Medical arid Veferinary Entomology (1992) 6, 188- 194
Patterns of sandfly distribution in tropical forest: a causal hypothesis J A N E M E M M O TT
Department of Pure arid Applied Biology, University of Leeds
Abstract. 1. In tropical rain forest, phlebotomine sandflies (Diptera: Psychodidae), such as Lutzoniyia vespertilionis and L.ylephiletor, have an aggregated distribution on their tree buttress diurnal resting sites, as studied during 1987-88 at Finca la Selva in the Caribbean lowlands of Costa Rica. 2 . Experimental transfer of flies to trees not used as resting sites indicated that many apparentlj suitable sites remain unoccupied. 3 . Observations of sandflies on the buttresses revealed that males and females are juxtaposed more frequently than expected by chance alone. Courtship behaviour by three of the four species of sandfly studied was observed on the butt r e s e s . 4. It is suggested that the use of buttresses as swarming sites for mating behaviour is more likely to account for the observed distribution patterns of sandflies than their use of buttresses simply as diurnal resting sites. Key words. Lutzomyia spp., Phlebotominae, aggregated distribution, swarming sites, tree buttress, tropical rain forest, Costa Rica.
Introduction In ecological studies it is usual to find that an organism has a contagious distribution (Southwood. 1980). A number of mathematical models have been developed describing such distributions, but the underlying biological cause of the heterogeniety usually remains unknown. A good example of such a species-specific contagious distribution is to he found in sandflies living among tree buttresses in a Central American tropical rain forest. Phlebotornine sandflies (Diptera: Psychodidae) are small. nocturnally active bloodsucking flies. In the tropical rain forest. diurnal resting sites include hollow trees, animal burrows, low shrubs. leaf litter and tree buttresses. A different spectrum of sandfly species is found on each site (Christensen rf d..lY83). In the study area, four specics of sandfly are commonly found on tree buttresses. f.ut;ornxiu shunriorii Dyar 1929, L.y[ephilefor Fairchild cYC Hcrtig 1952. I..trtcpidoi Fairchild 8: Hertig 1952 and I.. ~ , ( ~ . ~ ~ ~ (Fairchild , ~ t ~ ~ i bi u ~Hertig z j . ~ 1947. When looking a~ the dktrihution o f these sandflies on tree buttresses, three patterns become apparent: ( 1 f 'The four species of sandfly are aggregated, to varying . on soiiie trees in the forest and on one or more. C'orrqmndence I>r Jane Memrnott, Centre for Population Biolog\ I m p c n ~ i lCollege at S ~ l w o o dPark, Axor, Berks SL? 7PY I'h
I sx
buttresses of a single tree. The diffcrentiation between buttresses is seen with all four sandfly species, in that contiguous and superficially similar buttresses often bear very different numbers of sandflies. In the most extreme case, L . vespertilionis is consistently restricted to a single buttress within a tree (Memmott, 1991). (2) When sandfly species occur together upon a buttress they are spatially segregated resulting i n a pattern of zonation (Chaniotis e f al., 1972; Mernrnott, 1 Y Y l ) . (3) The sex ratio of sandflies on tree buttresses is male biased (e.g. Christensen et al., 1983), whereas the sex ratio of sandflies emerging from laboratory cultures is 1: 1 (Theodor, 1965). These three factors suggest that the tree buttress is rather more than a simple diurnal resting site. The aim of this paper is to determine the cause of these patterns using two methods of investigation: ( I ) By direct observation of sandflies on buttresses, thereby looking for any behaviour which could cause an aggregated distribution. (2) By altering the suitability of the resting site and directly testing hypotheses accounting for the sandflies' choice of where to settle.
Methods Sricdy site. The study was conducted at Finca La Selva,
Patterns o j sandjy distribution in tropical forest an Organization for Tropical Studies field station in the Caribbean lowlands of Costa Rica, Central America. Fieldwork was undertaken during March- August 1987 and April-August 1988. The area has primary forest, secondary forest, swamps and abandoned plantations (Holdridge et a l . , 1971). Studies were undertaken in the primary forest and parts of the secondary forest with large trees. The trees used throughout this study were examples of Sloania, Inga, Ceiba pentandra and Dipteiyx panamemis, all buttressed and of canopy or emergent height. Observations of sandflies on tree buttresses. Sandflies were observed during four periods: daytime, night-time, dawn and dusk. Day-time observations were made whenever sandflies were being collected from trees. The night, dawn and dusk observations were restricted to four favoured trees, on which sandflies were watched from dusk through until dawn on twelve occasions. Observations on pairs of sandfles. Since sandfly species are zoned upon the buttress resting sites, further departures from a random distribution on a buttress may provide clues as to the cause of their diurnal aggregation. Observations made while collecting flies had shown that some were positioned in pairs, characteristically with one fly displaced a few millimetres behind another. It was suspected that the flies were male/female pairs. To test for this, juxtaposed pairs of flies (closer than 5 mm) were collected from aggregations of sandflies. The flies were identified and the number of male/male, male/female and female/ female pairs were compared with that expected by chance alone. The expected frequencies were calculated from the observed sex ratios on the buttresses, male proportion: L.ylephiletor = 0.64, Lshannoni = 0.75 (Memmott, 1991). Field experiments. Sandfly identification usually involves clearing the dead specimen, mounting and examining the spermathecae or male genitalia under high power (Theodor, 1965). Obviously this taxonomic method is not compatible with identification of living specimens in the field prior to field experimentation. However, external morphology has been used to identify man-biting species in Panama (Chaniotis, 1974) and a similar method was developed for differentiating the four species of sandfly on tree buttresses (Memmott, 1989). For these Costa Rican sandflies the size, wing angle, colour and resting position on a buttress provided a method of differentiating the species. Representative specimens identified in the field were checked in the laboratory by microscopic examination of genitalia, using the keys of Murillo & Zeledon (1085), and all the field determinations were found to be correct. Transplant of sandflies to favoured and unfavoured trees or buttresses. With respect to the aggregation of sandflies upon certain trees in the forest, the simplest explanation is that only a few trees are suitable for use as diurnal resting sites. This possibility was tested by means of transplant experiments. For tracing transplanted sandflies, they were marked with fluorescent dusts and subsequently relocated using an ultraviolet lamp (Killick-Kendrick et al., 1984). L..shannoni and L.ylephiletor were transplanted to both ‘favoured’ and ‘unfavoured’ trees. A favoured tree was
189
