American Journal of Botany 85(6): 835849. 1998.

THE

CASHEW NUT,

ANACARDIUM OCCIDENTALE

(ANACARDIACEAE), AND ITS PERENNIAL ASSOCIATION WITH ANTS: EXTRAFLORAL NECTARY LOCATION AND
THE POTENTIAL FOR ANT DEFENSE1

FRED R. RICKSON2,4
2

AND

MELINDA M. RICKSON3

Department of Botany, Oregon State University, 2082 Cordley Hall, Corvallis, Oregon 97331-2902; and 3 Corvallis, Oregon 97330

Cashew nut trees are consistently ant-visited throughout the year, with the ants attracted to a large number of extraoral nectaries on the leaves, inorescences, owers, and developing nuts. The commercial production of cashew nut, for example, in India, Brazil, and east Africa, consistently applies pesticides, especially insecticides, in large monoculture plantings. Each year prophylactic spraying begins with the rst ush of new leaves, continues through owering, ending at about mid-nut development. We surveyed for ant diversity in sprayed and unsprayed cashew monocultures of various sizes and ages in Sri Lanka, India, and Malaysia to document the ant-cashew relationship and to explore the potential of ants replacing chemical pesticides in insect control. Using for-prot, commercial-size plantations as examples, we present information that cashew has a strong potential for arthropod-dependent protection from pests and suggest important habitat considerations for encouraging ants within cashew plantings. Key words: agroecology; Anacardiaceae; Anacardium occidentale; ant plant; cashew nut; plantation crops.

The commercial cashew nut, native to coastal Brazil, is grown as a plantation crop and has become naturalized in tropical countries throughout the world. Collectively, cashew is usually considered the third or fourth greatest nut of commerce (by mass) worldwide (Food and Agricultural Organization of the United Nations, 1993), and as an agricultural crop provides important local and na1 Manuscript received 26 November 1996; revision accepted 25 September 1997. This study, spanning 11 years and including efforts in three countries, was made possible by the willing help of a number of individuals. We thank our colleagues Drs. Nimal and Savi Gunatilleke, and S.A. Kulasooriya, Head, Botany Department, University of Peradeniya, Peradeniya, Sri Lanka for constant help, friendship, encouragement, and invaluable advice and access to Botany Department facilities during our visit. Mr. Tissa Jayatilaka, Executive Director, United States Educational Foundation in Sri Lanka, offered continuous help in facilitating our efforts from our rst day in the country until we nished our stay. Mr. Percy Udalagama, Director, Sri Lanka Cashew Corporation facilitated our stay and work at the East and West Cashew Research Stations. Mr. Nalin Warusavitarana, Superintendent of the western Sri Lankan Cashew Corporation Research Station, made our efforts at his Station possible, and introduced us to Panadura Estate and other plantings in the area. Mr. and Mrs. G. Pushparanghnam welcomed us to their Sri Lankan estate, and Informatics Agrotech (Put) Ltd., Colombo, allowed us access to their extensive cashew plantings. Dr. Max Goldensohn, Development Alternatives, Inc. facilitated our use of private cashew estates in eastern Sri Lanka within the Mahaweli Agriculture and Rural Development Project, and graciously allowed us to lodge at staff private residences while in the eld. Dr. B.K. Nayar, Head, Department of Botany, Calicut University, Calicut, India initially pointed out that ants associate with cashew. The 1992 effort in Kerala, India was facilitated by Messrs S. Rajan, Babu Alexander, George Oommen, and Mathew K. Thayil. Mr. David Jones facilitated permission to sample at the Malaysian Agricultural University. Dr. Stephen Shattuck, CSIRO, Canberra, Australia, identied the ants, truly making the study possible, and Dr. Rudy Kohoot, Queensland Museum, Australia, identied the Polyrachis species. This research was supported by two Fulbright awards, the Oregon State University Research Council, and U.S. National Science Foundation Grant INT-9116312, to FRR. 4 Author for correspondence.

tional employment, and hard export currency, for a number of developing countries in Asia, Africa, and South and Central America (Andrighetti et al., 1994; Yaacob and Subhadrabandhu, 1995; Martin et al., 1997). Nuts from one to several individually owned trees are often harvested, and after a few days of sun drying, sold in local markets, sold to commercial buyers, or bartered. The nut is also roasted and consumed locally, while the inated, eshy pedicle of the fruit, the cashew apple, is eaten fresh or squeezed for juice. Processing plants, located in rural areas, purchase nuts, provide employment for women, and represent a local, diffuse cash infusion. After husking of the nut, the shells are often extracted for production of cashew shell liquor, an important deterrent to pests of boat hulls, shing nets, and stem borers of trees, which is also exported for use as a paint and rubber additive. The residue of cracked or expressed shells can be used as a fuel source in production level roasting of raw cashew nuts, or household cooking, thereby conserving local fuelwood and literally utilizing every last piece of the crop. Our interest in cashew began in 1985 with the observation that single, and small groups of cashew trees naturalized around Calicut, Kerala, India were visited by foraging ants, spiders, and wasps to a much greater degree than adjacent vegetation. It was the type of activity one commonly associates with a plant having a population of honeydew-producing Homoptera. Observation of the ants activity over a 3-wk period, revealed that ve different ant species were visiting extraoral nectaries located on both upper and lower leaf surfaces, the inorescence axis, and at the base of owers. The ants were foraging to the cashew trees from remote nest sites, following the trunk/branching system until encountering a nectar-producing leaf or inorescence. The ants methodically fed at a number of nectaries before descending the branch/trunk system, and returning to their nests. The 835

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trees, which produced a crop of nuts and inated pedicles harvested by local residents, showed no evidence of herbivory and there were no Homoptera present. Our initial hypotheses were that cashew represents an unreported example of plant-ant mutualism and that cashew represents a world crop that has the potential for being naturally ant protected. Further observations in Karala revealed that owners of individual trees or small plots of 510 trees are not concerned with pests and recognize that ants are often in the trees, but seemingly cause no problems. However, when cashew is grown in commercial-size, monoculture plantings, one consistently hears and reads of potential pest problems that become automatic justication for the worldwide recommendation of pesticide application; ants are often included in published pest lists. This led to another hypothesis that there is some minimal group number of trees below which, for whatever reason, the trees do not need chemical protection to produce a crop, and above which insects cause sufcient damage to warrant chemical intervention. The insect Helopeltis spp. (Hemiptera: Miridae) is endemic to, and drives insecticide usage, in Southeast Asia, India, and east Africa (Hill, 1983; George, Singh, and Peter, 1984). All tissues above the feeding location of this insect die, and if an attack comes early in the growing season each affected branch produces no leaves or owers/fruits for the year. A severe attack will see 75% of a trees branches damaged. A number of other pests cause minor disgurement of leaves and fruits, but do not seriously affect nut production and are usually ignored by growers. Currently, cashew pest abatement consists of recommendations for chemical formulations, application amounts, and timing, often based on what is used on coconut, which has been in production for a longer period of time and is frequently interplanted with cashew. We found several anecdotal notations in the Indian literature of incidental ant predation of certain cashew pests (Abraham, 1958; Ambika and Abraham, 1984; Pillai, Dubey, and Singh, 1976; Sundararaju, 1984), but nothing addressing the broader question of ants replacing chemical pest control as part of general crop management. Alternatives to chemical control have not been actively followed in any government cashew system we know of, and we are not aware of any ongoing trials using alternative pest control. In Brazil, the leading country in nut export, current practice calls for a pesticide effort, and in a recent summation of cashew growing and nut production (Lima, 1988), each perceived insect pest (18 in total plus two mites) is followed by a specic chemical pesticide for each organism (Melo and Cavalcante, 1988). We are not aware of any literature reference to cashew possessing extraoral nectaries. Cashew encourages a prophylactic, by-the-calendar pesticide application schedule because new growth onset is predictably triggered by a wet-dry seasonal weather change. A continuous production of new leaves is followed by owers and nishes with fruit, all on the same single branch system. It is easy to follow such an observable series of crop waypoints, initially spraying the rst or second new leaves, followed with an application at ower production, and ending with a third application

