JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY 59(4), 1986, pp. 580-587

Distribution and Abundance of D?ptera in Flypaper Traps at Theobroma cacao L. (Sterculiaceae) Flowers in

Costa Rican Cacao Plantations

Allen M. Young

Invertebrate Zoology Section, Milwaukee Public Museum, Milwaukee, Wisconsin 53233

abstract: Small (4.0 x 2.5 cm) pieces of sticky flypaper were placed among freshly opened flowers of Theobroma cacao L. (Sterculiaceae) in two Costa Rican cacao plantations

during the 1982 rainy season to determine the kinds and relative abundances of Diptera

visiting flowers. Censuses of small-bodied dipterans, involving five cacao trees at each

locality, were taken to determine differences between day and night activity. A cacao tree was deliberately deflowered to determine if flowerless trees would attract fewer flies. A

total of 17 dipteran families were collected. Phoridae accounted for 52% of the combined

sample followed by Sciaridae (13%) and Drosophilidae (12%). Sixty percent of all dipterans were trapped at night at both localities combined. Patterns of abundance between night and day were consistent between localities. No difference in abundance of dipterans was

found between flower-intact and deflowered trees, possibly a result of small, dispropor tionate sample sizes.

Various taxa of small-bodied (3-7 mm) Diptera are floral visitors and effective

pollinators of the Neotropical rain forest understory tree Theobroma cacao L.

(Sterculiaceae) (e.g., Jones, 1912; Harland, 1925; Posnette, 1944, 1950; Soetardi, 1950; Van der Knapp, 1955; Saunders, 1959; Walker, 1959; Glendenning, 1962;

Gorrez, 1962; Hernandez, 1965; Sampayan, 1966; Amponsah, 1975; Soria and

Wirth, 1979; Soria et al., 1980; Young, 1983). The mechanism of pollination of cacao flowers by Ceratopogonidae, the dipteran family considered to be the most effective pollinators, is summarized by Bystrak and Wirth (1978). As part of

continuing studies on the floral biology of cacao and related species of Theobroma

(Young et al., 1984), I present here a preliminary floral visitor profile for cacao that was obtained by trapping flying insects within the immediate vicinity of open flowers. Although it is generally accepted that cacao pollinator activity is greatest in the daylight morning hours (Hernandez, 1965; Bystrak and Wirth, 1978), my

study included an examination of day and night insect visitors to the vicinity of cacao flowers for two localities in Costa Rica.

Materials and Methods

These studies were conducted during July 1982, at two cacao plantation local

ities within the Atlantic or Caribbean watershed of Costa Rica: Finca La Tigra, near La Virgen (10?23'N, 84?07'W; 220 m elev.), Sarapiqui District, Heredia

Province; Finca Experimental La Lola, near Siquirres (10?06'N, 83?30'W; 50 m

elev.), Limon Province. Observations on Diptera in cacao trees were conducted

80 meters from the perimeters of the plantations at both localities. Studies were

conducted during a peak period of flowering activity in cacao, a highly seasonal

phenomenon in Costa Rica (Young, 1984a). Although highly cauliflorous, the

Accepted for publication 29 January 1986.

VOLUME 59, NUMBER 4 581

relatively small, compact flowers of T. cacao render them suitable for enclosing with flypaper rectangles to snare small-bodied dipterans (Fig. 1). I used locally available flypaper, Papel Matamuscas, and cut it into approximately 4.0 x 2.5 cm pieces. I then positioned two or three pieces of the flypaper, using pins, around each cacao flower (Fig. 1). I randomly selected 10 to 30 flowers on each of several trees to conduct a census of flying insects approaching flowers. Sampling was

divided into two major periods: 1700 to 0700 hours for a night census which

included dusk and dawn periods, and 0700 and 1700 hours for a day census. At

the end of each census, the flypaper pieces were collected by pinning them to a

large sheet of sturdy cardboard carried into the field. The flypaper was always replaced between censuses. For the census period beginning at 1700 hours, I

selected flowers just in the initial phase of opening (Fig. 1) to follow the cycle of

anthesis previously described for cacao (Wellensiek, 1932). Flowers were fully open for the day census beginning at 0700 hours (Fig. 1). Censuses conducted in this manner were: La Tigra, day censuses: 10, 11, and 29 July; night censuses:

11, 12, 13, and 27 July 1982; La Lola, day censuses: 20 and 22 July 1982; night censuses: 17, 18, 19, 21, and 23 July. For two of the La Tigra censuses (one day and one night census) and three of the La Lola censuses (one day and two night censuses), I removed all open flowers and mature floral buds from one tree during each census. I then distributed flypaper pieces on branches of these deflowered trees while simultaneously distributing flypaper pieces around flowers in two or

three nearby trees. For the La Lola studies, I used the cacao cultivar UF-677 for all censuses, while at La Tigra, I used a mix of undetermined cultivars. In T.

cacao, different cultivars often have varying degrees of floral pigmentation, al

though such differences apparently do not influence floral attractiveness to pol

linating insects (Alvim, 1984). At the La Tigra site, the 3-9 trees used for all censuses were 2-7 m apart, but at La Lola trees immediately adjacent (2 m apart)

were used. In the laboratory, I excised small portions of flypaper bearing trapped insects and placed them in 70% ethanol in small glass vials for later examination.

With few exceptions, I avoided teasing trapped insects from the flypaper since

they are easily destroyed by this procedure. Samples were then shipped to the Insect Identification and Beneficial Insect Introduction Institute in Beltsville,

Maryland for determinations.

Additionally, I attempted to trap insects directly on cacao flower stigmas and

styles by coating 250 open flowers in one night census at La Tigra and one day census (9-10 July 1982). To do so, I prepared a 20% concentration gum arabic solution and carefully painted stigmas and styles. Each treated flower was marked

with a color-capped pin to facilitate relocation 10-12 hours later. The treated flowers (250 day and 250 night) were examined for trapped insects. At La Lola

(21 July 1982), using a red-cellophane-covered standard flashlight, I gently tapped and attempted to trap insects on a total of 200 randomly-selected open flowers between 1900 and 2200 hours. Each flower was tapped after placing a large glass vial over it to catch any fleeing insects.

Results

No insects were trapped in the gum arabic-coated stigmas and styles of the 500 treated cacao flowers at La Tigra. Additionally, no insects were dislodged from 200 flowers during the night time survey at La Lola.

582 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

Fig. 1. Floral biology of Theobroma cacao L. (Sterculiaceae). Clockwise, from upper left photo:

one-day-old flowers and mature floral bud; ceratopogonid midge perched on petal hood concealing

anthers; freshly-opened flower at about 0800 hr and showing positioning of flypaper rectangles; flypaper

rectangles positioned around flowers in the initial stage of opening (about 1700 hr).

The flypaper rectangles collected 17 families of Diptera, in addition to an

occasional ant and several thrips. Considering both day and night censuses and

both localities combined, the most abundant dipterans were Phoridae, comprising 52% of all dipterans captured by this technique (Table 1). Megaselia was the most common genus of phorids found in the samples. Sciaridae were only one-fourth as abundant (13.11%) followed closely by Drosophilidae (11.89%) (Table 1). Cer atopogonidae, one of the principal groups of effective pollinators of T. cacao,

comprised 8% of the total sample. The percent composition of dipteran families was strikingly similar between the two localities, although the Sciaridae were more

than twice as abundant at La Lola than at La Tigra (Table 1). Trapped insects in

VOLUME 59, NUMBER 4 583

Table 1. The taxonomic composition and abundance of Diptera trapped in flypaper traps both

day and night at two cacao plantation localities in the Atlantic (Caribbean) watershed region of Costa

Rica during the rainy season (July 1982).a

Family

No. of individuals at La Tigra

No. of individuals at La Lola % of total sample

Day Night Total Day Night Total La Lola La Tigra Combined

Phoridae 34 Drosophilidae 6

Ceratopogonidae 2

Sciaridae 3

Chironomidae 1

Mycetophilidae 0 Empipidae 1

Milichilidae 3 Syrphidae 1

Asteriidae 1

Acroceridae 0

Cecidomyiidae 0

Leptogastridae 0

Simuliidae 0 Ephydridae 0

Psychodidae 0

Dolichopodidae 0

Total 52

La Tigra:

La Lola:

Both localities combined:

49

15

8

9

1

6

0

0

0

0

2

0

0

0

0

0

1

91

83

21

10

12

2

6

1

3

1

1

2

0

0

0

0

0

1

143

26 0 3

11 2 0 0 0 0 0 0 0 1 1 1

0 1

46

17 8 6 9 6 3 1

0 0 0 0 3 0 0 0 1 1

55

43 8 9

20 8 3 1

0 0 0 0 3 1 1 1 1

2

101

% day, flying insects, all groups: % night, flying insects, all groups:

% day, flying insects, all groups: % night, flying insects, all groups:

% day, flying insects, all groups: % night, flying insects, all groups:

58.04% 14.69%

6.99%

8.39%

1.40%

4.20%

42.57%

7.92%

8.91%

19.80% 7.92%

2.97%

51.64%

11.89%

7.79%

13.11%

4.10%

3.69%

52/143 = 36.36% 91/143 = 63.64%

46/101 = 45.54% 55/101 = 54.46%

98/244 = 40.16% 146/244 = 59.84%

1 Data given are for all censuses (see "Materials and Methods").

the La Tigra samples were 25% more abundant than in the La Lola samples (Table

1). The night samples at both localities yielded more insects than the day censuses

(Table 1), but at La Lola there were more night censuses than day censuses.

A higher percentage of flypaper pieces contained trapped dipterans on cacao

trees with flowers present than on neighboring deflowered trees (Table 2). Inter

estingly, even though there was close to a 30% increase in the number of flowers treated with flypaper traps on flower-intact trees for La Tigra, exactly the same

number of flypaper pieces had trapped insects for the two localities (Table 2). Furthermore, the total number of trapped insects was higher for the census with

both fewer flowers and fewer flypaper traps (La Lola) (Table 2).

Discussion

These data indicate that sticky flypaper rectangles placed on branches of both flower-intact and deflowered T. cacao trees during the Central American rainy season will trap numerous small-bodied adult Diptera representing many families.

Furthermore, such traps will snare dipterans both day and night. Since cacao trees are grown in a typical plantation setting for commercial purposes, it is not sur

prising to find high numbers of dipterans in both flower-intact and deflowered

Table 2.

Rica.

The comparative abundance of flypaper-trapped Diptera between flower-intact Theobroma cacao L. at two cacao plantation localities in Costa

Locality Total flowers used Total flypaper

pieces used Total pieces

occupied

Total flying insects

trapped

O G

>

O

H 33 m

>

m Z H O S o r O

S o > r m O

Q

La Tigra

La Lola

flower-intact trees (6) deflowered trees (2) flower-intact trees (6) deflowered trees (3)

Combined localities and censuses

(N = 5 censuses)

% flypaper pieces occupied, flower-intact trees (12):

% flypaper pieces occupied, deflowered trees (5):

120 0

98 0

369 (x ? SD = 73.80 ? 20.69) 157 (x? SD = 31.40 ? 1.51)

92/369 = 24.93% 22/157 = 14.01%

66

181 91

92(18.40 ? 7.09) 22 (4.40 ? 4.03)

46 57 7 13

46 78 15 17

135 (27.00 ? 12.00) 30(6.00 ?6.12)

a For La Tigra: 3 flower-intact trees and 1 deflowered tree used for each of 2 censuses or total of 8 trees (6 + 2); La Lola: 2 flower-intact trees and 1 deflowered

tree for each of 3 censuses or total of 9 trees (6 + 3). La Tigra censuses: 27-28 July 1982 (night and day); La Lola: 20-21 July 1982 (1 day and 2 nights).

VOLUME 59, NUMBER 4 585

trees. Some studies indicate that cacao-pollinating dipterans such as Ceratopo

gonidae fly considerable distances among flowering cacao trees (Entwistle, 1972). Furthermore, relatively little is understood about the attraction of insects to the

flowers of T. cacao. Although it is believed that cacao flowers have little or no

fragrance for attracting pollinators (Bystrak and Wirth, 1978), recent studies reveal

both the presence of nectar and fragrance (Young et al., 1984; Strand, 1984).

Stejskal (1969) reported the presence of nectaries in cacao flowers.

The data suggest that a portion of local Diptera assemblages in cacao habitats

in Costa Rica are active throughout the day and night. The flowers of T cacao

generally begin to open in the late afternoon and are fully open by 0500 hours the following morning (Wellensiek, 1932). Anthers dehisce shortly thereafter, and

pollen presumably is liberated throughout the day. A dipteran assemblage active

throughout the day may ensure continual pick up of pollen grains during visits to cacao flowers. Bees or bee body parts (i.e., wings) were notably absent from the flypaper samples. Stingless bees are occasional floral visitors of T. cacao in

the American tropics (Soria, 1975; Young, 1981, 1984b). The low abundance of both Ceratopogonidae and Cecidomyiidae, two groups of dipterans known to be

pollinating agents of T. cacao (e.g., Posnette, 1944, 1950; Soetardi, 1950; Her

nandez, 1965; Saunders, 1959; Kaufmann, 1973, 1975; Bystrak and Wirth, 1978

[review]; Young, 1985), is not surprising since these midges occur in low densities in cacao flowers (Entwistle, 1972). Cecidomyiid midges pick up large quantities of T. cacao pollen grains by 0700 hours in the Ivory Coast (Lucas, 1981).