defined as a tree consistently used as a diurnal resting site by the transplanted species of fly. An unfavoured tree was defined as one on which the transplanted species of fly was rarely, if ever, found. By comparing the rate at which the flies leave the trees, the relative suitability of the two categories can be compared. The rate was assessed over two time periods: during daylight hours and overnight. The flies were collected into pots designed to maintain a high humidity (Chaniotis, 1975). They were then transferred to pots in which they were marked with fluorescent dust, and from these the flies were released onto favoured and unfavoured buttresses. The transplants took place at 08.00-09.00 hours after any resident sandflies had been removed before the transplant took place. Transplanted flies were recounted between 08.00 and 00.00 hours the following morning and, on three occasions (two of L.ylephiletor and one of L.shannoni), they were also recounted at 16.00 hours on the day of transplantation. Lshannoni was transplanted nine times to a favoured tree and seven times to an unfavoured tree; L.ylephiletor was transplanted nine times to a favoured tree and four times to an unfavoured tree. The disparity in the number of transplants to favoured and unfavoured trees relates to vagaries in climatic conditions. Transplants were only run when the weather was fine: it is difficult to find, identify and manipulate the fies in rain, due to the low light levels then found at the bases of tree buttresses. Totals of 354 L.shannoni and 349 L.ylephiletor were transplanted during the experiments. In the case of Lvespertilionis, the sandfly species restricted to a single buttress per tree (Memmott, 1991), the simplest explanation for this pattern is that the distribution of its host animal determines its pattern of distribution. This sandfly species feeds exclusively upon bats (Tesh et al., 1972) and emballonurid bats were seen periodically in all of the buttresses used by Lvespertilionis. To test this hypothesis, L.vespertilionis were collected, marked with fluorescent dusts and transplanted between a pair of sites on the same tree: a favoured buttress and an adjacent unfavoured buttress. The rate of dispersal on the buttresses was compared in order to assess their relative suitability as diurnal resting sites. Three experiments comprising six transplants were run, using 12-33 L. vespertilionis per transplant. As for the other species, transplants took place between 08.00 and 09.00 hours; flies were recounted at 16.00 hours the same day and 08.00-09.00 hours the following morning. Any sandflies already on the buttresses were removed before a transplant experiment took place.
Results
Direct observations Pairs offlies. Sixty-five pairs of flies were collected from the tree buttresses. Of these, sixty-one pairs consisted of conspecifics. Using a Chi-squared test to compare the observed and expected frequencies of malelmale, male/ female and female/female pairs, both L..sharzrzorii and L .ylephiletor showed significant differences between the
observed and random results (Table I ) , with fewer male/ male pairs and more male/female pairs than would be expected from chance alone. Thus, as might be expected, it appears that males and females become associated on tree buttresses. Ohservatioris of satidfries oti tree buttresses. Day-time observations: the sandflies remained stationary upon the tree for the vast majority of time. All four species of Lutzomyia adults of both sexes sat facing upwards and, if disturbed, would jump up the buttress a few centimetres. While collecting L.sharitzorii from buttresses, pairs were observed copulating on twelve occasions. This was a rare event as approximately 6000 L.shanriorii were collected from buttresses over the study period. Dusk observations: courtship behaviour was observed among L. iqx,rriliotris and L.plephi/efor. For the latter. the behaviour consisted of the males vibrating their wings and hopping short distances. Wing vibrations and hops by one male usually initiated identical behaviour in adjacent males. L. w.spertiliotiis had similar courtship behaviour and, in addition. L.i~e.sparriliorzi.smales frequently made a lateral waggling motion of the abdomen. Lshanriotii was observed simply to leave the tree at dusk and Ltrapidoi was not observed during this period. Night-time observations: on only one occasion out of twelve night watches were sand flies seen throughout the night. Generally the flies left the tree overnight and were seen at dawn and dusk only. In the case where flies rernaincd on the buttresses all night. there was a great deal of activity with flies moving all over the surface of the buttrcsces. N o sandflies werc seen on adjacent trees. The sandflies were sampled by collecting from one of the trees’ four buttresses at 09.00, 11.00, 04.30 and 06.30 hours (dusk and dawn were at 18.00 and 05.30 hours respectively). L.ylephi/etor was seen throughout the night, while t.trapitloi and L.shannoni were most numerous at dawn did not use this tree as a resting site. (Fig. 1). L.~~esperti/ionis Dawn observations: Lshaririorii moved up and down
Table 1. O b x n e d and expected frequency of male/malc. male/ femalc nnd tcmale/female pairs of sandflies ( a ) L viephileior. (t?) L \hunnorfl (a) I , v l q ~ / d e r o (proportion r inale
=
100 80
21.00 hours
60 40
20
0
120 I
100
04.30 hours
80 60 40 20 0 50
06.15 hours
40 30 20 10
0
Y
T
S
Fig. 1. The abundance and identity of the sandflies observed swarming on a tree at four times of’dayand night. Y . Lvlephilelor: T, L.irapidoi: S. L.shannoni.
the buttresses in a series of short hops describing a circle, eventually coming to rest at the base of the buttress. The top of the circle was approximately l m above ground level. When another sandfly was encountered, the flies usually stopped moving, vibrated their wings and then recommenced circling behaviour. L.trapidoi was not seen showing any sign of courtship behaviour. However, this is the most difficult of the four species to observe because of its pale colour. It is also the most easily disturbed of the four, tending to fly from the buttress when alarmed.
Field experimerits
0.61) ~~~
Ohservcd values Expectcd valucs 1’ = 7.6. df
Male/male
Femaldfemale
Malc/female
0 17.6
6
28
5.8
19.8
= 2.
0.05.
( b ) I ,hcrnnoni (proportion male
=
0 75)
~~
Mdlelmale
O h e r r c d valuc5 Expected value\
x’z
hh
6 10 1
’I = 2 . I ’ . 0 05
~~~~
Female/femalc
Malelfemale
0 11
12 68
Analysis. Numbers of replicates are small: only four L.viephiletor transplants to unfavoured trees, and only three L . iwprtilioriis transplants to both favoured and unfavoured buttresses. Data is given in the form of pcrcentage recapturc: as different numbers of flies were trdnsplanted during each experiment. Chi-squared tests were used to assess the significance of differences in the proportions o f flies remaining on favoured and unfavoured trees. The data is presented in its original form to show the level of variation between replicates. Trarisplarit of L..shatrtroni arid L.ylephiletor to favoured arid unfavoured trees. (a) During daylight hours (Table 2 ) . In the three transplants checked at 16.00 hours on the day of release. the vast majority of the flies had remained on
Patterns of sandfiy distribution in tropical forest
191
Table 2. Thc dispersal rate of L.shannoni and L.ylephi1etor on favoured and unfavoured trees during daylight hours.