at mid-nut development stage. Chemical pest control of cashew involves traditional spray schedules using compounds like DDT (dichloro diphenyl trichloroethane), azinphos-ethyl, and gamma-BHC (benzene hexachloride) among others (Anonymous, 1995), which are often banned in developed countries (Farm Chemicals Handbook, 1994). At this time, usage of such materials on export crops does not seem to have caused any detectable residue problems, although as testing becomes more thorough this problem may arise. Of immediate concern, however, is that these toxic carbamates, organochlorines, organophosphates, and organosulfurs, are often applied with little or no concern for either the applicator or the environment. We spent 19911992 in Sri Lanka, West Malaysia, and southern India visiting cashew-growing establishments in order to qualify and quantify tree growth and development, examine the plantant association, sample cashew agroecosystem diversity (Risch, Andow, and Altieri, 1983), and to try and understand how Asian nut growers deal with pests. Because of other teaching and research obligations, and politically induced travel restrictions, we were not able to establish and revisit long-term ant exclusion experiments in order to quantify pest damage to cashew with and without visiting ants. Instead, we used a correlative approach of searching for examples of successful nonpesticide and pesticide-use estates, and then interviewing the growers to obtain historical information on such topics as tree selection, cultural practices, land use over time, crop size, disposition, and pricing, and pest encounters. As we identied suitable plantings, we identied a contrasting planting as physically close as possible. We then made multiple ant sampling efforts in those plantings for which we could obtain complete growing information. Our ndings support our overall hypothesis that large, monoculture cashew plantings do not automatically need regular, prophylactic, by-the-calendar chemical pesticide application provided certain ecologically important growing conditions are met. This paper summarizes our ndings from 1985 through 1996, and sets out recommendations for pesticide-free cashew growing from initial planting to mature trees. Potential use of ants in pest controlNumerous studies have shown that ants can interfere with herbivores (see, e.g., Brown, 1959a, b; Buckley, 1982; Beattie, 1985; Gotwald, 1986; Jolivet, 1986), and Bentley (1983) addressed the general context of ants as potential biocontrol agents in agriculture. Three studies deal expressly with the antplant components operating in cashew: Bentley (1977) using Bixa orellana in Costa Rica, Tilman (1978) on Prunus serotina in Michigan, and Inouye and Taylor (1979) on Helianthella quinquenervis in Colorado each described host plants possessing ant-attracting extraoral nectaries that show very specic temporal/tissue secretion patterns. These patterns attract and focus ants to areas susceptible to pest damage as varied as ower buds (Bixa), new leaves (Prunus), and immature seeds (Helianthella). The ability of ants to function as antiherbivore agents in a crop monoculture situation is documented in the well-known manipulation of Oecophylla in citrus and lychee orchards in China (Huang and Yang, 1987). The earliest record dates from 304 A.D., and the

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practice is ongoing today. Dutch Indonesian cacao plantations in the 1920s imported nests of the black cacao ant and its honeydew-producing coccids as an antipest agent (van der Meer Mohr, 1927), and Baker (1972) notes that the crazy ant, Anoplolepis gracilipes (Smith), is also manipulated as a cacao pest control agent in Papua New Guinea. In Cameroon, articial rafa nests are used to trap and transport Wasmannia auropuncta Roger to cacao plantations for the control of several insects (Bruneau de Mire, 1969). Recently, Peng, Christian, and Gibb (1995) reported that the presence of the weaver ant Oecophylla smaragdina is correlated with a reduction of Helopeltis in certain Australian cashew plantings. The suggestion from their work was that weavers might be manipulated to function in cashew pest control much like the Chinese have used weaver ants in citrus for 1500 yr. Majer and Delabie (1993) have correlated the presence of certain ant species with a corresponding reduction in various insect groups in Brazillian cacao plantations. Helopeltis spp. are also major pests of cashew in other Asian countries and east Africa (Hill, 1983) and we decided to restrict our attention to this pest when conditions of observation were limited. Helopeltis spp. is recorded as a common pest in all of our research sites (Stonedahl, 1991; Stonedahl, Malipatil, and Houston, 1995; local growers), and we found several individuals in each tree plot even during the off-season. The secreted nectar also attracts predatory and parasitic wasps, which, by their slow searching behavior, appear to hunt for prey within the tree space (Pemberton and Lee, 1996). ObjectivesOver the past 11-yr period, we have addressed ve questions centered on our initial hypotheses: (1) does cashew consistently attract ants as a natural aspect of its biology, and, if so, what anatomical, morphological, and behavioral characteristics are related to the ant association? (2) do these characteristics result in maintaining an ant guard during growth periods coincident with pest presence? (3) is there a demonstrable number of trees growing in close association above which pests pose a serious problem? (4) can evidence be found of variables in the cashew-growing environment that enhance or lessen the ants presence? and (5) do examples of large, protable, pesticide-free cashew plantations exist, and can models for enhancing ant involvement in cashew nut production be developed? MATERIALS AND METHODS
The locations of our study sites and details of each growing operation are given in the Appendix. In 1985 we sampled trees and ground-baited in the Calicut, Kerala, India area for 3 wk. Collections and observations within Sri Lanka were made during repeated visits to selected sites and trees, between November 1991 and July 1992, with a minimum of three visits made to each of 11 study sites. The 1992 collections in India consisted of 0.5 d at each site, collecting from trees only. We spent one complete day collecting from cashew trees and from the ground at the Agricultural University near Kuala Lumpur, Malaysia in 1992. The 1992 single collections in India and Malaysia were made on days with full sun and no rain. All examples from government and private estates represent efforts to sell cashew nuts for prot. Yield from these plantations was consid-

ered satisfactory and all growers were interested in pest protection and the costs of doing business. We identied cashew plantings that varied in insecticide usage, tree age, location, and understory habitat. From these plots we collected data on yield, cultural practices, production costs, and nal disposition of the nut crop. Precise tree age was available for plantings up to 12 yr, after which records were incomplete or missing. Our best estimate of a planting of large, mature trees was PANA #3, which was estimated at 2225 yr by the estate manager, although no individual had been at that location for that period of time. We therefore placed all large, mature trees into an arbitrary 25-yr category, which seemed reasonable considering similar height, spread, and trunk diameter characteristics. Further, all of the larger trees were producing well and their phenology was similar in opening a comparable amount of new leaves throughout the year. We surveyed ant species richness on trees and on the ground adjacent to trees using visual collection, beating sheets, and baiting with sh and honey as separate offerings. At each individual collection site (single tree or bait) we rst noted and collected all morphospecies present to establish a working list of species. Since the greatest diversity encountered was 12 species in 810 genera it was not difcult to quickly identify taxa to a 23 word code list for rapid estimation of individual species abundance. Random beating sheet samples were used to conrm the visual observations of ants present. A minimum of ve random trees within a single-age growing plot was then fully sampled to determine species richness for the plot as a whole. The number of trees sampled within a single age plot was expanded as time and multiple visits permitted, with all trees usually included in plots under 1.5 ha. The results of individual tree collections within each age plot were pooled to develop a list of ant species present within each separate tree plot. Estimates of ground ant diversity and abundance were made by continuously censusing a bait trapline, with individual bait stations 3 m apart, on a 20-min cycle until the bait was completely removed. When possible, we baited within the same collection of trees from which we sampled ants, allowing a day or two to elapse between collections so that removal of ants on one occasion would not impact the next sample. On each selected tree, we observed all/most branch sections, new leaf clusters, and inorescences, and noted both species richness and an estimate of abundance over some unit of time. Aspirating ant samples from cashew can be almost impossible for some species due to their wariness and quickness (Camponotus spp. and Tetraponera rufonigra) and offers no problem with other taxa (Oecophylla, Technomyrmex albipes, and small Tetraponera). Relying on visual abundance numbers obtained from a mixed population of 12 ant species will not provide the precise numbers obtained from pitfall traps used to census groundforaging ants. Bait placed on a tree only gave an indication of species dominance, rather than attracting all taxa to the site. If one were to rely on bait to census for all arboreal species, we estimate that 3050% of the taxa could be missed due to their exclusion from an area where large numbers of a dominant species have congregated at the bait excluding subordinate species. At the same time, all species coexist when the diffuse nectaries are the sole food source, or within a few hours of a bait being totally removed. For the above reasons we did not formally quantify ant abundance in this presentation, or derive the corresponding diversity and evenness indices. Sufce it to say that certain ant species are present as scattered, sometimes difcult to locate individuals, while others form loose columns as they move around a tree. Additionally, it seems that before information on ant abundance would be valuable in the context of pest control, one should know something of the effect of each species on some target pest species. For example, while 100 small Tetraponera sp 2. and Technomyrmex albipes were mixed foraging within a single cashew tree, one might nd only 46 individuals of the large, aggressive Tetraponera rufonigra present in a few trees, with their location shifting from day to day. Which ant is more, or less, effective in pest control and against what size pests? There is simply no way, at this time, to make a judgment on the efcacy in pest control as a correlation with ant species richness

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or general diversity. We did nd one example of a cluster of Monomorium sp. cutting up and removing the remains of a small lepidopteran larva. This report discusses ant diversity as a qualitative function of plant age, phenology, habitat heterogeneity, and pesticide usage. Judgments were made regarding plot habitat heterogeneity for both living plant material and debris such as dead wood and stones. We did not have time to perform a formal, line- or quadrat-based vegetation survey, and so used broad classications such as grasses, herbs, annual crop species, perennial crop species, and shrubs expressed as an estimated combined percent of ground cover. A judgment was also made as to the presence of a vegetational edge at the plot boundary which was more complex than the growing area. The edge could consist of woody secondary growth vegetation across a wire fence or small dirt road, or an adjacent untended grass/herb/shrub mix from some fairly recent clearing event. We traced two ant species (Camponotus sericeus at PANA #3 and Tetraponera rufonigra at INFO #3), which were foraging to cashew trees from across such an edge.

