FORAGING AND HABITAT SELECTION BY TWO SPECIES OF

NEAR LORE LINDU NATIONAL PARK IN , IMDONESIA

A Thesis

Presented to

The Faculty of Graduate Studies

of

The University of Guelph

by

DAWN RENEE BAKKER

In partial fiilfilment of requirements

for the degree of

Master of Science

July, 1999

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FORAGiNG AND HABITAT SELECTION BY TWO SPECIES OF HONEY BEE NEAR LORE LMDU NATIONAL PARK IN SULAWESI, MDONESIA

Dawn Renee Bakker Advisor: University of Guelph, 1999 Professor Gard W. Otis

Near Lore Lindu National Park in Central Sulawesi, the honey bee A. cerana nests almost exclusively in disturbed habitats, while A. nigrocinctn main1y nests in fores!.

After standardizing dance curves, waggle dances of foragers were observed at an ecotone to detemine foraging distributions. Both species foraged much more in mixed habitat and in a nearby cleanng than in forest or in highly disturbed agricultural areas. Little difference in foraging locations was found between species, but A. nigrocincta foraged farther than A. cerana, and each species concentrated on a different source.

Swarms were set up along the ecotone and dances of scouts were quantified to detemine locations of possible nest sites scouted by A. cerana and A. nigrocincta. Scouts of both species danced for locations in forested and disturbed areas. Swarms of A. nigrocincta decided on locations in both areas, but swarms of A. cerana decided on nest sites only in disturbed areas. ACKNOWLEDCE,MENTS

1 dedicate this thesis to my brother Arlo, who came to to help me with my fieldwork. His cheemilness, patience, and Company throughout our time there were muc h appreciated.

1 thank Dr. G.W. Otis, my advisor. for his friendship and support. It has been a pleasure to work with him in the past two years. I also thank the other members of rny cornittee, Dr. T. Nudds and Dr. P.G. Kevan, for their enthusiasrn for my project.

Many people helped me along the way in my studies. Teny Gillespie of Land

Resource Science helped me with the azimuth equations needed to interpret the honey bee dances. 0. Brian Allen and Gatot Ilhamto helped with the statistics and gave statistical advice. Don Hamilton graciously gave assistance with some of the visual aids.

1 gratefully acknowledge the help of numerous people in Indonesia who helped my brother Ar10 and myself during our time in Indonesia: Ayub, who collected bees for us; Bapak and Ibu Fentje, who cared for us during our time in Kamarora; Ikhsan, who faithfully delivered Ietters and supplies when needed: and Duncan Neville, who shared his hospitality and English humour with us. Special thanks go to the staff of the Nature

Conservancy's Palu Field Office, and to the staff of Lore Lindu National Park.

The research was funded by an NSERC PGSA scholarship, two University of

Guelph Graduate Scholarships, the 1998 Maurice Smith Award. the 1998 Soden

Mernorial Scholarship, the 1998 Townsend award, and the 1998 Beatty Munroe

Scholarship. Travel costs were defrayed by an Arthur D. Latomell Graduate Travel

Grant. TABLE OF CONTENTS

... LISTOFTABLES ...... 111

LISTOFFIGURES ...... iv

ACKNOWLEDGEMENTS ...... vi

CHAPTER 1 GENEML INTRODUCTION ...... 7 1.1 Introduction to Honey Becs ...... 7 1.2 Apis nigrocincta ...... 7 1.3 The Uniqueness of Sulawesi ...... 9 1.4 Objectives of Study ...... 11

CHAPTER 2 DANCE CURVES AND FORAGING BY APIS CERRNA AND APIS NIGROCINCTA ...... 13 2.1 INTRODUCTION ...... 13 2.1.2 The Dance Language ...... 17 2.1.3 Colony Level Foraging ...... 19 2.1.4 Cornparison of Foraging Between A . cerana and A . nigrocincta ...... *...... 21 2.2 MATERIALS AND METHODS ...... -23 2.2.1 Dance Curves ...... 23 2.2.2 Foraging Maps ...... 24 2.3 RESULTS AND DISCUSSION ...... 27 2.3.1 Dance Curves ...... 27 2.3.2 Foraging Maps ...... 29 2.3.3 Foraging Ranges ...... -39 2.3.4 Pollen Collection ...... 44 2.3.5 Temporal Resource Partitioning ...... 48 2.3.6 Possible Sources of Variation ...... 56 2.3.7 Resource Use and Resource Preferences ...... 57 2.3.8 Conclusion ...... 59

CHAPTER 3 THE INFLUENCE OF HABITAT ON NEST SITE SCOUTING BY SWARMS OF AND APIS NIGROCINCTA ...... 61 3.1 INTRODUCTION ...... 61 3.1.1 Behaviour and Nest Site Selection ...... 61 3.1.2 General Overview of Habitat Selection ...... 63 3.1.3 Honey Bees and Habitat Selection ...... 74 3.2 MATERIALS AND METHODS ...... 76 3.3 RESULTS AND DISCUSSION ...... 8 1