Favoured tree
Unfavoured tree
Day 1
Day 1
Expt
Species
08.00 hours
16.00 hours
Per cent recapture
1
L.shannoni L.ylephiletor L.ylephiletor
24 32 29
24 32 29
85
8.5
2 3 Total
the buttress. For the analysis L.shannoni and L.ylephiltor are considered together. Only two out of the 175 flies transplanted left the tree during daylight hours. N o significant difference was found in the behaviour of the flies on favoured and unfavoured trees (x2 = 1.9, df = 1, P > 0.05). (b) Overnight (Table 3 ) . For both favoured and unfavoured trees, the majority of both L.shannoni and L.ylephileror left the tree overnight. For L.shannoni but not L . ylephiletor there is a significant difference between the numbers of flies remaining on favoured and unfavoured Table 3. The dispersal rate of (a) Lshannoni and (b) L.ylephiletor on favoured and unfavoured trees overnight.
(a) L.shannoni Favoured tree Expt
Unfavoured tree
Day 1 Day 2 Yo recapture Day 1 Day 2 YOrecapture 31 16 13 14 24 14 17 24 5.5
Total 208
1 1 0 0 2 0 1 5
10.3 14.7 0 0 0 14.3 0 4.2 9
24 31 21 19 18 18 27
1 1 0 0 0 0 0
4.16 3.22 0 0 0 0 0
10
4.8
158
2
1.3
0
(b) L.ylephiletor ~~
08.00 hours
16.00 hours
Per cent recapture
100 100
31 31 28
31 31 26
100 93
100
90
88
98
100
100
x2
trees (L.shannoni: = 3.95, df = 1, P< 0.05; L.ylephiletor: x2=2.07, df = 1, P>O.O5). However, as can be seen from the data (Table 3 ) , there is considerable variation between replicates in the numbers leaving both favoured and unfavoured trees. Thus, caution must be used with the interpretation of this result. Transplants of L. vespertilionis to favoured and unfavoured buttresses. (a) During daylight hours (Table 4 ) . As in L.shannoni and L.ylephiletor, the vast majority of L . vespertilionis remained upon the buttress during daylight hours. No significant difference was found in the behavwur of L . vespertilionis on favoured and unfavoured trees during this period = 0.005, df = 1, P > 0.01). (b) Overnight (Table 5 ) . The type of buttress onto which L. vespertilionis was transplanted influenced its dispersal behaviour overnight. With transplants to favoured buttresses, some of the L.vespertilionis remained on the buttress overnight. When transplanted to an unfavoured buttress, no L . vespertilionis remained overnight. These results are significant (x2=24.1, df = 1, P < 0.OOOl). Although no L . vespertilionis stayed on the unfavoured buttress overnight, some did remain upon the tree. In all cases these flies had returned to the adjacent favoured buttress. The difference in behaviour on favoured and unfavoured buttresses is consistent between the three replicates. Thus, it appears that L. vespertilionis can readily discern between a favoured and an unfavoured buttress. The only obvious difference between favoured and unfavoured buttresses is that bats were seen on occasions in the favoured buttresses but not in unfavoured buttresses.
(x2
~
Favoured tree
Unfavoured tree
Discussion Expt
Day 1 Day 2 Yo recapture Day 1 Day 2 YO recapture 32 29 30 46 28 29 5.5 33 39
0 1 0 18 7 2 11 3 9
0 3 0 39 25 6.8 20 9.1 23
31 28 37 38
2 0 20 7
6 0 54.1 18.4
Total 321
51
16
134
29
21
1 2 3 4
5 6 7 8 9
Transplant experiments demonstrated that there was no significant difference in the turnover rate of Lutzomyia sandflies on favoured and unfavoured trees during daylight hours. The vast majority of flies remain on both types of tree throughout the diurnal resting period. This indicates that the unfavoured tree is suitable for use as a diurnal resting site, but it is apparently lacking in some other attribute of importance to the flies. Further support for this is provided by the behaviour of L . vespertilionis after its transplant to an unfavoured buttress. This species also remained upon the buttress throughout the diurnal resting
192
June Memmott Table 4. The dispersal rate of Lvesperrilionis on favoured and unfavoured trees during daylight hours.
Transplant to unfavoured buttress
Transplant to favoured buttress
Day 1
Day 1 Expt
Per cent recapture
08.00 hours
16.00 hours
Per cent recapture
08.00 hours
16.00 hours
16 16 33
16
2 3
15 33
100 94 100
12 32 15
12 32 14
100 100 93
Total
65
64
98
59
58
98
~
~~
1
Table 5. The dispersal rate of L.vespertilionis on favourcd and unfavoured trees overnight.
Transplant to favoured buttress
Transplant to unfavoured buttress
Day 2
Day 2
Day 1: No.
Espt
transplanted
1
16
2 3
16 33
Total
65
Day 1: Favoured buttress
Other buttress
No.