RESULTS AND DISCUSSION Ant attractionAnts are attracted to cashew trees by functioning extraoral nectaries on young leaves, the developing inorescence, and young fruits. Leaf nectaries secrete for 6 mo until the leaf becomes mature, while inorescence and fruit nectaries are active for a much shorter, but specic, period of time. There is no difference in nectary location or abundance associated with specic cashew varieties, and not a single tree was found during the past 11 yr that did not possess the extraoral nectaries. NectariesLeafLeaf nectaries are oblong shallow pits with an inner surface of papillate, glandular cells (Fig. 1). Nectaries are always associated with junctions of the midrib and rst-order veins on the abaxial (lower) surface (Fig. 2, along midrib), and 68 nectaries are found at the base of the blade on the adaxial (upper) surface (Fig. 4). Secretion begins when the leaf is only 10% of its nal size, and can be demonstrated by encasing a leaf within a plastic bag and noting the drop of nectar that collects on each nectary within 30 min. Nectaries on an upper leaf surface are very unusual; each cashew leaf develops a minimum of 3540 feeding sites. In 61% of the trees examined in this study (N 400 over all sites), nectaries also exist at the junctions of secondary and tertiary veins and even at higher order junctions (Fig. 2) over the abaxial lamina surface. These nectaries and their secreting papillate surface are smaller than those nectaries associated with the midrib, but even the smallest attracts ants. Leaves with a full complement of nectaries will possess a total of 225 (150300) antfeeding locations per leaf depending on mature leaf size. At 10 yr, a 3-m tree with one-third of its branches in leaf ush (six leaves per ush, 25 ushes per tree) will possess 35 000 total leaf nectaries, and this condition can be found throughout the year due to intermediate leaf production. A far greater number of active nectaries exists at the height of new leaf production (see Phenology, below). InorescenceAn inorescence develops from the axillary bud of a leaf-like bract, and during its development and elongation it lies at near the bract adaxial surface (Fig. 3). Although lacking active nectaries, the develop-

ing ower system, by its proximate position to the bract surface, is visited by ants foraging for nectar from the adaxial bract nectaries and consequently moving over and around the developing oral system (Fig. 4). Twenty-four hours before the rst owers open, the ower stalk rises through 45 , lifting it from the bract surface and making the terminal owers readily available to pollinators. As the inorescence elevates from the bract surface, secretion begins from nonstructured sites at the axil of each branching site of the ower stalk system, and at the abaxial base of each bract that subtends a ower bud (Fig. 5). Finally, secretion occurs at the base of each ower bud. When an inorescence elevates and has both open and closed owers, there are a constant 68 nectary sites functioning, which attract ants to patrol the total ower system (Fig. 6). Whereas the leaf and inorescence bract nectaries are morphologically differentiated pit-like structures with secretory cells, nectaries on the inorescence stalk system and on the owers are nonstructured. That is, secretion takes place at a precise location, although there is no external or internal anatomical structure associated with the event. However, there are open stomata located at each of the ant feeding locations. FruitThere is one stage of fruit development where ants (Camponotus or Oecophylla at our locations) are attracted to a specic region of the developing nut (Fig. 7). We call this the one-half grown nut stage because this represents an approximate visual development stage of the fruit at which feeding occurs. Ants congregate on the inside of the curve, which mirrors the nal cashew nut shape, and visual inspection shows the ants to remain for varying times with their mouth on or near the fruit surface and then to leave and move off the ower/fruit system and down the tree. The feeding site has a rough darkened appearance when compared with the smooth green surface of the remainder of the nut. If ants are removed from the area and the nuts encased within a plastic bag, a uid collects at the site within 30 min. Scanning electron microscopy revels pores with a secretion (Fig. 8), and microscopic sections show these pores to be stomata with an opaque material both within the substomatal area and on the outside surface of the nut. Subsequent to this nut development stage, secretion stops, the nut surface becomes a gray color, and the epidermal cell walls become highly lignied. Ants may forage over, but do not target the nut after secretion stops. Ant movementWe followed individual ants on a tree to judge foraging patterns associated with nectary placement, and we followed the reciprocal event of observing individual nectaries to judge how frequently a single nectary can be revisited. Over 200 observations yielded the following ndings: (1) ants visit 710 nectaries on each trip to a tree usually all within a single cluster of new leaves and/or inorescence, (2) the visit to each leaf nectary lasts 4.7 s, although all times depend on how much time has elapsed since the previous ants visit, (3) visits to the nonstructural inorescence nectaries average 7.8 s, but duration is also dependent on time since the last visitor to the area. A single nectary can be visited by a succession of ants

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Figs. 16. Nectary location. 1. Scanning electron micrograph of a cashew leaf nectary located along the midrib. Note the pit-shaped morphology and individual papillate secretory cells. Bar 0.25 mm. 2. Photocopy of a typical abaxial (lower) leaf surface from a phenotype having nectaries associated with the midrib and most lateral veins. Each black dot represents one of 274 individual nectaries, each of which has a structure identical to that shown in Fig. 1. 3. Developing inorescence (photographed from above) illustrating how the structure closely parallels and lies at against the subtending adaxial bract surface. 4. Camponotus feeding at a nectary on the adaxial inorescence bract surface. 5. Camponotus feeding at a nectary at the base of a bract subtending a group of unopened ower buds. 6. Ant feeding at the base of an unopened ower on an inorescence that has fully open owers standing for pollination. Arrow points to a ower at full anthesis.

each staying for 1 s, the ants then continuing to forage on the leaf surface until a nectary having a collectable amount of nectar is found. Movable feastCashew belongs to a group of plants known for providing a movable feast (Tilman, 1978; Fiala and Maschwitz, 1992) as foraging ants are led around the plant by both temporal and spatial functioning of extraoral nectaries, thereby focusing ants at

sites most susceptible to herbivory. During the course of a complete growing season, the order of ant attraction in cashew is: (1) nectaries on both surfaces of new leaves, (2) nectaries on leaf-like bracts subtending developing inorescences, (3) secretion from axis junctions on the inorescences, (4) secretion from the sepal base of each ower, and (5) secretion from stomata at the inside curve of the developing nut at the one-half grown stage.

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Figs. 78. Nut at the one-half grown stage. 7. One-half grown nut stage with ants feeding at a site of open stomata. 8. Scanning electron micrograph of the one-half grown nut stage showing one open stoma and presumptive secreted material on the nut surface. Area collected after ant exclusion for 30 min.