CHAPTER 4 GENERAL DISCUSSION AND CONCLUSION ...... 91

APPENDIX A DANCE DATA FROM FORAGINC STUDY...... 105 A.1 Apiscerana ...... 105 A.2 Apis nigrocinctu...... 110

APPENDIX B DANCE DATA FROM SWARMING STUDY ...... 115 B. 1 Apis ceranu ...... 115 B.2 Apisnigrocincta ...... 117 LIST OF TABLES

Table 1. Parameters of distance distributions inferred frorn dances of A. cerana and A. nigrocincia to natural foraging sites...... 43

Table 2. Surnrnary of weather information during six days of hive observation near Lore Lindu National Park in Central Sulawesi...... 55

Table 3. Summary of swarms used for swarming study near Lore Lindu National Park in Central Sulawesi...... -78

Table 4. Location of trap hives and comments on damage andior occupancy of each hive during swarming experiment near Lore Lindu National Park in Central Sulawesi . LIST OF FIGURES

Figure 1. Map showing location of Sulawesi in the Indonesian archipelago...... 10

Figure 2. Waggle dances, oriented on vertical comb in order to communicate the direction from the hive of diagrammed food sources...... 18

Figure 3. Relationship between flight distance and circuit duration for A. cerana and A. nigrocincto in Central Sulawesi...... 28

Figure 1. Map of locations of food resources visited by A. >zigi.oci~zc~aforagers, as inferred from waggle dances in an observation hive on November 10, 1998. .. 30

Figure 5. Map of locations of food resources visited by A. nigrocincta foragers, as inferred from waggle dances in an observation hive on November 12, 1998. .. 3 1

Figure 6. Map of locations of food resources visited by A. nigrocincta foragers, as inferred from waggle dances in an observation hive on November 14, 1998. . 32

Figure 7. Map of locations of food resources visited by A. cerana foragers. as inferred from waggle dances in an observation hive on November 9, 1998...... 33

Figure 8. Map of locations of food resources visited by A. cerana foragers, as inferred from waggle dances in an observation hive on Novernber 1 1, 1998...... 31

Figure 9. Map of locations of food resources visited by A. cerana foragers, as inferred from waggle dances in an observation hive on November 13, 1998...... 35

Figure 10. Proportion of foragers of A. cerana and A. nigrocincta in four different types of habitat...... 36

Figure 1 1. Locations inferred from dances of A. cerana in an observation hive near the edge of Lore Lindu National Park in Central Sulawesi on Novernber 13, 1998. 38

Figure 12. Frequency distribution of flight distances inferred from dances of A. nigrocincta and A. cerana to natural food sources ...... 40

Figure 13. Mean distances inferred from dances of A. nigrocincta and A. ceranrr near the boundary of Lore Lindu National Park...... 41

Figure 14. Relative proportion of pollen of different colours brought into the hive by A. nigrocinctu foragers ...... 45

Figure 15. Relative proportion of pollen of different colours brought into the hive by A. Figure 16. Distribution of bees observed entering observation hives throughout the day ...... 49

Figure 17. Distribution of dances observed throughout the day...... 5 1

Figure 18. Distribution of foragers entering the hive with pollen throughout the day. . 53

Figure 19. Approximate locations of nest sites inspected. as inferred from dances of 4. cerana scouts on swmns hung at the ecotone between forest and disturbed agrïcultural area...... 82

Figure 20. Approximate locations of nest sites inspected. as inferred from dances of A. nigrocincto scouts on swarms hung at the ecotone between forest and disturbed agriculturalarea...... 83

Figure 2 1. Map indicating approximate distance and direction of sites agreed upon by A. cerana swarrn scouts...... 84

Figure 22. Map indicating approximate distance and direction of sites agreed upon by A. nigrocincta swarm scouts...... 85 CHAPTER 1

GENERAL INTRODUCTION

1.1 Introduction to Honey Bees

Honey bees are arguably the most well-known and well-studied species on

earth. Yet the vast majority of our knowledge centres around Apis mellifea, the cavity

nesting honey bee which is found throughout Europe, North and South Arnenca, and

Africa. Until recently, generally only three other species of honry bee in addition to A.

mellfera were recognized: Apis cerana. the eastem cavity-nesting honey bee; , the dwarf honey bee; and , the giant honey bee (Ruttner, 1988).

Relatively iittle was known about these three species.

A. cerana, sometimes termed the eastem equivalent of A. mellfera (Ruttner,

1988), is found throughout most of Asia from Pakistan in the West to the Philippine

islands and the Indonesian archipeiago in the east (Ruttner, 1988; Crane, 1995). To the

nonh, A. cerana's range extends into southem Russia and Japan, excluding Hokkaido

(Koeniger, 1995). Over this wide geographical range, A. cerona occupies both tropical

and temperate climates (Ruttner, 1988). Three distinct A. cerana subspecies have now

been widely recognized (A. c. indica, A. c. cerana, and A. c. jnponica), and evidence

suggests that more cavity-nesting honey bee populations might actually be subspecies

(Damus, 1995; Damus and Otis, 1997, and references therein).