transplanted
Unfavourcd buttress
Other buttress ~
12 32
5
0 0 0
22
0
9 8
period. but overnight the flies either left the tree or moved to the adjacent favoured buttress. Thus the unfavoured buttress, like the unfavoured tree, is suitable for use as a diurnal resting site, but it is apparently lacking in some other attribute of importance to the flies. In the case of the favoured and unfavoured trees. the nature of the attraction is not clear. In the case of L . vespertilionis on favoured and unfavoured buttresses the evidence strongly suggests that the attractant is a bat. I n view of the fact that L.ve.sperti1ioni.s feeds habitually on bats' blood, initially it would appear to be a simple case of the flies being attracted to their food source. However, 75% of all L. vespertilionis caught on tree buttresses were male (Memmott, 1991) and male sandflies do not feed on blood. If it is not the bat per se which is serving as the attractant to the male L. vespertilionis, then it is probably female L. vesperrilionis feeding upon the bat which forms the attractant. The female foraging site is one of the sites at which male insects usually concentrate their mating efforts (Thornhill & Alcock, 1983). Aggregations of the oriental sandfly Phlehotomus nrgentipes on cattle in Sri Lanka: with a majority of males, were reported by Lane et al. (1990). They described courtship behaviour of the sandflies on their host animals which clearly served to assemble both sexes of P.argentipes together for reproductive purposes. Lutzomyia spp. were observed to swarm on tree buttresses at dusk and dawn and, on one occasion, throughout the night. At these times the sandflies were seen circling in a series o f jumps on the buttress and approaching and
~~
15
0 0 0
4 4 1
59
0
9
~
vibrating their wings at nearby sandflies. The circling behaviour is typical of swarming Diptera in general (Downes, 1969) and the wing vibrations are typical of courting sandflies in particular (Chaniotis, 1967; Ward et al., 1988). Such behaviour would not be expected if buttresses were simply diurnal resting sites. The aim of this study was to determine the cause of the pattern of aggregation in sandflies. The transplant experiments strongly suggest that the buttress is more than just a diurnal resting site and observations of sandfly aggregations at dawn and dusk demonstrate that the tree is used as a swarming site. Although tree buttresses serve well as diurnal resting sites, 1 would propose that the process which determines the pattern of aggregation on the trees and buttresses is more probably the use of buttresses as swarming sites. Thus, the aggregations of sandflies found on buttresses represent two-dimensional static swarms which ceased their dynamic activity with the advent of daybreak. The use of tree buttresses as swarming sites accounts for the three patterns described in the introduction: (1) The aggregated distribution: by definition swarming results in an aggregated distribution. ( 2 ) The spatial segregation of species found on the same buttress: observations of multispecies Diptera swarms have repeatedly demonstrated that differences in timing or position (e.g. Gibson, 1945; Downes, 1969) are important isolating mechanisms. (3) A male bias sex ratio: the behaviour of male and female flies is different; males engage primarily in mating ef-
Patterns of saridfy distribution in tropical forest
fort while females invest largely in parental care (Thornhill, 1980). Thus, there is a higher turnover of females in the swarm and a male bias sex ratio. There are four sites at which male insects may concentrate their efforts in mate location: female emergence sites, oviposition sites, female foraging sites and neutral landmark sites (Thornhill & Alcock, 1983). For L.vespertilionis the buttress represents a female foraging site. The other three species of sandfly feed on hosts such as sloths, primates and rodents (Tesh et al., 1972), none of which are present regularly on buttresses. Hence the buttress is unlikely to represent a female foraging site for these three species. The buttress is also unlikely to be an oviposition site for these species, as it is known that the oviposition site is not the buttress for Panamanian sandflies found on buttresses (Rutledge & Mosser, 1972). By elimination, therefore, it would appear that if the tree buttress is a mating site for L.shannoni, L.ylephiletor and L.trapidoi, it must represent a neutral landmark site. A neutral landmark site is a distinctive topographical or physical feature of the environment which is used as a mating site (Thornhill & Alcock, 1983). Landmark swarming sites are believed to represent a default mating strategy used when no more profitable alternative exists (Bradbury, 1981). Thus, the male sandflies may also swarm on other sites, for example on the female foraging site. This would explain why the flies do not remain upon the observed buttresses for any length of time. In many landmark-based systems, the frequency of copulation is very low. For example, in 450 h of observation of a butterfly landmark site (a hilltop), matings were observed on only twelve occasions. However, although mating was rarely observed, courtship behaviour was frequently reported (Alcock, 1987). The fact that observations of sandfly matings were uncommon on the buttresses is not surprising if the site is considered as of the landmark type. The landmark mating system facilitates aggregation for mate location in organisms living in a large, spatially complex habitat such as a rain forest. Why some trees are used as swarming sites and others are not is unclear. There is usually no discernible difference to the human eye between such trees. It is believed that sandflies have pheromones which are used during courtship (Lane et al., 1985; Ward et al., 1988). However, it is unlikely that these are used to attract sandflies from any distance to the buttresses, as there is little air movement in the rain forest understorey to transport pheromones about the forest. Attempts have been made to control sandflies by spraying tree buttresses with residual insecticides. However, as already stated, swarming at landmark sites is believed to be a default strategy of swarming insects, used when no more profitable alternatives exist. Thus a major portion of a sandfly population may not be using the buttresses, in which case the loss of the buttress swarming site will probably not have a great effect on the size of the sandfly population. In a pilot study in Manaus, Brazil, Ready et al. (1985) found no decrease in the nocturnal flying population of Lumbratilis after tree buttress resting sites were sprayed
193
with DDT. This result would be predicted if tree buttresses are considered as a default swarming site rather than an essential resting site.
Acknowledgments
The work was carried out under the tenure of a NERC studentship which fully supported the field work in Costa Rica. I thank both the Department of Pure and Applied Biology and the Organization of Tropical Studies for the use of their facilities. I also thank Dr R. P. Lane for advice and helpful discussions during the course of this study.
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Tesh. R.B., Chaniotis, B.N.. Aronson, M.D. & Johnson, K.M. (1972) Further studies on the natural host prefercnces of Panamanian sandflies. American Journal of Epidemiology, 95.88-93. Theodor, 0 . (1965) On the classification of American Phlebotomidae. Journal of Medical Entomology, 2, 171- 197. Thornhill, R. (1980) Sexual selection within mating swarms of the lovebug Pleciu neartica (Diptera: Bibionidae). Animal Behaviour. 28, 405-412. Thornhill, R. & Alcock, J . (1983) The Evolution ofInsect Mating Systems. Harvard University Press, Cambridge, Mass. Ward, R.D., Phillips, A . , Burnet, B. & Brisola, C.M. (1988) The Lutzomyia longipalpis complex: reproduction and distribution. Biosystematics of Haematophagous Arthropods (ed. by M. W. Service). pp. 257--269. Oxford University Press. Accepted 29 March 1W2
Patterns of sandfly distribution in tropical forest: a causal hypothesis J A N E M E M M O TT
Department of Pure arid Applied Biology, University of Leeds
Abstract. 1. In tropical rain forest, phlebotomine sandflies (Diptera: Psychodidae), such as Lutzoniyia vespertilionis and L.ylephiletor, have an aggregated distribution on their tree buttress diurnal resting sites, as studied during 1987-88 at Finca la Selva in the Caribbean lowlands of Costa Rica. 2 . Experimental transfer of flies to trees not used as resting sites indicated that many apparentlj suitable sites remain unoccupied. 3 . Observations of sandflies on the buttresses revealed that males and females are juxtaposed more frequently than expected by chance alone. Courtship behaviour by three of the four species of sandfly studied was observed on the butt r e s e s . 4. It is suggested that the use of buttresses as swarming sites for mating behaviour is more likely to account for the observed distribution patterns of sandflies than their use of buttresses simply as diurnal resting sites. Key words. Lutzomyia spp., Phlebotominae, aggregated distribution, swarming sites, tree buttress, tropical rain forest, Costa Rica.