PhenologyIn addition to the main leaf/ower/fruit production period, a secondary leang occurs continuously throughout the year, even during extremely dry conditions (Sri Lanka in 19911992 experienced a 100yr drought and 99 % of trees continuously produced new leaves). This secondary leaf production insures ant attraction and dispersal over the entire tree throughout the year. The nectar functions as a food source for the ants during the dry season when food, in general, is low (Levings, 1983). There is little evidence that mature cashew foliage is attacked by herbivores in general, or by Helopeltis in particular, during the dry season, therefore we see the new leaf production throughout the year acting primarily as a food source for local ants, especially Oecophylla, which nests within the trees. All nectar secretion from cashews extraoral nectaries is conned to the usual targets for herbivory, e.g., new leaves, inorescences, and developing fruits. Cashew extraoral nectaries also attract a variety of spiders and wasps throughout the year. Of all cashew trees we have observed over the 11-yr period, only three (one in Kerala, India, and two in Sri Lanka) were completely lacking new leaves during our visits. These trees possessed only one or two individual foraging ants, while adjacent partially leang trees possessed a full complement of ant species. We found no indication of a saturation effect of too many trees in an area possessing too few ants to cover available trees. Every tree in a typical 23 ha planting block will have a common complement of ants visiting its new leaves. Tree architectureThe architecture of maturing cashew trees affects the number of shoot tips (the number of potential ushes of new leaves), which in turn relates to the actual number of nectaries on a plant. A new plant propagated by air layering is rather unbranched, mimicking the end of the single shoot that it represents, while a seedling of the same length is slightly more branched. A new plant produced either from cuttings or seeds initially has a pronounced upward growth form, with some, but not excessive, side branching for the rst 14 yr. At 3 4 yr, or when the plant reaches 1.52.0 m height, secondorder branching increases from existing laterals and cashew takes on its usual pyramidal wide as is tall habit. This growth form is only seen in untrimmed plants where the lowermost branches are not removed. Certain growers

trim the lower branches, even from young trees, to facilitate later ground harvesting of the fruit. We point these architectural and maintenance features out because if the plants are left uncut for their early years, the extra, lower branches provide an additional source of ant-attracting leaf nectaries. Ant diversity vs. age of tree and habitat heterogeneityTable 1 summarizes characteristics of each sampling site arranged by increasing tree age. Age establishes a directional criterion that relates to, and predicts, tree size and architecture, which, in turn, relate to available antfeeding sites. The youngest sites changed somewhat during the year as the interplanted crops matured and the cover vegetation became more complex, but we found no changes in ant species richness where we made repeated sampling trips over the year. Table 2 lists the 43 arboreal ant species in 17 genera collected from cashew during this study. Four species, Cataulacus taprobanae, C. n. sp., Lepisiota, and Diacamma, were collected only once during this study, and probably represent general foraging individuals rather than ants that were targeting cashew extraoral nectaries. All other ants were a regular part of a species mix common to trees in the same growing plot. Refer to Tables 37 for a list of ant species associated with each site. Fig. 9 is a plot of ant species collected from knownage trees at each study location. The trend line for species number indicates the increase in species richness for increasing tree age, but the R2 indicates the amount of variation across the sites is high. Part of the variation among similar-age plots relates to pesticide use and/or habitat modication, which will be discussed later. Species richness data are from pooled collections over the total planting so there is no variation description for trees within a site. Each age class and obvious deviations from the trend will be discussed under separate headings below. The data show a general increase in ant species richness over increasing age and size of trees over all sampling sites. Confounding a simple correlation with tree age are corresponding changes in habitat heterogeneity accompanying increase in tree age, up to canopy closure. At canopy closure, ground vegetation decreases at the same time that the trees are reaching their large mature size, thereby providing the maximum number of extrao-

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TABLE 1. Site reference, plot size, tree age, species richness, and brief habitat description for the 16 research sites used in this study. Sri Lanka PANA, INFO, SLCCW, SLCCE, PUSH; India CALI, KOTTA, DIST; Malaysia MALAY.
No. ant Tree age spe(yr) cies

Site ID

Area (ha)

Site features

PANA #1 INFO #1 INFO #2 INFO #3 INFO #4 PANA #2 CALI #1 SLCCW #1 MALAY #1 PUSH #1 SLCCE #1 SLCCW #2 PANA #3 KOTTA #1 DIST #1 MALAY #2

10 0.5 1 2 0.5 4 1.5 20 2 2.5 4.5 15 12 10 3 2

1.5 2 4 7 7 7 8 11 11 25 25 25 25 25 25 25

2 3 7 9 2 8 5 5 11 12 8 11 8 6 12 12

Unsprayed; 80% bare soil; bananas and melons; no edge effect. Unsprayed; 50% bare soil; new coconuts and chilies; straw around coconuts; one side edge effect. Unsprayed; 100% grass cover; one side edge effect. Unsprayed; 10% bare soil; bananas, pineapple, grass, and herbs; teak at edge. Sprayed; 100% bare soil with weeding; heavy pesticide use; demonstration plot. Unsprayed; 5% bare soil; thick grass cover with few herbs; no edge effect. Unsprayed; 25% bare soil on hard basalt; thin grass cover; no edge effect. Sprayed; 50% bare soil; slight grass cover; some eld cleaning. Unsprayed; 100% thick grass cover; two sides edge effect. Unsprayed; 25% bare soil; thin grass with herbs and small shrubs; closed canopy; two side edge effect. Sprayed; 25% bare, this soil on exposed granite; thin grass with herbs; woody debris; open canopy; hot, exposed site; no edge effect. Unsprayed; 5% bare soil; thick grass with herbs, shrubs, woody debris, stones; open canopy. Unsprayed; 50% bare soil; thin grass with herbs; closed canopy; two sides edge effect. Sprayed; 30% bare soil; thin grass with herbs; semiclosed canopy; two sides edge effect. Sprayed; 10% bare soil; grass, herbs; woody debris; stones; 80% closed canopy; two side edge effect. Unsprayed; 15% bare soil; sand base; grass, herbs, woody debris; closed canopy; three sides edge effect.

ral nectaries for foraging ants. In addition to tree size and habitat vegetation, our ndings suggest that both management techniques and pesticide use also affect the overall relationship between cashew and ants. Before we discuss data relating to ant species richness, we must comment on two caveats relating to landmass and its effect on species number. Numerous studies involving both true and habitat islands have established the validity of a positive speciesarea relationship. Therefore, even if the impossible condition of comparing number of ant species among identical cashew habitats were achieved in this study, one could still expect more ant taxa per unit area in India and Malaysia than in Sri Lanka. In addition to the area consideration, Vandermeer (1995) has re-emphasized the impossibility of two eld plots being truly identical and suggests that all we can hope for is some acceptable level of similarity between study locations. We have paired our sprayed and unsprayed plots within 35 km distance of each other separated by 150 km across Sri Lanka, while our two Indian sites are 10 km apart out of a 900-km band of cashew growing along the length of Karala. Trying to argue for identical comparative research locations can lead to reports full of qualifying statements when discussing results (van der Werf, 1993). New plantingsTrees planted from either seed or airlayered stock, usually 0.51.0 m tall, will attract at least one and often two or three ant species (Table 3). All of our sampling sites were interplanted, and the more ecologically complex (INFO #1) had the greatest number of ant taxa and abundance. Hand pesticide applications to the interplanted chilies at this planting had no effect on the ability of ants to nd and occupy the young cashew plants. Straw piled around the base of interplanted coconut seedlings encouraged Camponotus and Crematogaster to nest within the plots. However, even this small effort is not absolutely necessary for ants to be present, as Technomyrmex albipes nested under very harsh conditions of bare soil directly under young plants at Panadura Estate (PANA #1; Fig. 10).

Three to twenty yearsThere appears to be a critical period with respect to ant diversity between the 2- and 4-yr period of a new planting. After the second year, a dense grass and herb layer begins to regrow in the planting area. Annual crops are not replanted, and the original biennial bananas are represented by a few scattered plants that have regrown naturally. From year 2 onward, the environment becomes increasingly complex as natural vegetation returns to the area. This assumes that a concerted weeding effort, which is rare, does not occur. During these early years a cashew trees architecture changes from essentially upward growth to a more spreading form through lateral branch development. The combination of increased habitat complexity and increasing extraoral nectary numbers, due to greater tree branching, leads to increased ant species diversity both within the habitat and on the trees (Tables 45). The effects of management techniques on ant species richness can be demonstrated by the four 78 yr old plantings (Table 5) in this study. Trees at INFO #3, in the eastern part of Sri Lanka, were part of a complex interplanting and possessed a mix of nine ant species. The species included several taxa that were present as foraging columns of several hundred individuals. At PANA #2, in western Sri Lanka, the trees were similar in height, but have had some lower branches removed in anticipation of commercial harvesting. The trees were growing in a thick mix of grass and herbs and possessed eight ant species, but only a Crematogaster was present in high individual numbers. Two trees at Calicut, India (CALI #1) were growing in a cut grass area, a lawn, isolated from any complex habitat. Additionally, the soil was very compact ow basalt. Five ants visited these trees and the ant complex remained constant in species mix and abundance over a 3-wk period. We found our most seriously disrupted planting of any age at the 78 yr stage at Informatics (Table 5, INFO #4). A 0.5-ha block of trees adjacent to the plantation entrance and seedling nursery was used as a demonstration planting for investors. The trees received regular and thorough soil-level weed-