1.2 Apis nigrocinctia

In 1989, Gard Otis and Soesiiawati Hadisoesilo found a different morph of cavity nesting honey bee on the island of Sulawesi. The bee was siightiy larger and distinctiy

7 lighter in colour than A. cerana. This bee rnorph was first described as A. nigrocincta by

F. Smith in 186 1, and was recognized as a species by Maa as late as 1953. For decades, however, most bee biologists considered it ro be a subspecies of A. cerana. Recently A. nigrocincta has been recognized as a separate species. In Sulawesi the two species can be easily distinguished because the hind femora and clypeus of A. nigrocincta are yellow and in A. cerana they are black (Hadisoesilo, 1997).

Genitals of the drones of each species are not ooticeably different (Hadisoesilo,

1997), suggesting that no physical bamer exists to prevent breeding between them.

However, species status for A. nigrocincta has been bestowed based on two main characteristics. First of dl, drones (and, by extension, queens) of the two species take their mating flights at different times of the day; this allows practically no oppominity for hybridization to occur (Hadisoesilo and Otis, 1996). The separation of mating flight times amounts to reproductive isolation between the species which, according to the biological species concept (BSC), is sufficient to accord species status to A. nigrocincta

(Hadisoesilo, 1997).

Few systematists today use the BSC. However, the second key defining characteristic is a difference in drone cells between the species; A. cerana sealed drone cells have a pore in the pupal cap (Hiinel and Ruttner, 1985; reviewed by Ruttner, 1988), while A. nigrocincta drone cells show no such pore (Hadisoesilo, 1997). This concrete and consistent physical difference between A. cerana and A. nigrocinaa is sufficient to give A. nigrocincta species status according to the phylogenetic species concept (PSC)

(Engels et al. in prep). in extensive morphometric and DNA analyses, only one possible exarnple of hybridization was found. Bees from one colony were A. nigrocincta

8 morphologically, but had the mt-DNA sequence of A. cerana (DR.Smith, penonal

communication to G.W. Otis).

1.3 The Uniqueness of Sulawesi

Otis and Hadisoesilo found A. nigrocincru on the island of Sulawesi (previously called the Celebes) in the middle of the Indonesian archipelago (Figure 1). Sulawesi is distinctive in shape; several long ams of land extend in different directions, so that any spot on the island is within 100 km of the Coast. Most of the land is above 500 m elevation (Coates et al. 1997). The island is geologically complex and biologically unique.

Alfred Russell Wallace, an explorer in the Indonesian archipelago in the 1800s, observed two distinct faunas in Indonesia; the one in the West was comprised of mostly

Asian taxa, and the one in the east had predominantly Australian fauna (Wallace, 1962).

Wallace suggested that different islands in Indonesia were at one time joined either to mainland Asia or to Australia. He suggested that the boundary between the two regions was located between Kalimantan and Sulawesi, but later decided that it should be rnoved east of Sulawesi and finally declared that it bisected Sulawesi. With time, the boundary came to be known as Wallace's Line. Located at the intersection of two biotically distinct regions, Sulawesi has a fauna sharing characteristics of both Asian and

Australian faunas (Whitten el al. 1987, p.6 1).

In addition to species resembling Asian and Australian species, Sulawesi also contains many which are endemic. Of the indigenous mammal species found in

Sulawesi, 62% are endemic, including the babirusa, a curly-tusked "pig-deer", and the anoa, a dwarf buffalo (Whitten et al. 1987). Of Sulawesi's land and fieshwater birds,

9 Figure 1. Map showing location of Sulawesi in the Indonesian archipelago. (Map from Whitrnore, 1987).

18% are endemic (Coates et al. 1997). Of the indigenous amphibians, 76% are endemic

(Whitten et al. 1987).

Although much Iess research has been done with on Sulawesi, A. nigrocincta may be among the endemic species found there. A. nigrocincta is widely distributed throughout Sulawesi and on the island of Sangihe to the north. Contrary to a previous report (Otis, 1996), it is not present on Mindanao, the southernmost island of the

Philippines (G.W. Otis, persona1 communication). In contrast to the widespread distribution of A. nigrocincta in Sulawesi. A. cerano has been collected only from the southern tip of South Sulawesi and fiom a small area of Central Sulawesi (Hadisoesilo.

1997). In these two areas, A. cerana and A. nigrocincta are largeIy allopatric with a narrow zone of sympatry.