Introduction In ecological studies it is usual to find that an organism has a contagious distribution (Southwood. 1980). A number of mathematical models have been developed describing such distributions, but the underlying biological cause of the heterogeniety usually remains unknown. A good example of such a species-specific contagious distribution is to he found in sandflies living among tree buttresses in a Central American tropical rain forest. Phlebotornine sandflies (Diptera: Psychodidae) are small. nocturnally active bloodsucking flies. In the tropical rain forest. diurnal resting sites include hollow trees, animal burrows, low shrubs. leaf litter and tree buttresses. A different spectrum of sandfly species is found on each site (Christensen rf d..lY83). In the study area, four specics of sandfly are commonly found on tree buttresses. f.ut;ornxiu shunriorii Dyar 1929, L.y[ephilefor Fairchild cYC Hcrtig 1952. I..trtcpidoi Fairchild 8: Hertig 1952 and I.. ~ , ( ~ . ~ ~ ~ (Fairchild , ~ t ~ ~ i bi u ~Hertig z j . ~ 1947. When looking a~ the dktrihution o f these sandflies on tree buttresses, three patterns become apparent: ( 1 f 'The four species of sandfly are aggregated, to varying . on soiiie trees in the forest and on one or more. C'orrqmndence I>r Jane Memrnott, Centre for Population Biolog\ I m p c n ~ i lCollege at S ~ l w o o dPark, Axor, Berks SL? 7PY I'h
I sx
buttresses of a single tree. The diffcrentiation between buttresses is seen with all four sandfly species, in that contiguous and superficially similar buttresses often bear very different numbers of sandflies. In the most extreme case, L . vespertilionis is consistently restricted to a single buttress within a tree (Memmott, 1991). (2) When sandfly species occur together upon a buttress they are spatially segregated resulting i n a pattern of zonation (Chaniotis e f al., 1972; Mernrnott, 1 Y Y l ) . (3) The sex ratio of sandflies on tree buttresses is male biased (e.g. Christensen et al., 1983), whereas the sex ratio of sandflies emerging from laboratory cultures is 1: 1 (Theodor, 1965). These three factors suggest that the tree buttress is rather more than a simple diurnal resting site. The aim of this paper is to determine the cause of these patterns using two methods of investigation: ( I ) By direct observation of sandflies on buttresses, thereby looking for any behaviour which could cause an aggregated distribution. (2) By altering the suitability of the resting site and directly testing hypotheses accounting for the sandflies' choice of where to settle.
Methods Sricdy site. The study was conducted at Finca La Selva,
Patterns o j sandjy distribution in tropical forest an Organization for Tropical Studies field station in the Caribbean lowlands of Costa Rica, Central America. Fieldwork was undertaken during March- August 1987 and April-August 1988. The area has primary forest, secondary forest, swamps and abandoned plantations (Holdridge et a l . , 1971). Studies were undertaken in the primary forest and parts of the secondary forest with large trees. The trees used throughout this study were examples of Sloania, Inga, Ceiba pentandra and Dipteiyx panamemis, all buttressed and of canopy or emergent height. Observations of sandflies on tree buttresses. Sandflies were observed during four periods: daytime, night-time, dawn and dusk. Day-time observations were made whenever sandflies were being collected from trees. The night, dawn and dusk observations were restricted to four favoured trees, on which sandflies were watched from dusk through until dawn on twelve occasions. Observations on pairs of sandfles. Since sandfly species are zoned upon the buttress resting sites, further departures from a random distribution on a buttress may provide clues as to the cause of their diurnal aggregation. Observations made while collecting flies had shown that some were positioned in pairs, characteristically with one fly displaced a few millimetres behind another. It was suspected that the flies were male/female pairs. To test for this, juxtaposed pairs of flies (closer than 5 mm) were collected from aggregations of sandflies. The flies were identified and the number of male/male, male/female and female/ female pairs were compared with that expected by chance alone. The expected frequencies were calculated from the observed sex ratios on the buttresses, male proportion: L.ylephiletor = 0.64, Lshannoni = 0.75 (Memmott, 1991). Field experiments. Sandfly identification usually involves clearing the dead specimen, mounting and examining the spermathecae or male genitalia under high power (Theodor, 1965). Obviously this taxonomic method is not compatible with identification of living specimens in the field prior to field experimentation. However, external morphology has been used to identify man-biting species in Panama (Chaniotis, 1974) and a similar method was developed for differentiating the four species of sandfly on tree buttresses (Memmott, 1989). For these Costa Rican sandflies the size, wing angle, colour and resting position on a buttress provided a method of differentiating the species. Representative specimens identified in the field were checked in the laboratory by microscopic examination of genitalia, using the keys of Murillo & Zeledon (1085), and all the field determinations were found to be correct. Transplant of sandflies to favoured and unfavoured trees or buttresses. With respect to the aggregation of sandflies upon certain trees in the forest, the simplest explanation is that only a few trees are suitable for use as diurnal resting sites. This possibility was tested by means of transplant experiments. For tracing transplanted sandflies, they were marked with fluorescent dusts and subsequently relocated using an ultraviolet lamp (Killick-Kendrick et al., 1984). L..shannoni and L.ylephiletor were transplanted to both ‘favoured’ and ‘unfavoured’ trees. A favoured tree was
189
defined as a tree consistently used as a diurnal resting site by the transplanted species of fly. An unfavoured tree was defined as one on which the transplanted species of fly was rarely, if ever, found. By comparing the rate at which the flies leave the trees, the relative suitability of the two categories can be compared. The rate was assessed over two time periods: during daylight hours and overnight. The flies were collected into pots designed to maintain a high humidity (Chaniotis, 1975). They were then transferred to pots in which they were marked with fluorescent dust, and from these the flies were released onto favoured and unfavoured buttresses. The transplants took place at 08.00-09.00 hours after any resident sandflies had been removed before the transplant took place. Transplanted flies were recounted between 08.00 and 00.00 hours the following morning and, on three occasions (two of L.ylephiletor and one of L.shannoni), they were also recounted at 16.00 hours on the day of transplantation. Lshannoni was transplanted nine times to a favoured tree and seven times to an unfavoured tree; L.ylephiletor was transplanted nine times to a favoured tree and four times to an unfavoured tree. The disparity in the number of transplants to favoured and unfavoured trees relates to vagaries in climatic conditions. Transplants were only run when the weather was fine: it is difficult to find, identify and manipulate the fies in rain, due to the low light levels then found at the bases of tree buttresses. Totals of 354 L.shannoni and 349 L.ylephiletor were transplanted during the experiments. In the case of Lvespertilionis, the sandfly species restricted to a single buttress per tree (Memmott, 1991), the simplest explanation for this pattern is that the distribution of its host animal determines its pattern of distribution. This sandfly species feeds exclusively upon bats (Tesh et al., 1972) and emballonurid bats were seen periodically in all of the buttresses used by Lvespertilionis. To test this hypothesis, L.vespertilionis were collected, marked with fluorescent dusts and transplanted between a pair of sites on the same tree: a favoured buttress and an adjacent unfavoured buttress. The rate of dispersal on the buttresses was compared in order to assess their relative suitability as diurnal resting sites. Three experiments comprising six transplants were run, using 12-33 L. vespertilionis per transplant. As for the other species, transplants took place between 08.00 and 09.00 hours; flies were recounted at 16.00 hours the same day and 08.00-09.00 hours the following morning. Any sandflies already on the buttresses were removed before a transplant experiment took place.