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Myrmicinae Cardiocondyla ?nuda Cardiocondyla sp. 1 Cataulacus taprobanae Cataulacus n. sp. Crematogaster sp. 1 Crematogaster sp. 2 Crematogaster sp. 3 Crematogaster sp. 4 Crematogaster sp. 5 Crematogaster sp. 6 Monomorium latinode Monomorium sp. 1 Monomorium sp. 2 Monomorium sp. 3 Pleidole sp. 1 Ponerinae Diacamma sp. 1 Tetraponera aitkeni Tetraponera difcilis Tetraponera rufonigra Tetraponera sp. 1 Tetraponera sp. 2 Tetraponera sp. 3 Tetraponera sp. 4

Dolichoderinae Dolichoderus (thoracicus gp.) Tapinoma indicum Tapinoma melanocephalum Technomyrmex albipes Formicinae Anoplolepis gracilipes Camponotus sericeus Camponotus sp. 1 Camponotus sp. 2 Camponotus sp. 3 Camponotus sp. 4 Camponotus sp. 5 Camponotus sp. 6 Lepisiota sp. 1 Oecophylla smaragdina Paratrechina longicornis Paratrechina sp. 1 Plagiolepis sp. 1 Polyrhachis thrinax Polyrhachis sp. 1 Polyrhachis sp. 2

ing and vegetation removal, and super-regular insecticide application. These trees were visited by only small numbers of two ant species and had been damaged severely by Helopeltis the previous year, showing 70% shoot tip death. Younger (4 yr), smaller trees, with a much smaller number of nectaries, located 200 m distant but unsprayed and with a dense grass ground cover (Table 4), possessed seven ant species and were not affected by Helopeltis. However, no ant species on these smaller trees was present in large numbers of individuals. From the age of 5 or 6 yr onward, to large mature trees, we found that understory complexity may contribute to ant diversity and abundance on a tree. If the understory is cleared to some degree, where shrubs and larger biennials are removed, and grass and small herbs remain as the understory, the number of ant species reached eight species on individual cashew trees (Table 5, PANA #2) with small numbers of each species present, whereas on similar size/age trees growing in a very complex habitat, the number of ant species was nine (Table 5, INFO #3), but the total number of ants present on any tree was 2.53 times that at Panadura. This relationship between ant species richness and abundance persists through large mature trees such as those at the Kottarakara Seed Farm, Kerala, India (Table 7, KOTTA #1) where the trees are large, but the understory is very orTABLE 3. Ant diversity observed on 1- and 2-yr-old cashew trees.
Location Species

derly, and the trees contained six ant species. At the District Farm only 10 km away, 12 ant taxa were collected from similar-aged trees growing in a more complex habitat (Table 7, DIST #1). The young trees in Malaysia, growing with a simple but very dense grass understory, and a possible edge effect on all sides, possessed 11 ant species (Fig. 11) (Table 6, MALAY #1). We also note that it is not absolutely necessary to allow vegetation to grow directly to the tree trunk to encourage ants (Fig. 12). Growers may wish to partly clean the area directly under a tree of larger vegetation to facilitate harvesting fruit from the ground or for general estate appearance. This type of rough clearing does not completely remove grasses, and herbs and ants will readily cross such a clearing, from a more complex habitat, to reach the tree. Two tree plots in western Sri Lanka (Table 5, PANA #2; and Table 7, PUSH #1) provide evidence of ants crossing fairly bare ground to access trees. Mature treesThe irregularly sprayed mature trees at SLCCW #2 (Fig. 13) and the nonsprayed trees at MALAY #2 (Fig. 14) were growing in the most complex habitat encountered in our study, with no under-tree clearing of any type and gaps created by missing trees allowTABLE 4. Ant diversity observed on 4-yr-old cashew trees.
Location Species

Informatics, eastern Sri Lanka. INFO #2

Panadura, western Sri Lanka. PANA #1 Informatics, eastern Sri Lanka. INFO #1

Paratrechina longicornis Technomyrmex albipes Camponotus sp. 1 Crematogaster sp. 1 Technomyrmex albipes

Anoplolepis gracilipes Camponotus sericeus Camponotus sp. 1 Crematogaster sp. 1 Monomorium latinode Paratrechina longicornis Tapinoma indicum

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Ant diversity observed on 78-yr-old cashew trees.

Location Species

TABLE 7.

Ant diversity observed on 25-yr-old cashew trees.

Location Species

Informatics, eastern Sri Lanka. INFO #3

Informatics, eastern Sri Lanka. INFO #4 Panadura, western Sri Lanka. PANA #2

Calicut, India. CALI #1

Anoplolepis gracilipes Camponotus sericeus Camponotus sp. 1 Camponotus sp. 2 Crematogaster sp. 2 Monomorium latinode Paratrechina longicornis Tapinoma indicum Tetraponera rufonigra Camponotus sericeus Monomorium latinode Camponotus sericeus Cardiocondyla sp. Monomorium sp. 1 Oecophylla smaragdina Paratrechina longicornis Polyrhachis sp. 1 Technomyrmex albipes Tetraponera sp. 2 Anoplolepis gracilipes Camponotus sp. 3 Crematogaster sp. 3 Tetraponera aitkeni Tetraponera difcilis

Pushparanghnam Estate, western Sri Lanka. PUSH #1

Sri Lanka Cashew Corporation-East, eastern Sri Lanka. SLCCE #1

Sri Lanka Cashew Corporation-West, western Sri Lanka. SLCCW #2

ing for a mixed ground vegetation. These trees attracted the greatest diversity of ant taxa, 11 and 12 species, respectively, each with three or four species present in 100 individuals per tree. A plot of mature, unsprayed trees in western Sri Lanka (Table 7, PANA #3; Fig. 15), 5 km from SLCCW, with a completely closed canopy and sparse grass understory, yielded eight ant species, including the most healthy and widespread colonies of treenesting Oecophylla smaragdina encountered. The irregularly sprayed SLCCW trees, in contrast, possessed only a few small colonies of O. smaragdina. In each location used for this study, especially when a complex vegetation edge was present, there were groundforaging ant species that were collected from close to the trees, but never within a tree. Pachycondyla, Aphaenogaster, and Odontoponera recruit to sh bait in large numbers ( 200 individuals), even within 1 m of a cashew trunk, but never appeared in tree samples.
TABLE 6. Ant diversity observed on 1012-yr-old cashew trees.
Location Species

Panadura Estate, western Sri Lanka. PANA #3

Kottarakara, Kerala, India. KOTTA #1

District Farm, Kerala, India. DIST #1

Sri Lanka Cashew Corporation-West, western Sri Lanka. SLCCW #1

Agricultural University, Malaysia. MALAY #1

Camponotus sp. 2 Cataulacus taprobanae Paratrechina longicornis Polyrhachis sp. 1 Tetraponera sp. 2 Anoplolepis gracilipes Camponotus sp. 4 Crematogaster sp. 4 Crematogaster sp. 5 Diacamma sp. 1 Paratrechina longicornis Paratrechina sp. 1 Polyrhachis sp. 2 Technomyrmex albipes Tetraponera rufonigra Tetraponera sp. 1

Agricultural University, Malaysia. MALAY #2

Camponotus sericeus Camponotus sp. 2 Crematogaster sp. 1 Crematogaster sp. 3 Lepisiota sp. Oecophylla smaragdina Paratrechina longicornis Plagiolepis sp. Polyrhachis sp. 1 Technomyrmex albipes Tetraponera rufonigra Tetraponera sp. 3 Anoplolepis gracilipes Camponotus sericeus Camponotus sp. 1 Crematogaster sp. 2 Monomorium sp. 2 Paratrechina longicornis Tapinoma indicum Technomyrmex albipes Camponotus sericeus Camponotus sp. 2 Cataulacus taprobanae Crematogaster sp. 3 Oecophylla smaragdina Paratrechina longicornis Polyrhachis sp. 1 Technomyrmex albipes Tetraponera rufonigra Tetraponera sp. 3 Tetraponera sp. 4 Camponotus sericeus Crematogaster sp. 3 Oecophylla smaragdina Paratrechina longicornis Pheidole sp. Polyrhachis sp. 1 Technomyrmex albipes Tetraponera sp. 2 Anoplolepis gracilipes Camponotus sericeus Camponotus sp. 5 Crematogaster sp. 6 Monomorium latinode Oecophylla smaragdina Anoplolepis gracilipes Camponotus sp. 5 Camponotus sp. 6 Cardiocondyla prob. nuda Cataulacus n. sp. Crematogaster sp. 1 Crematogaster sp. 2 Dolichoderus (thoracicus gp.) Paratrechina longicornis Pheidole sp. Plagiolepis sp. Polyrhachis thrinax Camponotus sp. 1 Camponotus sp. 4 Cardiocondyla sp. Crematogaster sp. 4 Monomorium sp. 3 Paratrechina longicornis Paratrechina sp. 1 Tapinoma melanocephalum Techomyrmex albipes Tetraponera rufonigra Tetraponera sp. 1 Tetraponera sp. 2

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Fig. 9. Plot of number of ant species collected (bars) on variousage cashew trees (line) across all sites used in this study. The regression line uses ant species as the dependent variable, and all sites were included in its calculation. Sites ordered by ascending age.