In areas of sympatry in Sulawesi, colonies of A. nigrocinc~aare found generally above 400 m elevation and A. cerana colonies are found beIow 400 m. In other locations throughout its range, A. cerana is found from sea level to higher elevations, in forests as well as disturbed agricultural areas (Ruttner, 1988). Hadisoesilo and Otis, while timing drone flights of A. cerana and A. nigrocincta in areas of sympatry, noticed a distinct distribution of each species. Nests of A. cerana were found almost exclusively in highly disnirbed agriculhiral areas and villages, but nests of A. nigrocincta were found predominantly in forests (Hadisoesilo, 1997). Honey-baiting experiments confirrned their observations; in the forest, only A. nigrocincta came to plants sprayed with honey water, but at the edge of the forest and beyond, a high proportion of A. cerana bees came to the baits (G.W. Otis, persona1 observation).

1.4 Objectives of Study

11 The obvious dichotomy in the location of these two species raises an intriguing question about the association of each species with different habitats. Do these bees actively select certain habitats? Are A. cerana and A. nigrocincta partitioning resources in areas of syrnpatry? The most obvious resources used by honey bees are food sources and nesting sites. In the following chapters, locations of food sources used by foragers and habitats searched by swmscouts are compared for A. cerana and A. nigrocincta.

The northem edge of Lore Lindu National Park in Central Sulawesi, Indonesia, is one of the locations where both A. cerana and A. nigrocincru are found. Jalan Jepang, a road, abruptly separates forest and disturbed agncultural land. By placing observation colonies and anificial swarms near this ecotone, the dances of foragers and scouts can be interpreted to gain insight into resource use and habitat selection of these sibling species.

Chapter 2 provides a comparison of A. cerana and A. nigrocincta in terms of dance dialects, foraging locations, foraging distances, pollen collection. and time of foraging. Chapter 3 is a comparison of habitat selection by A. cerana and A. nigrocincra swarm scouts. Chapter 4 summarizes the results of my study. CHAPTER 2

DANCE CURVES AND FORAGING BY APIS CERANA AND APIS NICROCINCTA

2.1 INTRODUCTION

2.11 Resource Partitioning

In a generally mutualistic relationship with flowering plants, honey bees gather

nectar and pollen from blossoms while at the same time transfemng pollen from anthers

to stigrnas, thus facilitating the reproduction of the plants. Nectar is later tumed into

honey by the bees in a nest, to provide energy in the fom of carbohydrates for the

colony. Pollen, a rich protein and lipid source, is stored in the hive and is an essential

food for developing brood and young adult bees.

In a single hp, a honey bee almost invariably collects from just one type of

flower (Free, 1970). For example, 99% of the pollen grains in pollen pellets camed by A.

mellijera have been shown to be from the same species of plant (Stimec et al.. 1997). A. cerana foragers also collect one kind of pollen in a single trip and continue to collect it

throughout the day (Naim and Bisht, 1989). Honey bees' floral constancy makes them

well-suited for pollination purposes. At any one time, a hive of bees may be collecting pollen from dozens of different plant species.

Yet not al1 honey bee species exploit the same floral resources. This is partly reflected in geographical variation, because honey bee species or subspecies ofien [ive in allopatric (ie. nonoverlapping) ranges which contain different types of vegetation. In cases of syrnpatry, resources may be partitioned in other ways.

13 For example. resources rnay be partitioned based on size. Oldroyd et al. (1992b) found evidence suggesting that pollen resources were partitioned arnong A. dorsata, A. cerana, A.florea, and A. andreniformis based on bee size. with the larger two species using the richest pollen resources.

Sometimes resources are partitioned when separate species forage at different times of day. In Bhubaneswar, India, A. cerana and A. dorsara were most active on niger plants at 1 1:O0 am. A. florea. in contrast, was more active in the afternoon (Panda et al.

1993).

Daily temporal differences in foraging may be related to temperature constraints.

In apple orchards in India, A. cerana indica and A. nielliféra showed different daily peak times of foraging. A. ceronn indica foraged mostly between 9:00 and 1 1:30 am, when the temperature was between 15.5 and 2 1°C. A. meilifera peak foraging occurred between 1 1 :O0 and 1 :30 pm, when the temperature ranged from 2 1 to 25°C (Verma and

Dulta, 1986; Verma, 1995). A. cerana also began foraging earlier in the moming and ended later in the day than A. meilifera (Verma, 1995).

In addition to different times of foraging, food resources rnay be partitioned spatially. For example, species rnay forage on different strata. Rinderer et al. (1 996) found that A. cerana and A. koschevnikovi in Sabah, , foraged more frequently at the tops of the yellow flame tree (Peltophorum pîerocarpunr) than at the middle or bottom levels. A. dorsata foraged equally at the top and middle of trees, while A. andrenifonnis foraged equally at al1 strata. These results suggest that species demonstrate stratum fidelity. Altematively, nectar and pollen production may be more pronounced at the top and middle of trees, and certain bees (e.g. A. cerana and A.

14 koschevnikovi) rnay competitively exploit the best resources.

