and heart were the cause of death. Survivors of paraquat poisoning often develop progressive pulmonary fibrosis within 5 to 10 d of exposure [18].

The simazine (6-chloro-N,N′-diethyl-1,3,5-triazine-2,4-diamine) herbicide family has also been used widely for preemergent weed control. Recent concerns of the effects of the triazine herbicides to wildlife populations and to aquatic ecosystems have resulted in current action by the EPA to limit the use of these compounds in areas where endangered species are found [69]. Glyphosate (N-(phosphonomethyl)glycine)use is also widespread on banana plantations. This substance is a highly effective systemic herbicide that partitions to sediments, where it can act on aquatic grasses and other plants, disrupting critical habitat [18].

Effects of agrochemicals on aquatic ecosystems

Aquatic systems are often incorporated into the drainage system of banana plantations so that excess water may run off of into local streams and rivers and not promote fungal growth [6]. Aquatic ecosystems are vulnerable to the insults of pesticide runoff because of the large amounts of runoff originating from drainage systems [6], compounded by the nature of many pesticides to leach into aquatic systems from the soil [29]. However, regulations to incorporate buffer zones between areas of banana production and aquatic systems can reduce the amount of pesticides that leach into these systems from the soil [70]. If buffer zone management is ignored, however, widespread contamination beyond the plantation could occur as pesticides are washed from plantations during irrigation and episodes of increased precipitation.

Contaminants that leach into riverine systems from the soil in agricultural areas may also remain in the system for extended periods and ultimately enter marine environments. For example, the pesticide DBCP can remain in aquatic systems for up to a month because its half-life increases as it converts into an aqueous form [18]. In the tropics, contaminants that do reach the coast can then be trapped and accumulate in mangrove swamps and coastal waters [71] and threaten the diverse wildlife that live in these habitats. Water movement can be reduced along tropical coastlines by lower tidal amplitudes that trap contaminants in coastal waters and prevent dissolution [71]. In shallow mangrove coastlines, for example, the prevention of eddy and tidal jet formation in shallow waters and the buoyancy effect of light freshwater on top of heavy saline water increased the residence time of runoff water in a mangrove swamp by at least 2 weeks [71].

Eddy formation between the coastline and coral reefs, however, has the opposite effect. Reefs form natural barriers for water entering the ocean from inland rivers and promote eddy formation between the coast and the reef [72]. These eddies can trap contaminants between the coast and reef, resulting in an increase in the duration of exposure of a reef to contaminants [72]. Coral reefs are highly vulnerable to both the pesticide residues in runoff and the increased amount of sediments carried in runoff because of erosion. Reef-building corals are highly adapted to survive in water with low concentrations of suspended particulate material and humic acid [72]. Alteration of water quality induced by activities associated with banana production are suspected of having effects on coral reef ecosystems. For example, the use of herbicides on banana plantations to eradicate understory vegetation can lead to increased incidence of erosion [6]. Erosion can increase particulate and humic material in marine environments, detrimentally affecting corals. Herbicides have also been shown to detrimentally affect coral reef species through direct toxicity [72]. A 10 ppm concentration of the herbicide 2,4-D caused considerable tissue loss and 100% mortality in exposed corals after 48 h, while another study showed that a concentration of 2,4-D of as little as 60 ppb had sublethal effects on the corals Montastrea annularis, Acropora cervicornis, and Madracis mirabilis. Residues of DDT are also suspected to reduce coral growth rates [72]. Tissue samples with detectable levels of herbicide residues from corals collected from dead and dying reef colonies have also been collected off the Pacific coast of Panama [72].

When viewing contamination of aquatic ecosystems in the tropics it is important not to base conclusions solely on models derived from temperate zone systems, because this can often lead to inadequate assessment of the situation. Variations that occur between tropical and temperate aquatic ecosystems can affect the way water pollutants behave in these systems (Appendix 2) [73].

Many of these variations could enhance the detrimental effects pesticides have on tropical ecosystems. Although contaminant depletion rates can be higher in the tropics, individuals organisms can show more rapid uptake of and increased sensitivity to agricultural chemicals that enter aquatic ecosystems [73]. Toxicity thresholds for certain individuals can also be lower in the tropics; however, considering the extensive use of pesticides, the high volume of runoff associated with tropical agriculture, and the hydrodynamics of tropical aquatic ecosystems, it is likely that environmental concentrations of pesticides and their metabolites often exceed threshold limits [71,73].