It seems noteworthy that there was a maximum of 12 ant species present in a single tree and that this number occurred in all three countries visited (Table 7, PANA #1, DIST #1, MALAY #2). At this number the actual species mix varied so any species presence or absence was not imposed by some dominant species. The three 25-yr tree plots with the least number of species present (SLCCE #1, PANA #1, KOTTA #1) had less diverse growing habitats due to a modicum of farm management at each site. Other arthropodsWe have concentrated on ants in this study, but probably encountered as many spider species as ants in the cashew trees. Small members of the families Lycosidae (wolf spiders) and Salticidae (jumping spiders), are difcult to nd visually, but appear in almost every sample taken with a beating sheet. It was common to nd 1012 individuals of 34 different species in a single beating sample. In addition to spiders, various wasps were often observed ying slowly within the trees branch system, and were occasionally seen feeding at the nectaries. Of course both spiders and wasps will take ants as prey, and presumably do so in this tree ecosystem, but their role as general predators of pests is well known (Bishop and Riechert, 1990; Kromp and Steinberger, 1992; Carter and Rypstra, 1995; Frank and Nentwig, 1995). One other group of arthropods, mites, can play a meaningful role in agricultural pest suppression (Kostiainen and Hoy, 1996). Mites were a nonfactor in our studies despite the numerous nectar sources on cashew. We suspect that the constant activity of ants at cashews nectaries keeps mites out of the system. Both Tapinoma and Technomyrmex are in the size range to consume mites if they are a part of their diet. Mites are not considered cashew pests in southeast Asia. Ant-nesting habitatOnly Oecophylla smaragdina nests on cashew trees, with all other ant species moving through the surrounding habitat to access the trunk. We found ants that can nest in bare soil next to the tree base, i.e., Technomyrmex albipes and Camponotus, and others that appear to require a more complex or less disturbed

habitat for nest sites, i.e., Crematogaster spp. and Polyrhachis using carton nests in nearby vegetation or accessing nearby arboreal locations. Possible within-plot habitat heterogeneity includes grasses, herbs, shrubs, small trees, stones, and woody debris of various sizes. All of these items when found within the growing plot provide potential nesting cover for ants that visit the trees. It should be remembered that we also found several ant taxa that live, and forage, within the growing site but do not move up the trees. Local ants that nest off the tree can be followed as they move to the trunk and then fan out to new leaves. For most of the ant species we observed, their foraging path was directed to new leaves and inorescences as opposed to a pathway where the ant might ascend a tree and randomly move about the stem and leaf system. With numerous ant taxa present on a single tree, one might hypothesize many antagonistic encounters between species. However, the opposite situation was far more common with different taxa passing closely while showing no interest in each other. We did observe the usual subordinate behavior of Camponotus (Andersen and Majer, 1991) causing it to be displaced from feeding at nectaries by the immediate presence of any other ant, and Oecophylla in Sri Lanka regularly stops and bites at one of the smaller Tetraponera, which, in turn, pulls itself close to the plant surface. However, this interaction is momentary with both ants continuing to forage after the encounter. It also appears that some species have identiable, more random foraging patterns, so that a tree is thoroughly searched even though the nectaries are in predictable, and perhaps previously visited, locations. For example, Tetraponera spp. and Camponotus spp. do considerable probing of bark ssures and general surface wandering even though both ultimately spend time ingesting liquid from nectaries. Conversely, Technomyrmex albipes, Anoplolepis gracilipes, and Paratrechina longicornis, which are strong searchers and recruiters, form almost single-line columns leading to clusters of new leaves. The presence of multiple ant taxa that travel some distance to access target trees suggests the need for a diverse habitat if these ants are to be encouraged. Some habitat management such as not weeding invasive grasses, herbs, and shrubs is passive, while placing at stones within the plot would require a minimum of effort. Controlling the amount of woody debris within a plot is problematical given that local villagers often harvest fallen branches and even twigs for fuelwood. However, any such debris will contribute to the desired habitat diversity. Even a sparse, interplanted crop has the effect of encouraging ants from weedy eld edges to intrude into the plantings and forage on cashew plants. Technomyrmex albipes, conversely, will establish a small nest in completely bare, lateritic soil at the base of a newly planted 0.5-m cashew and forage directly to and from the plant. Our data are not sufcient to dissect out whether the increase in ant taxa recorded with increasing plant age/ size is due to the increasing number of nectaries available (increased number of new leaves related to plant size), increasing plant foraging surface (allowing antagonistic ant species to avoid each other), or to the increasing area heterogeneity with planting age (natural accumulation of

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Figs. 1015. Cashew-growing sites. 10. First-year interplanting of cashew and bananas. Note the stark growing conditions, yet Technomyrmex albipes or Paratrechina longicornis was associated with 50% of the cashew plants. Arrow indicates cashew plant. 11. Young trees in Malaysia growing with a fairly homogeneous, dense, grass understory. These trees produced 11 ant species during 4 h of collecting. 12. Young tree at Panadura Estate with a basal area of soil cleared to facilitate nut harvest. Eight ant species crossed the bare soil to access the trees. 13. Mature cashew trees at SLCCW, growing with an open canopy, other tree species, and a very heterogeneous ground cover, including grasses, herbs, shrubs, dead woody debris, and stones of various size. Eleven ant species were collected from these trees. 14. Trees at Malaysia Agriculture University. The area has a nearly closed canopy with a grass/herb understory and numerous pieces of woody debris. Twelve ant species were collected from these trees in 4 h. 15. Panadura Estate mature trees originally interplanted with coconut, which is still present. The canopy is closed and a sparse ground cover of grass is all that is allowed to grow under the trees. Eight ant species are present on the trees; compare this growing habitat with Figs. 13 and 14 for contrast in habitats encountered among unsprayed, successful plantings.

understory vegetation and debris). However, regarding the last point, we found that habitat heterogeneity usually begins with simple denuded soil, increases in complexity through interplanting followed by grasses, herbs and shrub invasion, and then decreases appreciably following mature tree canopy closure. Throughout this period the number of ant taxa found on trees continues to show an upward trend. The absolute ant species richness seems decoupled from habitat, and follows the steady increase in plant size. We found a great amount of variation in ground cover for a given age class of trees, with the least amount of cover being in those intensive plantings where a crop of annuals and biennials had been planted and the area manually weeded for 2 yr (Table 1). Conversely, if there was no accompanying interplanting, the widely

spaced cashew were placed within a small circle ( 1.5 m) of roughly cleared ground with the original intervening habitat of grass, herbs, woody shrubs, dead wood, and stones intact. This latter condition offers an innitely more equitable home for resident ants and potential cashew foragers. If the original plantings are not highly maintained, trees die and gaps exist in the mature groves, resulting in a weedy vegetation including shrubs and woody debris (Figs. 13, 14). Ants as a problemSome people in agricultural occupations, even those in university experiment station environments, consider any ant on a crop plant potentially dangerous because of their often seen ability to tend coccids or aphids. However, the ants that we found on hun-