Roubik (1993) investigated the stratal associations of 20 bee species from IO genera in Panamanian forests. He found large variation in stratum association; rnost bees foraged at both heights or came consistently to the lower traps. Only two noctumal bee species foraged mainly in the high canopy, and some diurnal species actually seemed to avoid the upper canopy (Roubik, 1993). In the Malayan forest. instead of solitary bees,

A. ceruna, A. dorsola, and a few Trigonu species seemed to be the main pollinators in the upper canopy (Appanah and Kevan, 1995).

Verma and Chauhan (1985) observed insect pollinators on apple trees and found that 40.6% foraged between 2 and 3 m fiom the ground. The rest foraged in roughly equal numbers above 3 rn and below 2 m. The higher numbers on the middle branches may indicate stratified foraging, but altematively may rnerely reflect a greater number of flowers on the middle branches.

Differences in proboscis lengths may be one way in which resources are partitioned between A. cerana and A. nigrocincta. with probosces of different sizes have been found to utilize flowers with corresponding corolla lengths

(Ranta and Lundberg, 1980). In rnorphometric analyses of A. cerana and A. nigrocincla, samples of each collected from locations only 12 km apart had significantly different proboscis lengths (P<0.0001) (Hadisoesilo et cil. 1995). A. cerana had a mean proboscis length of 4.7 16 i 0.063 1 mm, and for A. nigrocincta the mean length was 4.995 * 0.05 12 mm (Hadisoesilo et al. 1995). These two species may handle some of the sarne flowers with differing amounts of ease because of their different proboscis lengths.

Extensive comp~sonshave been made betweenAfricanized and European

15 honey bees, which belong to the same species (Apis nlelliféï-a)and freely interbreed but which are nonetheless geographically distinct races (Pesante et al. 198%). Comparisons of foraging by these two species are of particular interest because of the overwhelming success of A. m. scurellata, the African bee, in South and Central America (reviewed in

Seeley, 1985a). Danka et al. (1990) found only minor differences in foraging flight characteristics between the two races. However, Afncanized bees made more visits for pollen than European bees (Danka et al. 1987; Pesante el al. 1%Va), and Ahcanized bees collected more pollen dunng the dry season (Pesante et ai. 1987a). In addition,

European and Africanized bees may have different diumal foraging strategies; both groups started out with similar foraging patterns early in the moming, but European bees had more foragers for the rest of the day (Danka et al. 1987).

Many other species besides honey bees exploit florai resources for nectar and pollen, and a single species of plant is often visited by many different species of bees. An investigation of Afncan honey bees (A. mellifea scutellato) and native social bees in French Guiana suggested that pollen and nectar sources overlapped by more than

50% between A. mellifra scutellata and two Mefiponu species (Roubik, 1983).

In Roubik's study (1 983), no evidence was found of short-term negative effects on the native Melipona species. But in interactions with other at a floral resource, honey bees tend to dominate (Schaffer et ai. 1979; Schaffer et al. 1983; Rouhik et al. 1986; Wilms and Wiechers, 1997). On Baltimora recta, a flowenng plant in Costa

Rica, A. rnellifra bees displayed flexible foraging behaviour with a wider foraging range and less time spent at each flower than several Temaspecies (Roubik, 198 1). In

Brazil, A. mellifru was found to dominate among social insects at feeding stations, and it

16 responded quickly to changes in food quantities (Martins and Aguilar, 1992).

2.1.2 The Dance Language

One of the reasons for honey bees' dominant role at floral resources is the unique systern they use to comrnunicate with other bees inside a hive. Honey bees communicate the distance and direction of food resources using round and waggle dances (von Frisch

1967). Round dances are used to indicate a close food source, and waggle dances are used when a destination is farther away. During the . a bee on a vertical comb in the darkness of the hive nins in a straight line, then tums and mns in a semi- circle back to the starting point. The bee wags its abdomen from side to side as it performs the straight run, each time circling back to the beginning (von Frisch 1967)

(Figure 2).

The waggle dance conveys to surrounding bees both the distance and direction of a far-away food source. Distance is shown through the length of time it takes a bee to perform the straight-run portion of the dance. The tempo decreases as distance increases; thus, the farther away a food source is, the longer the corresponding straight run will take

(von Frisch, 1955).

In flight, a bee's perception of direction is dependent on the polarkation of light and on the way that light is perceived by the bee. A bee's eye consists of thousands of ommatidia, each one arranged at a slightly different angle (von Frisch, 197 1). Light from the Sun, when seen against the blue sky, is polarized to a certain extent. This means that the light waves are vibrating directionally rather than scattering equally in al1 different directions (von Frisch, 197 1). W photorecepton along the dorsal rim of a honey bee's eye contain analyzers oriented in different directions, each of which is maximally

17 Figure 2. Waggle dances, oriented on vertical comb in order to communicate the direction from the hive of the diagramrned food sources. Square boxes denote location of hive. If a flower is located 60" to the right of the Sun, the dance will be 60" to the right of vertical. If a flower is in the same direction as the Sun, the bee will dance straight up (Figure from Winston, 1987). sensitive when lined up with e-vectors of polarized skylight. Frorn the different outputs of' these analyzers, a bee is able to infer the position of the Sun (Rossel and Wehner,

1987). With its ability to detect polarized light, a bee does not necessarily need to see the sun in order to orient itself with respect to the sun's position; a patch of blue sky is sufficient (von Frisch, 1955).