Phorids such as Megaselia pollinate Herrania species (Sterculiaceae) in Costa Rica (Young, 1984c). Theobroma and Herrania are closely related within the Sterculiaceae (Cuatrecasas, 1964). Other Neotropical relatives such as Sterculia

possess flowers highly adapted for pollination by several families of saprophilus Diptera (Taroda and Gibbs, 1982). Whether or not phorids such as Megaselia actually visit the flowers of T. cacao has not been determined. But the observed

high relative abundance of phorids in my study suggests the group warrants closer

scrutiny in terms of T. cacao pollination. Both phorids and cecidomyiids are

possible pollinators of some rain forest grasses in Central and South America

(Soderstrom and Calder?n, 1971). Phorids are crepuscular floral visitors at Her rania trees in Costa Rica (Young, 1984c), and T. cacao flowers have not been

intensively studied at these hours. Taroda and Gibbs (1982) report a close cor relation between the diurnal activity pattern of dipterans with anthesis and nectar release in Sterculia chicha St. Hil. in Brazil. Fontanilla-Barroga (1962) noted

pollination of T. cacao in the Philippines to occur throughout the day, but with a peak of activity at about 1500 hours. Most studies of cacao pollination, in fact, have focused upon the abundance of floral visitors in the daylight morning hours, and generally not at other times of the day. A complete understanding of polli nation in cacao and related species of Theobroma might necessitate detailed stud ies at other times of the day, i.e., at dawn and dusk.

Acknowledgments

This research was funded by grants from the American Cocoa Research Institute of the United States of America. I am most grateful for the patience and coop eration of entomologists at the Systematic Entomology Laboratory, U.S. De

partment of Agriculture, for their willingness to examine messy flypaper-trapped

586 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

small dipterans. Technical assistance with sorting of samples was provided by Melanie Strand. I thank Dr. J. Robert Hunter for providing access and hospitality for the La Tigra studies, and to the Cacao Program at C.A.T.I.E., Turrialba, Costa

Rica, for logistical assistance for the La Lola studies. Comments on the manuscript by a reviewer and the editor of this journal were most helpful in revising the

paper.

Literature Cited

Alvim, P. de T. 1984. Flowering of cocoa. Cocoa Grower's Bull. 35:23-3 \.

Amponsah, N. 1975. Studies on natural pollination of cocoa in Ghana. 4th Internat. Cocoa Res.

Conf., Trinidad & Tobago.

Bystrak, P. G., and W. W. Wirth. 1978. The North American species of Forcipomyia, subgenus

Euprojoannisia (Diptera: Ceratopogonidae). U.S. Dept. Agrie. Tech. Bull. No. 1591. 51 pp.

Cuatrecasas, J. 1964. Cacao and its allies. A taxonomic revision of the genus Theobroma. Contribu?.

Nat. Herb. 35:379-614.

Entwistle, P. F. 1972. Pests of Cocoa. Longmans, London. 779 pp.

Fontanilla-Barroga, S. 1962. A progress report on the study of insects associated with pollination of

Theobroma cacao with special emphasis on midges. Philipp. J. Agrie. 27:147-159.

Glendinning, D. R. 1962. Natural pollination of cacao. Nature 193:1305.

Gorrez, F. 1962. The flower biology, morphology, and pollinating and crossing habits of cacao.

Philipp. Agri. 46:288-302.

Harland, S. C. 1925. Studies in cacao. Part I. The method of pollination. Ann. Biol. 12:403-409.

Hernandez, J. 1965. Insect pollination of cacao (Theobroma cacao L.) in Costa Rica. Doctoral

Dissertation. Univ. of Wisconsin, Madison. 84 pp.

Jones, G. A. 1912. The structure and pollination of the cacao flower. West Indian Bull. 12:347-350.