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dreds of Southeast Asian cashew trees do not normally tend coccids or aphids. We found one instance each of Oecophylla, and Camponotus tending aphids on developing fruit, and one group of T. albipes were tending a few coccids on one new leaf ush. These were isolated examples, and we did not see tending on trees that had a healthy mixed population of ant species. We suspect that with up to 12 taxa of ants simultaneously present and foraging in a dispersed manner on a single tree, competition for prey is too strong to allow for potential food items to be protected by their hosts in the way one ant species can surround and dominate a single bait. Ants on cashew present no special problems to the tree and also pose no problems for eld workers as the fruiting unit is collected from the ground. Even the aggressive weaver ant, Oecophylla, is harmless, with bare-legged children often playing in trees possessing this ant. Ant diversity over timeIn the 3 wk we sampled from Kerala trees, and the 9 mo of repeated sampling in Sri Lanka, we found almost no change in ant species composition. Due to uncertainties of scheduling and transportation, we tried to make our initial sampling efforts as complete as possible, often spending 1 h on a single mature tree. Part of this extended time period was to familiarize ourselves with the ant taxa present so that we did not have to make actual ant collections once diversity was known, and part because we did not want to overlook small species. As a result of the intense rst effort and as a function of the stability of the ant diversity across seasons (in Sri Lanka), we added only two species to initial lists after the rst collections. Additionally, no ant species dropped from the sample except for the four species found only as single collections, and during weather conditions such as cloudiness or actual rain during which ant diversity always decreased. Our one example of a predictable ant diversity change is the case of Tapinoma indicum only being found entering fully open owers on trees in eastern Sri Lanka. This ant was not collected from vegetative trees, but was always found on owering individuals. RECOMMENDATIONS We present positive data to answer our objective questions 1 and 2 that ants are a natural part of cashews biology, probably throughout the world. A system of continuous leaf and extraoral nectary production throughout the year maintains a perennial, multispecies ant association in all locations known to us. We also found evidence of a detrimental effect of pesticides (objective question 3) by lowering ant diversity, however the effect does not seem devastating and the ant populations rebound during the nonmajor leaf, ower, and fruit production times of year when spraying does not occur. During early years of tree growth, any heterogeneous habitat augmentation encourages ant diversity, however ant numbers remain high in mature plantations even if the habitat becomes less heterogeneous through canopy shading or general clean-up of debris (objective question 4). Finally, answering objective question 5, we found pesticide-free plantations of 100200 ha in size in Sri Lanka that have

experienced no signicant pest problems for years and use no pesticides. The Indian and Brazilian government recommendation that continual spraying is absolutely necessary is open to question in light of the examples we report. Some type of pest scouting IPM (integrated pest management) system (Price and Waldbauer, 1994), augmented by selective, very localized pesticide application, would work perfectly with naturally ant-occupied cashew trees. We suggest that the trend line for ant species diversity in Fig. 9 can be used as a predictor for the number of ant species present in cashew trees of various ages in most farm habitats, and that this number provides an indication of the level of potential pest protection present in the system. Figure 9 also shows how perturbations of pesticide use or habitat modication that reduce complexity can negatively affect the ant relationship (McLaughlin and Mineau, 1995). Pesticide spraying can now be seen in light of the general ant populations found on cashew trees throughout the year. Our study of cashew indicates that only Oecophylla smaragdina nests within the tree, with all other ants using the trunk or bridging vegetation to access a plant. Oecophylla will leave a tree and forage at ground bait, whereas without an added food source we did not nd this ant out of the upper portion of a tree. Clearly Oecophylla, nesting within the trees, should, and seems to be, the most impacted by any pesticide used, as we found consistently fewer Oecophylla in sprayed plantations. We need a critical demographic analysis of the direct effect of spraying on Oecophylla during the primary leang, owering, and fruiting season, as the work of Peng, Christian, and Gibb (1995) indicates the potential importance of this ant in cashew pest abatement in Australia. Our counts of the numerous ant taxa in trees at Kottarakara and the District Farm in Kerala, India, which are sprayed, demonstrate the potential of off-tree nesting ants to re-establish their presence following cessation or lessening of a regular spraying program. In contrast with tree-nesting Oecophylla, ant species that nest away from cashew trees seem very resilient after pesticide spraying, except where usage is very heavy (INFO #4). Our study did not address the effects of pesticides used during the owering period on pollinators or pollination success. Sufce it to say that an insecticide application during owering, as a prophylactic against Helopeltis, should affect insect mediated pollination in a negative way (Freitas and Paxton, 1996). A particularly detrimental effect must occur to honey bees when a Sevin-based (carbaryl) pesticide is applied directly to owers, a common procedure in many Southeast Asian cashew plantations. Three small ants (Crematogaster sp., Monomorium latinode, and Tapinoma indicum) regularly enter open owers (and move primarily from ower to ower) and could prey on ower thrips or mites. These ants occur on fully producing trees, and so do not appear to interfere with pollinators. We did not survey for the total suite of potential soillevel pest predators. Along with the noted ant species that forage only at ground level, we presume that members of the beetle families Carabidae and Staphylinidae con-

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tribute to a ground-level cadre of potential pest predators (see Perfecto and Vandermeer [1994] and Perfecto and Snelling [1995] for studies on a ground ant fauna associated with coffee). Pillai, Dubey, and Singh (1976) in discussing general pests of cashew in India note leaf miners, webbers, and defoliators, and several cashew apple and nut borers, all of which pupate in the soil and would be susceptible to terrestrial arthropod predation. Any question of the effectiveness of a pest abatement program (or lack of one) should contain some estimate of a crop economic damage threshold (Dent, 1991). Some unsprayed cashew in our study did show a variety of leaf damage caused by thrips, leaf miners, and assorted herbivores, but sprayed plantings also show this general damage. Each minor pest needs quantication to determine its actual level of occurrence and importance, however we found all growers and eld managers willing to accept some background damage, and to be mainly worried about Helopeltis and to a slightly lesser degree the stem borer Rhytidogera simulans White (Coleoptera: Cerambycidae), which can be manually removed by farm workers. If a prophylactic spray schedule is currently in use, especially a heavy three application per season regime, we would suggest a gradual cessation of the spraying program, beginning with elimination of the application during owering. Although Helopeltis can kill 80% of a trees current vegetative growth, the extent of an outbreak is usually patchy, and a pest scouting and tree-by-tree spraying program could be implemented if an outbreak of Helopeltis is detected. This approach would demand an IPM program of attention to small outbreaks by staff trained to spot trouble situations, and then pesticide use for this outbreak area only (Pimentel, 1986; Vandermeer and Andow, 1986; Greathead, 1995). One of our purposes throughout this effort has been to nd evidence that a diverse assemblage of natural predators can replace chemical pesticides, thereby saving money for cashew producers of all sizes (Risch, Andow, and Altieri, 1983). We studied only natural anttree interactions, as opposed to any form of cost-requiring intervention, such as moving ant colonies into a planting. On a pure cost basis, the plantings at Pushparhanangian, Informatics, and Panadura estates in Sri Lanka, and the Malaysian plantings, document that a pesticide-free, income-producing crop can be successfully grown within areas where government agriculturists consider pesticides an absolute necessity. We suggest that a gradual cessation of pesticide application, perhaps over several years, and coupled with increased habitat diversication, will be effective in encouraging ants to enter a cashew planting. The spraying during owering or mid-fruit would be our rst choice for elimination. If the ant population is initially low due to existing pesticide use or habitat degradation, then not spraying at the beginning of new vegetative growth could release Helopeltis to a high damage level at this critical stage of growth. Modication to a spray schedule could be developed (either upward or downward) as a monitoring program indicates need. Cost savings and habitat enhancement in crop production are of interest to all growers, and we encourage governments to adopt the approach of trying to decrease and hopefully eliminate the use of pesticides in cashew. We also chal-