Ln the waggle dance, a bee transposes an angle in relation to the azirnuth of the

Sun into an angle in relation to gravity. A straight run directed vertically (against gravity) means that the destination is in the same direction as the sun. By the same token, a dance

60" to the nght of vertical denotes a flighr direction 60" to the ïight of the sun (von

Frisch, 197 1) (Figure 2).

Some scientists do not accept the hypothesis that honey bees use the distance and direction information encoded in the dance to locate floral resources (eg. Wenner and

Wells, 1990). However, even Wenner concedes that the dance information can be quantified and interpreted by humans (Wenner et al. 199 1). By observing the waggle dance, measuring the angle of the straight run with respect to vertical, recording the time of day, and timing several dance circuits, one can infer the distance and direction of the resource that was visited by the dancer. The distance, which corresponds to a certain dance duration, varies between races (Gould, 1982) and species (Punchihewa et al. 1985;

Dyer and Seeley, 1991) of honey bees. Because colonies differ in their dance dialects, the specific relationship between distance and dance duration must be calibrated before dance information can be properly interpreted.

2.1.3 Colony Level Foraging

In ecological terms, the ability of a honey bee colony to coordinate individuals by

19 means of the dance allows for effective exploitation of food resources. But exactly what benefit does a honey bee colony gain from colony-level foraging? Surprisingly, cooperation within a hive does not seem to lessen search costs; in one study, recruits actually spent more time searching for patch sites than scouts did! However, recruits consistent1y located patc hes of higher forage quality than did scouts (Seeley and

Visscher, 1988). And although an individual recruit might spend a great deal of time looking for a patch, at the colony level bees very quickly adjust to new food sources.

Seeley ( l985b) has proposed that individual recruits follow three simple "rules": they abandon unprofitable patches; locate new patchrs by following dances; and recruit other bees only to high-quality forage patches. With a small proportion of foragen scouting for new sites and a much larger proportion of foragers acting as recruits. honey bees seem able to balance exploration of new patches with exploitation of nch resources

(Seeley, 1987). In the hive, the "unemployed foragers following dances do not seem to evaluate and selectively respond to those dances indicating the best food resource.

Rather, each bee seems to sample just one dance at random before departing from the hive. Foragers actively exploiting profitable food sources dance more energetically and for longer penods of time than do foragers dancing for poorer resources; the resulting increase in the fraction of dances for a profitable food source reduces recruitment to poorer sites (Seeley, 1995).

Colonies are able to locate food sources in a large area surrounding the hive.

Colonies of Italian bees (A. meIlifera ligustica) in Connecticut were found to have a probability of 0.70 of discovering a forage patch 1000 m fiom the hive and a probability of 0.50 of finding a patch 2000 m away. No bees from the four experimental colonies

20 were observed at a food source 3000 m fkom the hive (Seeley, 1987).

Regdation of foraging seems to occur at a colony level. A colony of honey bees can be described as an information centre (Seeley, 1985b). Assessment of the colony's needs seems to happen indirectly, as forager bees interact with and engage in trophallaxis with receiver bees. The eue for a worker to forage for nectar or pollen may be an inhibitory cue via a negative feedback loop (Camazine, 1993). In fact, protein transfer fiom nurse bees to foragers may very well be the cue conceming a colony's need for pollen (Camazine et al. 1998). A similar hypothesis has been proposed for nectar foragers; upon receiving nectar from receiver bees, they may be able to estirnate the relative sugar concentration of their own patch (Seeley. 1985b, 1986). Thus the patches in which honey bees forage are indirectly evaluated and preferentially exploited in companson to other patches.

2.1.4 Cornparison of Foraging Behveen A. cerana and A. nigrocincta

The similar size and resource needs of A. cerana and A. nigrocincta (e.g. cavities for nesting; pollen and nectar of many species for food) suggest that these species could share similar ecological niches, yet in zones of sympatry they seem to occupy different habitats. Does A. cerana preferentially forage in the disturbed agricultural areas which it seems to preferentially inhabit? Does A. nigrocincta forage in the forest, as we rnight expect fiom previous observations (Hadisoesilo, 1997)?