Results
Direct observations Pairs offlies. Sixty-five pairs of flies were collected from the tree buttresses. Of these, sixty-one pairs consisted of conspecifics. Using a Chi-squared test to compare the observed and expected frequencies of malelmale, male/ female and female/female pairs, both L..sharzrzorii and L .ylephiletor showed significant differences between the
observed and random results (Table I ) , with fewer male/ male pairs and more male/female pairs than would be expected from chance alone. Thus, as might be expected, it appears that males and females become associated on tree buttresses. Ohservatioris of satidfries oti tree buttresses. Day-time observations: the sandflies remained stationary upon the tree for the vast majority of time. All four species of Lutzomyia adults of both sexes sat facing upwards and, if disturbed, would jump up the buttress a few centimetres. While collecting L.sharitzorii from buttresses, pairs were observed copulating on twelve occasions. This was a rare event as approximately 6000 L.shanriorii were collected from buttresses over the study period. Dusk observations: courtship behaviour was observed among L. iqx,rriliotris and L.plephi/efor. For the latter. the behaviour consisted of the males vibrating their wings and hopping short distances. Wing vibrations and hops by one male usually initiated identical behaviour in adjacent males. L. w.spertiliotiis had similar courtship behaviour and, in addition. L.i~e.sparriliorzi.smales frequently made a lateral waggling motion of the abdomen. Lshanriotii was observed simply to leave the tree at dusk and Ltrapidoi was not observed during this period. Night-time observations: on only one occasion out of twelve night watches were sand flies seen throughout the night. Generally the flies left the tree overnight and were seen at dawn and dusk only. In the case where flies rernaincd on the buttresses all night. there was a great deal of activity with flies moving all over the surface of the buttrcsces. N o sandflies werc seen on adjacent trees. The sandflies were sampled by collecting from one of the trees’ four buttresses at 09.00, 11.00, 04.30 and 06.30 hours (dusk and dawn were at 18.00 and 05.30 hours respectively). L.ylephi/etor was seen throughout the night, while t.trapitloi and L.shannoni were most numerous at dawn did not use this tree as a resting site. (Fig. 1). L.~~esperti/ionis Dawn observations: Lshaririorii moved up and down
Table 1. O b x n e d and expected frequency of male/malc. male/ femalc nnd tcmale/female pairs of sandflies ( a ) L viephileior. (t?) L \hunnorfl (a) I , v l q ~ / d e r o (proportion r inale
=
100 80
21.00 hours
60 40
20
0
120 I
100
04.30 hours
80 60 40 20 0 50
06.15 hours
40 30 20 10
0
Y
T
S
Fig. 1. The abundance and identity of the sandflies observed swarming on a tree at four times of’dayand night. Y . Lvlephilelor: T, L.irapidoi: S. L.shannoni.
the buttresses in a series of short hops describing a circle, eventually coming to rest at the base of the buttress. The top of the circle was approximately l m above ground level. When another sandfly was encountered, the flies usually stopped moving, vibrated their wings and then recommenced circling behaviour. L.trapidoi was not seen showing any sign of courtship behaviour. However, this is the most difficult of the four species to observe because of its pale colour. It is also the most easily disturbed of the four, tending to fly from the buttress when alarmed.
Field experimerits
0.61) ~~~
Ohservcd values Expectcd valucs 1’ = 7.6. df
Male/male
Femaldfemale
Malc/female
0 17.6
6
28
5.8
19.8
= 2.
0.05.
( b ) I ,hcrnnoni (proportion male
=
0 75)
~~
Mdlelmale
O h e r r c d valuc5 Expected value\
x’z
hh
6 10 1
’I = 2 . I ’ . 0 05
~~~~
Female/femalc
Malelfemale
0 11
12 68
Analysis. Numbers of replicates are small: only four L.viephiletor transplants to unfavoured trees, and only three L . iwprtilioriis transplants to both favoured and unfavoured buttresses. Data is given in the form of pcrcentage recapturc: as different numbers of flies were trdnsplanted during each experiment. Chi-squared tests were used to assess the significance of differences in the proportions o f flies remaining on favoured and unfavoured trees. The data is presented in its original form to show the level of variation between replicates. Trarisplarit of L..shatrtroni arid L.ylephiletor to favoured arid unfavoured trees. (a) During daylight hours (Table 2 ) . In the three transplants checked at 16.00 hours on the day of release. the vast majority of the flies had remained on
Patterns of sandfiy distribution in tropical forest
191
Table 2. Thc dispersal rate of L.shannoni and L.ylephi1etor on favoured and unfavoured trees during daylight hours.