CONCLUSIONS

The use of pesticides in agriculture has definitely lead to increased yields of agricultural products throughout the world. Pesticides, however, can have detrimental effects on both wildlife and human populations when carelessly used. Developing countries have high incidences of pesticide-related poisonings, and improper handling and storage are common. A variety of pesticides are applied to banana crops in large quantities to control the pests that abound in tropical climates. These chemicals can ultimately be dispersed over large areas where their toxic affects may be experienced by a variety of organisms far from the agricultural site. Aquatic ecosystems can become contaminated with pesticide residues, soil erosion can be promoted through herbicide misuse, and humans and wildlife can suffer health effects such as dermal sensitization, severe reproductive impairment, and death.

New pesticide formulations used in the production of agricultural goods may degrade rapidly but pose a considerable hazard for acute toxicity. Humans living in agricultural areas or working with these pesticides are generally untrained and are often poisoned when the pesticide application is not contained and protective equipment is not used. Chronic exposure to lower doses of OP and carbamate pesticides can also result in delayed neuropathy, aberrant behavior, and congenital abnormalities. Persistent pesticides can alter normal endocrine functions, resulting in abnormal cell growth and proliferation, decreased reproductive success, and reduced immune system competence. Continuous exposure leads to bioaccumulation of these chemicals in wildlife and humans alike. Biomagnification of OCs through the trophic levels can affect individuals high in the food chain and can possibly result in acutely toxic levels in individuals during migration or during other stressful episodes.

Aquatic ecosystems are especially at risk to the effects of agrochemicals because of the large amounts of runoff that occur during irrigation and episodes of increased precipitation. Acute toxicity can occur throughout the trophic levels and can result in either death or impairment of affected individuals. Communities of aquatic microorganisms may also fluctuate in response to the effects of chemicals as they enter these systems in runoff. This would have indirect effects on organisms occupying higher trophic levels that depend on these organisms for their survival.

The EPA published a framework for conducting ecological risk assessments [74] that has become an operational paradigm both within and outside the EPA. Indeed, the Office of Research and Development in the EPA has reorganized around this paradigm so that both health and ecological risks can be fully integrated [75]. The value of the risk assessment paradigm is that it allows researchers to examine multiple impacts on populations or ecosystems and prioritize future research to deal with the most pressing problems. The EPA's risk assessment paradigm has been successfully applied to terrestrial [76] and aquatic [77] systems in the United States. The larger picture of the exposure of agricultural chemicals to terrestrial wildlife in general has also been examined from a risk perspective [78] in a manner analogous to the current situation in the cultivation of bananas in the tropics. The environmental problems that developing countries face are as large in scope and as expensive to resolve as those that we face in the United States. Therefore, the environmental risk assessment paradigm would be of tremendous value to developing nations by allowing them to prioritize their research activities to make the most effective use of limited funds. Sufficient data currently exist to conduct a formal environmental risk assessment of the use of agricultural chemicals on banana plantations so that priorities for future research and mitigation can be clearly defined and planned in the most cost-effective manner. Such a risk assessment would form the basis for future research on projections of environmental impacts over time under a variety of ecological and management scenarios [79].

APPENDIX 1

Table  . Agrochemicals used on banana production in Latin America
 
Insecticides
  Methomyl
  Diazinon
  Triclorfon
  Bacillus thurigiensis
  Carbofuran
  Chlorpyrifos (Dursban)
  Carbaryl (Sevin)
  Aldicarb (Temik)
Nematocides
  Mocap
  Fenamiphos (Nemacur)
  Turbufos (Counter)
  Dibromochloropropane (Nemagone)
  1,3-dichloropropene (Telone)
Fungicides
  Bitertanol
  Tridemorph
  Propiconazole
  Mancozeb
  Chlorothanolonil
  Benomyl
  Thiobendazole
  Methyl thiophene
Herbicides
  Paraquat
  Glyfosate
  Diuron
  Atrazine
  Glufosinate ammonium
Petroleum-based agricultural oils
  Spraytex
  Banole
  Probex
  Orohex
Emulsifiers
  Adsee 775
  NP-7
  Triton

APPENDIX 2

Table  . Characteristics of tropical aquatic ecosystems compared to those of temperate aquatic ecosystems [71]
CharacteristicTropical aquatic ecosystem
Biological uptake rateHigher
Biological release rateHigher
Rate of physiochemical degradationHigher
Rate of biological degradationHigher
Rate of oxygen depletionHigher
Biological impact of nutrientsHigher
Biological impact of suspended solidsHigher
Solubility of liquids and solidsHigher
Solubility of gasesLower
Toxicity thresholdsLower

Ancillary