The nul1 hypothesis of my study is that honey bees do not show habitat preferences when they forage; that is, that they forage indiscriminately with respect to habitat. The alternative hypothesis, suggested by the previously observed distribution of

A. cerana and A. nigrocincta nests in zones of sympatry (Hadisoesilo, 1997) and by

21 results of honey baiting experiments (G.W. Otis, persona1 observation ), is that A. cerana forages in disturbed habitats and A. nigrocincta forages more extensively in forested areas. The nul1 hypothesis is tested by using dance information from colonies of each species to infer natural foraging sites. 2.2 MATERIALS AND lMETHODS

Fieldwork was done with the help of Ar10 Bakker. For this reason, plural

pronouns are used throughout the following Materials and Methods section.

2.2.1 Dance Curves

To calibrate the distance dialects of A. cerana and A. nigrocincfa, we first

established colonies in observation hives and then trained bees out to feeding dishes. We

trained one colony of A. cerana bees to thirteen distances between 5 m and 300 m. We

trained three colonies of A. nigrocincfa bee-,; the first was trained to eight distances

between 5 m and 75 m, the second to eight distances between 15 m and 150 m, and the

third to only two distances. Values from this last colony were not used to calculate the

dance curve.

Feeding dishes contained a 5050 sugar and water solution (von Frisch, 1967) scented with a few drops of either vanilla extract (A. nigrocincta, colony 1) or maple extract (A. nigrocincta, colony 2; A. cerano). Bees were marked at the dishes with a dab of enamel or automobile paint on the thorax, and their dances were timed with a stopwatch upon their remto the hive. We measured 3-1 3 circuits (mean k SD = 8.6 I

1.97), then detemined the average duration per circuit for each dance. We measured 12-

44 dances (mean & SD = 24.9 i 9.35) at each distance.

Mean time per dance circuit was plotted against the distance, and a regression analysis was performed on the data using SAS PROC GLM (SAS, Cary, NC) to find the equation of a line which would best explain the data. A separate linear regression was done for A. cerana between 10 and 25 m, because a visual inspection of the data points

23 when time per circuit was plotted against distance revealed two sections of obviously

di ffering slopes.

A. nigrocincta bees performed round dances up until25 m. Round dances have

not been show to convey distance information as do waggle dances (von Frisch, 1967);

for this reason, dance values could only be plotted when bees were performing waggle

dances at 25 m and beyond. A. cerana bees perfomed a round dance at 5 m but were

doing waggle dances by 10 m, so only dance values fiom 10 m and beyond were used to

calculate the linear regression.

2.2.2 Foraging Maps

To determine approximate foraging locations for bees of each species, one colony

of A. cerana and one colony of A. nigrocincta were set up in observation hives along the

ecotone between forest and disnirbed agricuiturai areas. Each colony was given several

days to adjust to new sumoundings before we staned observing dances. Hives were

located under roofs, about 25 m apart. The open sides of these shelters were blocked off

with cloth to prevent the bees from seeing the sky; if a dancing bee can see blue sky, its

dance is no longer oriented solely with respect to gravity (von Frisch, 1967). We

observed colonies of A. cerana on November 9, 1 1, and 13, 1998, and those of A.

nigrocincta on November 10, 12, and 14, 1998. On each day, we observed a hive for 30

minutes of each hour between 6:00 am and 200 pm. We recorded the number of bees

entering and exiting the hive, both with and without pollen. For bees doing waggle

dances, we tirned circuits using a stopwatch, and measured dance angles using a compass

with a level attached. Throughout the experiments, DMtook al1 dance measurements to eliminate the possibility of variation resulting corn measurements by different people.

24 We scan sampled dances by dividing the comb into several squares and rnethodically

checking each square left to right, from row to row. Between two and eleven circuits

were observed for each dance (mean * SD = 5.1 * 1.57). Occasionally a forager's dance

may have been recorded twice consecutively, for example when a forager danced for a

long time and there was little activity on the rest of the comb. In addition, we observed

dances on only one side of the comb, and therefore rnissed some dances. However,

neither of these considerations is of great concem, because we wanted an estimate of the

fiequency of dancing for different forage sites irrespective of which bee was dancing or how many bees danced.

The A. cerana colony contained approximately 2800 bees. and the A. nigrocincta colony roughly 2200 bees. We noticed queen cells in both hives; the A. cerclna bees did not have a queen and had begun raising a new one. and the A. nigrocincla queen was caged within the colony and was being replaced by the workers. We did not get an estimate of the percentage of comb containing brood in each hive. Estimates of percent cloud cover were made each hour. Weather throughout the six days of observations was similar, mainly cloudy and cool (around 25°C).

We used the mean dance duration and the dance dialect graphs to extrapolate the approximate distance signalled by each dance. To the measured angles, we added the angie of the sun's azimuth at the time of observation. Azimuths were calculated from an astronorny program called "Solar System Live" located on the web

(http://foumilab.ch/solar). Following the rnethod of Visscher and Seeley (1982)' we constructed "foraging maps" to show the approxirnate location of foragers in relation to their nest. We constructed graphs using Sigma Plot, and compared the species in terms of foraging distance, distribution of bees observed dancing throughout the day, distribution of bees entering the hive throughout the day, and colour of pollen collected.