Favoured tree
Unfavoured tree
Day 1
Day 1
Expt
Species
08.00 hours
16.00 hours
Per cent recapture
1
L.shannoni L.ylephiletor L.ylephiletor
24 32 29
24 32 29
85
8.5
2 3 Total
the buttress. For the analysis L.shannoni and L.ylephiltor are considered together. Only two out of the 175 flies transplanted left the tree during daylight hours. N o significant difference was found in the behaviour of the flies on favoured and unfavoured trees (x2 = 1.9, df = 1, P > 0.05). (b) Overnight (Table 3 ) . For both favoured and unfavoured trees, the majority of both L.shannoni and L.ylephileror left the tree overnight. For L.shannoni but not L . ylephiletor there is a significant difference between the numbers of flies remaining on favoured and unfavoured Table 3. The dispersal rate of (a) Lshannoni and (b) L.ylephiletor on favoured and unfavoured trees overnight.
(a) L.shannoni Favoured tree Expt
Unfavoured tree
Day 1 Day 2 Yo recapture Day 1 Day 2 YOrecapture 31 16 13 14 24 14 17 24 5.5
Total 208
1 1 0 0 2 0 1 5
10.3 14.7 0 0 0 14.3 0 4.2 9
24 31 21 19 18 18 27
1 1 0 0 0 0 0
4.16 3.22 0 0 0 0 0
10
4.8
158
2
1.3
0
(b) L.ylephiletor ~~
08.00 hours
16.00 hours
Per cent recapture
100 100
31 31 28
31 31 26
100 93
100
90
88
98
100
100
x2
trees (L.shannoni: = 3.95, df = 1, P< 0.05; L.ylephiletor: x2=2.07, df = 1, P>O.O5). However, as can be seen from the data (Table 3 ) , there is considerable variation between replicates in the numbers leaving both favoured and unfavoured trees. Thus, caution must be used with the interpretation of this result. Transplants of L. vespertilionis to favoured and unfavoured buttresses. (a) During daylight hours (Table 4 ) . As in L.shannoni and L.ylephiletor, the vast majority of L . vespertilionis remained upon the buttress during daylight hours. No significant difference was found in the behavwur of L . vespertilionis on favoured and unfavoured trees during this period = 0.005, df = 1, P > 0.01). (b) Overnight (Table 5 ) . The type of buttress onto which L. vespertilionis was transplanted influenced its dispersal behaviour overnight. With transplants to favoured buttresses, some of the L.vespertilionis remained on the buttress overnight. When transplanted to an unfavoured buttress, no L . vespertilionis remained overnight. These results are significant (x2=24.1, df = 1, P < 0.OOOl). Although no L . vespertilionis stayed on the unfavoured buttress overnight, some did remain upon the tree. In all cases these flies had returned to the adjacent favoured buttress. The difference in behaviour on favoured and unfavoured buttresses is consistent between the three replicates. Thus, it appears that L. vespertilionis can readily discern between a favoured and an unfavoured buttress. The only obvious difference between favoured and unfavoured buttresses is that bats were seen on occasions in the favoured buttresses but not in unfavoured buttresses.
(x2
~
Favoured tree
Unfavoured tree
Discussion Expt
Day 1 Day 2 Yo recapture Day 1 Day 2 YO recapture 32 29 30 46 28 29 5.5 33 39
0 1 0 18 7 2 11 3 9
0 3 0 39 25 6.8 20 9.1 23
31 28 37 38
2 0 20 7
6 0 54.1 18.4
Total 321
51
16
134
29
21
1 2 3 4
5 6 7 8 9
Transplant experiments demonstrated that there was no significant difference in the turnover rate of Lutzomyia sandflies on favoured and unfavoured trees during daylight hours. The vast majority of flies remain on both types of tree throughout the diurnal resting period. This indicates that the unfavoured tree is suitable for use as a diurnal resting site, but it is apparently lacking in some other attribute of importance to the flies. Further support for this is provided by the behaviour of L . vespertilionis after its transplant to an unfavoured buttress. This species also remained upon the buttress throughout the diurnal resting
192
June Memmott Table 4. The dispersal rate of Lvesperrilionis on favoured and unfavoured trees during daylight hours.
Transplant to unfavoured buttress
Transplant to favoured buttress
Day 1
Day 1 Expt
Per cent recapture
08.00 hours
16.00 hours
Per cent recapture
08.00 hours
16.00 hours
16 16 33
16
2 3
15 33
100 94 100
12 32 15
12 32 14
100 100 93
Total
65
64
98
59
58
98
~
~~
1
Table 5. The dispersal rate of L.vespertilionis on favourcd and unfavoured trees overnight.
Transplant to favoured buttress
Transplant to unfavoured buttress
Day 2
Day 2
Day 1: No.
Espt
transplanted
1
16
2 3
16 33
Total
65
Day 1: Favoured buttress
Other buttress
No.