Kaufmann, T. 1973. Preliminary observations on cecidomyiid midge and its role as a cocoa pollinator in Ghana. Ghana J. Agrie. Sei. 6:193-198.

-. 1975. Biology and behaviour of cocoa pollinating Ceratopogonidae in Ghana. Environ.

Entomol. 4:347-351.

Lucas, P. 1981. Etude des conditions de pollinisation du cacaoyer au Togo. The Cafe, Cacao 25:

113-120.

Posnette, A. F. 1944. Pollination of cacao in Trinidad. Trop. Agrie. (Trinidad) 21:115-118. -. 1950. The pollination of cacao in the Gold Coast. J. Hort. Sei. 25:155-163.

Sampayan, T. S. 1966. Flower biology, fruiting habit and compatibility relationship in cacao. Philipp. J. Plant Indust. 31:193-201.

Saunders, L. G. 1959. Methods for studying Forcipomyia midges, with special reference to cacao

pollinating species (Diptera, Ceratopogonidae). Can. J. Zool. 37:33-51.

Soderstrom, T. R., and C. E. Calder?n. 1971. Insect pollination in tropical rain forest grasses.

Biotropica 3:1-16.

Soetardi, R. G. 1950. De Betekenis van Insecten Bij Bestuiving van Theobroma caco L. Arch.

Koffiecult. Indon?sie 17:1-31.

Soria, S. de J. 1975. O papel des abelhas sem farrao (Meliponinae) na polinzacao do cacaueiro na

America Tropical. Rev. Theobroma 5:12-20.

Soria, S. de J., and W. W. Wirth. 1979. Ceratopogonid midges (Diptera: Nematocera) collected from

cacao flowers in Palmira, Columbia: an account of their pollinating abilities. Rev. Theobroma

9:77-84.

Soria, S. de J., W. W. Wirth, and R. K. Chapman. 1980. Insect pollination of cacao in Costa Rica.

1. Preliminary list of the ceratopogonid midges collected from flowers. Rev. Theobroma 10:

61-68.

Stejskal, M. 1969. Nectar y aroma de las flores del cacao. Oriente Agropeuc. 1:75-92.

Strand, M. A. 1984. Comparative floral morphology of four Theobroma (Sterculiaceae) species in

relation to pollination biology. Master's Thesis. Univ. of Wisconsin, Milwaukee. 77 pp.

Taroda, N., and P. E. Gibbs. 1982. Floral biology and breeding system of Sterculia chicha (Ster

culiaceae). New Phytol. 90:735-744.

Van Der Knapp, W. P. 1955. Observations on the pollination of cacao flowers. Rept. 14th Internat.

Hort. Congr. 2:1287-1293.

VOLUME 59, NUMBER 4 587

Walker, C. 1959. Notes on the botany of cacao. Agricult. J. (Fiji) 29:56-61.

Wellensiek, S. J. 1932. Flower biological observations with cocoa. Arch. Koffiecult. Indon?sie 6:87

101.

Young, A. M. 1981. The ineffectiveness of the stingless bee Tr?gona jaty (Hymenoptera: Apidae:

Meliponinae) as a pollinator of cocoa (Theobroma cacao L.). J. Appl. Ecol. 18:149-155.

-. 1983. Seasonal differences in abundance and distribution of cocoa-pollinating midges in

relation to flowering and fruit-set between shaded and sunny habitats of the La Lola Cocoa

Farm. J. Appl. Ecol. 20:801-831. -. 1984a. Flowering and fruit-setting patterns of cocoa trees (Theobroma cacao L.) (Sterculi

aceae) at three localities in Costa Rica. Turrialba 34:129-142.

-. 1984b. Research on the natural pollination of cocoa in Central America: overview of current

directions. Proc. 9th Internad. Cocoa Res. Conf., Lome, Togo. pp. 557-565.

-. 1984c. Mechanism of pollination by Phoridae (Diptera) in some Herrania species (Stercu

liaceae) in Costa Rica. Proc. Entomol. Soc. Wash. 86:503-518. -. 1985. Studies of cecidomyiid midges (Diptera: Cecidomyiidae) as cocoa pollinators (Theo

broma cacao L.) in Central America. Proc. Entomol. Soc. Wash. 87:49-79.

Young, A. M., M. Schaller, and M. A. Strand. 1984. Floral nectaries and trichomes in relation to

pollination in some species of Theobroma and Herrania (Sterculiaceae). Amer. J. Botany 71 :

466-480.