lenge governments to initiate projects to dissect the suite of natural predators and parasitoids, including ants, into their functional ecological roles within cashew plots. Finally, it must be appreciated that this study is a rst approximation of the relationship between cashew nut and ants. We pooled our within-plot collection data and, while not evident to us during our visits, there is probably variation in ant species richness among individual trees. Also, given the vegetational complexity of land adjacent to our study sites, some varying edge effect seems inevitable. However, the relationship with ants is not an incidental or trivial event and demands more detailed study if it is to lead to elimination of pesticide use in cashew nut production. LITERATURE CITED
ABRAHAM, E. V. 1958. Pests of cashew (Anacardium occidentale) in south India. Indian Journal of Agricultural Science 28: 531543. AMBIKA, B., AND C. C. ABRAHAM. 1984. Bio-ecology of Helopeltis antonii Sign. infesting cashew trees. In E. V. V. B. Rao and H. H. Khan [eds.], Cashew: research and development, 299300. Indian Society for Plantation Crops, Kasaragod, Kerala, India. ANDERSEN, A. N., AND J. D. MAJER. 1991. The structure and biogeography of rainforest ant communities in the Kimberley region of northwestern Australia. In N. L. McKenzie, R. B. Johnston, and P. G. Kendrick [eds.], Kimberley rainforests, 333346. Surrey Beatty & Sons, Chipping Norton, Australia. ANDRIGHETTI, L., G. F. BASSI, P. CAPELLA, A. M. DE LOGU, A. B. DEOLALIKAR, G. HAEUSLER, G. A. MALORGIO, F. M. C. FRANCA, G. RIVOIRA, L. VANNINI, AND R. DESERTI. 1994. The world cashew economy. Edizioni Linchiostroblu, Bologna, Italy. ANONYMOUS. 1995. Cashew growers, your attention please. The Cashew 8: 2. BAKER, G. 1972. The role of Anoplolepis longipes Jerdon (Hymenoptera: Formicidae) in the entomology of cacao in the Northern District of Papua New Guinea. In International Congress of Entomology, Abstracts, 327. Canberra, Australia. BEATTIE, A. J. 1985. The evolutionary ecology of antplant mutualisms. Cambridge University Press, Cambridge. BENTLEY, B. L. 1977. The protective function of ants visiting the extraoral nectaries of Bixa orellana L. (Bixaceae). Journal of Ecology 65: 2738. . 1983. Nectaries in agriculture, with an emphasis on the tropics. In B. Bentley and T. Elias [eds.], The biology of nectaries, 204 222. Columbia University Press, New York, NY. BISHOP, L., AND S. E. RIECHERT. 1990. Spider colonization of agroecosystems: mode and source. Environmental Entomology 19: 1738 1745. BROWN, E. S. 1959a. Immature nutfall of coconuts in the Solomon Islands. I. Distribution of nutfall in relation to that of Amblypelta and of certain species of ants. Bulletin of Entomological Research 50: 97133. . 1959b. Immature nutfall of coconuts in the Solomon Islands. II. Changes in ant populations, and their relation to vegetation. Bulletin of Entomological Research 50: 523558. BRUNEAU DE MIRE, P. 1969. Une fourmi utilisee au Cameroun dans la lutte contre les mirides du cacaoyer Wasmannia auropuncta Roger. Cafe Cacao The 8: 209212. BUCKLEY, R. C. 1982. Antplant interactions: a world review. In R. C. Buckley [ed.], Ant-plant interactions in Australia, 111162. Junk, The Hague, The Netherlands. CARTER, P. E., AND A. L. RYPSTRA. 1995. Top-down effects in soybean agroecosystems: spider density affects herbivore damage. OIKOS 72: 433439. DENT, D. 1991. Yield loss assessment. Chapter 3 in Insect pest management. C.A.B. International, Redwood Press, Wiltshire, UK. FARM CHEMICALS HANDBOOK. 1994. Meister Publishing Company, Willoughby, OH. FIALA, B., AND U. MASCHWITZ. 1992. Food bodies and their signicance for obligate ant-association in the tree genus Macaranga (Euphor-

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their control in Indiaa review of current status. Journal of Plantation Crops 4: 3750. PIMENTEL, D. 1986. Acroecology (sic) and economics. In M. Kogan [ed.], Ecological theory and integrated pest management practice, 299319. John Wiley & Sons, New York, NY. PRICE, P. W., AND G. P. WALDBAUER. 1994. Ecological aspects of pest management. In R. L. Metcalf and W. H. Luckmann [eds.], Introduction to insect pest management, 3572. John Wiley & Sons, New York, NY. RISCH, S. J., D. ANDOW, AND M. A. ALTIERI. 1983. Agroecosystem diversity and pest control: data, tentative conclusions, and new research directions. Environmental Entomology 12: 625629. STONEDAHL, G. M. 1991. The Oriental species of Helopeltis (Hemiptera: Miridae): a review of economic literature and guide to identication. Bulletin of Entomological Research 81: 465490. , M. B. MALIPATIL, AND W. HOUSTON. 1995. A new mirid (Heteroptera) pest of cashew in northern Australia. Bulletin of Entomological Research 85: 275278. SUNDARARAJU, D. 1984. Cashew pests and their natural enemies in Goa. Journal of Plantation Crops 12: 3846. TILMAN, D. 1978. Cherries, ants and tent caterpillars: timing of nectar production in relation to susceptibility of caterpillars to ant predation. Ecology 59: 686692. VAN DER MEER MOHR, J.-C. 1927. Au sujet du role de certaines fourmis dans les plantations coloniales. Bulletin agricole du Congo belge et du Ruanda-Urundi 31: 97106. VAN DER WERF, E. 1993. Agronomic and economic potential of sustainable agriculture in south India. American Journal of Alternative Agriculture 8: 185191. VANDERMEER, J. 1995. The ecological basis of alternative agriculture. Annual Review of Ecology and Systematics 26: 201224. , AND D. A. ANDOW. 1986. Prophylactic and responsive components of an integrated pest management program. Journal of Economic Entomology 79: 299302. YAACOB, O, W. A. R. NGAH, AND A. J. KAMAL. 1984. Effect of rainfall, age and position on the nutrient content of cashew nut leaf on tin tailing in Malaysia. In E. V. V. B. Rao and H. H. Kahn [eds.], Cashew: research and development, 8590. Indian Society for Plantation Crops, Kasaragod, Kerala, India. , AND S. SUBHADRABANDHU. 1995. The production of economic fruits in South-East Asia. Oxford University Press, Kuala Lumpur, Malaysia. APPENDIX Study site locationsThe site locations were not irrigated except for 1st-yr plantings in Sri Lanka. The Sri Lankan and India locations experience a pronounced dry season, while the Malaysia location, south of Kuala Lumpur, is much wetter year-round. There were no unsprayed locations in India (except the 1985 Calicut site), and no sprayed locations in Malaysia. Sri LankaThree sampling plots were used in western Sri Lanka near the village of Vannativillu, 20 km north of Puttalam at 8 10 N, 79 50 E. Two sampling locations were identied in eastern Sri Lanka 30 km S of Walikanda, at 7 40 N, 81 15 E, within the Mahaweli Development Project. WEST 1. Sri Lanka Cashew Corporation Station (SLCCW); 250 ha with a wide variety of tree ages and ground vegetation present. Insecticide is applied using the standard three applications per growing season. Some older plantings are irregularly sprayed. A well-managed, productive government cashew research station with a working staff and on-site manager. 2. Panadura Estate (PANA); private ownership of 200 ha with a range of trees from 1 yr to over 20 yr. Large area of new plantings with banana, melon, or chili interplanting. No spraying on any part of the estate, which is located 3 km N of SLCCW. A well-managed, strong producing cashew estate with working staff and on-site manager. 3. Pushparanghnam Estate (PUSH); small private ownership of 2.5 ha

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with a single grove of 20-yr-old, unsprayed trees. Mixed scrub vegetation outside of planting grove with mixture of vegetation around and under cashew trees. This is an example of a small plot from which the owner hopes to collect and sell nuts each year with little or no cash input. EAST 4. Sri Lanka Cashew Corporation Station (SLCCE); 100 ha in size but not all planted. Mostly mature trees with little upkeep, and there is mixed shrub vegetation around and under cashew trees. The trees are unsprayed. 5. Informatics Agrotech (Pvt.) Ltd. Plantations (INFO); a well-run, 200 ha, private estate with a eld work staff and an on-site manager. Plantings consist of mostly younger trees, the oldest being 810 yr and the youngest 1 yr. Some complex interplanting including bananas, chilies, pineapple, and teak; a mixture of grass and small shrubs were present under the older plantings. A mixture of sprayed and unsprayed planting blocks were available. The Informatics plantings are 5 km from SLCCE. IndiaOur 1985 observations took place around Calicut, Kerala, India (CALI) at 11 20 N, 75 30 E.

Two government research stations in Kerala, Quilon District, were sampled in 1992. The stations were similar in being well run and having on-site managers and a large working staff. The sites are 10 km apart at 9 20 N, 77 00 E. Both sites used insecticides during the growing season. 1. Kottarakara State Seed Research Farm (KOTA), with 10 ha of mature 20 yr old cashew planted at 200 trees per ha on 7-m square spacing. Each year fertilizer is applied to a shallow trench around each tree. 2. District Agricultural Farm (DIST), with yr-old trees. 3 ha of well-tended, 15-

West MalaysiaThe main cashew growing region is in the northeast, which we did not visit. We sampled two adjacent research plots growing on sand tin mine tailings, 96.4% sand and 3.6% clay silt (Yaacob, Ngah, and Kamal, 1984) 1.5 m thick, on the campus of University Pertanian Malaysia (Malaysia), Serdang, Selangor, West Malaysia (MALAY) 25 km S of Kuala Lumpur at 3 2 N, 101 40 E. One block of trees is 2030 yr old with no upkeep whatsoever. A younger planting of trees, all 810 yr, was also sampled. None of the trees receives any insecticide treatment or upkeep except for occasional mowing of the grass around the younger trees.