transplanted
Unfavourcd buttress
Other buttress ~
12 32
5
0 0 0
22
0
9 8
period. but overnight the flies either left the tree or moved to the adjacent favoured buttress. Thus the unfavoured buttress, like the unfavoured tree, is suitable for use as a diurnal resting site, but it is apparently lacking in some other attribute of importance to the flies. In the case of the favoured and unfavoured trees. the nature of the attraction is not clear. In the case of L . vespertilionis on favoured and unfavoured buttresses the evidence strongly suggests that the attractant is a bat. I n view of the fact that L.ve.sperti1ioni.s feeds habitually on bats' blood, initially it would appear to be a simple case of the flies being attracted to their food source. However, 75% of all L. vespertilionis caught on tree buttresses were male (Memmott, 1991) and male sandflies do not feed on blood. If it is not the bat per se which is serving as the attractant to the male L. vespertilionis, then it is probably female L. vesperrilionis feeding upon the bat which forms the attractant. The female foraging site is one of the sites at which male insects usually concentrate their mating efforts (Thornhill & Alcock, 1983). Aggregations of the oriental sandfly Phlehotomus nrgentipes on cattle in Sri Lanka: with a majority of males, were reported by Lane et al. (1990). They described courtship behaviour of the sandflies on their host animals which clearly served to assemble both sexes of P.argentipes together for reproductive purposes. Lutzomyia spp. were observed to swarm on tree buttresses at dusk and dawn and, on one occasion, throughout the night. At these times the sandflies were seen circling in a series o f jumps on the buttress and approaching and
~~
15
0 0 0
4 4 1
59
0
9
~
vibrating their wings at nearby sandflies. The circling behaviour is typical of swarming Diptera in general (Downes, 1969) and the wing vibrations are typical of courting sandflies in particular (Chaniotis, 1967; Ward et al., 1988). Such behaviour would not be expected if buttresses were simply diurnal resting sites. The aim of this study was to determine the cause of the pattern of aggregation in sandflies. The transplant experiments strongly suggest that the buttress is more than just a diurnal resting site and observations of sandfly aggregations at dawn and dusk demonstrate that the tree is used as a swarming site. Although tree buttresses serve well as diurnal resting sites, 1 would propose that the process which determines the pattern of aggregation on the trees and buttresses is more probably the use of buttresses as swarming sites. Thus, the aggregations of sandflies found on buttresses represent two-dimensional static swarms which ceased their dynamic activity with the advent of daybreak. The use of tree buttresses as swarming sites accounts for the three patterns described in the introduction: (1) The aggregated distribution: by definition swarming results in an aggregated distribution. ( 2 ) The spatial segregation of species found on the same buttress: observations of multispecies Diptera swarms have repeatedly demonstrated that differences in timing or position (e.g. Gibson, 1945; Downes, 1969) are important isolating mechanisms. (3) A male bias sex ratio: the behaviour of male and female flies is different; males engage primarily in mating ef-
Patterns of saridfy distribution in tropical forest
fort while females invest largely in parental care (Thornhill, 1980). Thus, there is a higher turnover of females in the swarm and a male bias sex ratio. There are four sites at which male insects may concentrate their efforts in mate location: female emergence sites, oviposition sites, female foraging sites and neutral landmark sites (Thornhill & Alcock, 1983). For L.vespertilionis the buttress represents a female foraging site. The other three species of sandfly feed on hosts such as sloths, primates and rodents (Tesh et al., 1972), none of which are present regularly on buttresses. Hence the buttress is unlikely to represent a female foraging site for these three species. The buttress is also unlikely to be an oviposition site for these species, as it is known that the oviposition site is not the buttress for Panamanian sandflies found on buttresses (Rutledge & Mosser, 1972). By elimination, therefore, it would appear that if the tree buttress is a mating site for L.shannoni, L.ylephiletor and L.trapidoi, it must represent a neutral landmark site. A neutral landmark site is a distinctive topographical or physical feature of the environment which is used as a mating site (Thornhill & Alcock, 1983). Landmark swarming sites are believed to represent a default mating strategy used when no more profitable alternative exists (Bradbury, 1981). Thus, the male sandflies may also swarm on other sites, for example on the female foraging site. This would explain why the flies do not remain upon the observed buttresses for any length of time. In many landmark-based systems, the frequency of copulation is very low. For example, in 450 h of observation of a butterfly landmark site (a hilltop), matings were observed on only twelve occasions. However, although mating was rarely observed, courtship behaviour was frequently reported (Alcock, 1987). The fact that observations of sandfly matings were uncommon on the buttresses is not surprising if the site is considered as of the landmark type. The landmark mating system facilitates aggregation for mate location in organisms living in a large, spatially complex habitat such as a rain forest. Why some trees are used as swarming sites and others are not is unclear. There is usually no discernible difference to the human eye between such trees. It is believed that sandflies have pheromones which are used during courtship (Lane et al., 1985; Ward et al., 1988). However, it is unlikely that these are used to attract sandflies from any distance to the buttresses, as there is little air movement in the rain forest understorey to transport pheromones about the forest. Attempts have been made to control sandflies by spraying tree buttresses with residual insecticides. However, as already stated, swarming at landmark sites is believed to be a default strategy of swarming insects, used when no more profitable alternatives exist. Thus a major portion of a sandfly population may not be using the buttresses, in which case the loss of the buttress swarming site will probably not have a great effect on the size of the sandfly population. In a pilot study in Manaus, Brazil, Ready et al. (1985) found no decrease in the nocturnal flying population of Lumbratilis after tree buttress resting sites were sprayed
193
with DDT. This result would be predicted if tree buttresses are considered as a default swarming site rather than an essential resting site.
Acknowledgments
The work was carried out under the tenure of a NERC studentship which fully supported the field work in Costa Rica. I thank both the Department of Pure and Applied Biology and the Organization of Tropical Studies for the use of their facilities. I also thank Dr R. P. Lane for advice and helpful discussions during the course of this study.
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Memmotr. J . (1989) Community ecology of phlebotornine sandflies. Ph.D. thcsis, University of Leeds. Memmott. J . (1991) Sandfly distribution and abundance in a tropical rain forest. Medical und Veferinury Enfornology. 5 , Jo3-4 11. Murillo. J. RL Zeledon R. (1985) Flebotomus de Costa Rica (Diptcra: Psychodidae). Brensia. 23. 1-137. Ready, P.D.. Arias, J.R. & Freitas. R.A. (1985) A pilot study to control Lutzomyia umbrafilis (Diptera: Psychodidae), the major vector of Leishmania brasilensisi guyanensis in a periurban rainforest of manaus, Amazonas State, Brazil. Memoirs Instirule Osnulrio Cruz. Rio de Janeiro, 80 27-36 Rutledgc. L.C. & Mosser. H.L. (1972) Biology of immature handflies at thc bascs of trees in Panama. Environmental Entotnologx. 1. 3M-309. Southwood. T.R.E. (19%)) Ecological Methods. 2nd cdn. Chapman & Hall, London.
Tesh. R.B., Chaniotis, B.N.. Aronson, M.D. & Johnson, K.M. (1972) Further studies on the natural host prefercnces of Panamanian sandflies. American Journal of Epidemiology, 95.88-93. Theodor, 0 . (1965) On the classification of American Phlebotomidae. Journal of Medical Entomology, 2, 171- 197. Thornhill, R. (1980) Sexual selection within mating swarms of the lovebug Pleciu neartica (Diptera: Bibionidae). Animal Behaviour. 28, 405-412. Thornhill, R. & Alcock, J . (1983) The Evolution ofInsect Mating Systems. Harvard University Press, Cambridge, Mass. Ward, R.D., Phillips, A . , Burnet, B. & Brisola, C.M. (1988) The Lutzomyia longipalpis complex: reproduction and distribution. Biosystematics of Haematophagous Arthropods (ed. by M. W. Service). pp. 257--269. Oxford University Press. Accepted 29 March 1W2