We did not attempt to compare total numbers of flights of foragers from the two hives because they differed in adult populations. 2.3 RESULTS AND DISCUSSION

2.3.1 Dance Curves

Figure 3 shows the dance dialects inferred frorn A. nigrocincta and A. cerana dances. The dance curve we calculated for A. cerana looks similar to that reported for A. cerana by Punchihewa et al. (1985) and by Lindauer (1956, data reported in Punchihewa et al. 1985). The dance tempo of A. cerana was more rapid (e.g. our line is slightly elevated) than that reported by Dyer and Seeley (199 1). Slopes of the lines for A. cerana and A. nigrocincta bcyond 25 m are not significantly different (Anova; P=0.3665). We used a linear least-squares regression on waggle-dance data points to fit the combined A. nigrocincta data from two separate colonies. We used DHO separate linear least-squares regressions for Our A. cerana results (up to 25 rn and beyond 25 m), in order to best fit the data. Obvious outliers (>3 standard residuals) were deleted in order to increase the likelihood of obtaining a best-fit line to be used for extrapolation.

Despite numerous attempts, we were only able to train A. nigrocincta bees to 150 m, yet in constructing foraging maps we had to extrapolate for much further distances

(i.e. dances of longer duration). For A. cerana, the linear best fit regression lines calculated for data fi-orn 0-150 rn and 0-300 m were similar; we assume the same would be true for A. nigrocincta. Although the dialect curve often looks slightly non-linear (von

Frisch, 1967; Dyer and Seeley, 1991), a linear regression fit our data beyond 25 m very well. Other published regressions (e.g. Punchihewa et al. 1985) are also linear. In the absence of information frorn further distances for A. nigrocincta, we assumed that its distance-duration retationship was linear. With other species of Apis, the slope of the

27 Figure 3. Relationship between flight distance and circuit duration for A. cerana and A. nigrocincta in Central Sulawesi. Shown are the least-squares linear regression lines and corresponding equations used to infer flight distance from waggle dances. Enor bars indicate *I SD. One colony of A. cerana and two colonies of A. nigrocincta were used in this analysis. Apis cerana x < 25 m,y = 0.0197 x + 0.99

Apis nigrocincta y = 0.0074 x + 1.26

100 150 200 Distance (metres) dance cuve gradually decreases as the distance from the hive increases (von Frisch,

1967; Gould, 1982; Dyer and Seeley, 199 1 ). If we had been able to train the bees out further, the slope of the line might have decreased slightly, and thus the distance estirnates extrapolated from the dance curve would be somewhm underestimated. Any resulting emor in foraging maps (see below) would be relatively minor, and would only affect the inferred distances, not the directions of food sources.

2.3.2 Foraging Maps

Figures 4-6 show the foraging rnaps inferred from the dances of A. nigrocincta foragers on three different dates. Figures 7-9 show the foraging rnaps inferred from A. cerana dances on three different days.

Both species concentrated their foraging in the area southwest of the cleanng, where cash crops (coffee, cacao) were interspersed among scattered ta11 forest trees

(mixed area). Contrary to the nul1 hypothesis, foraging by these bees, as inferred from their dances, was not randorn. Both bees concentrated foraging to the south and west of the observation hives. A. nigrocincta foraged at a mean angle of 193*, with a mean vector of .59. (The mean vector is an indication of the variance; a mean vector of 1 .O indicates no variation). A. cerana foraged at a mean angle of 2 1Y, with a mean vector of

SB. Lengths of the mean vectors for each species indicate that the probability of a random distribution for each is less than 0.00 1 (Batschelet, 198 1 ).

Four different types of habitats are shown in Figures 4-9: disturbed agriculiural area; forest; mixed area; and a clearing containing corn fields and various trees and bushes. The ratios of foragers of each species in the four habitats are significantly different (X2=43.95;dg3; P=0.01). Figure 10 shows the proportion of foragers in each

29 Figure 4. Map of locations of food resources visited by A. nigrocincta foragers, as inferred from waggle dances in an observation hive on November 10, 1998. 1) primary forest of LLNP; 2) disturbed agricultural habitats; 3) "mixed" habitat; 4) cleanng with corn fieIds. November 10, 1998 Figure 5. Map of locations of food resources visited by A. nigrocirzcta foragers, as inferred from waggle dances in an observation hive on November 12, 1998. 1) pnmary forest of LLNP;2) disturbed agncultural habitats; 3) "mixed" habitat; 4) cleanng with corn fields. November 12,1998 Figure 6. Map of locations of food resources visited by A. nigrocincta foragers, as inferred from waggle dances in an observation hive on November 14, 1998. 1) primary forest of LLNP; 2) disturbed agricultural habitats; 3) "mixed" habitat; 4) cleanng with corn fields. November 14, 1998 Figure 7. Map of locations of food resources visited by A. cerana foragers, as inferred fkom waggle dances in an observation hive on November 9, 1998. 1) pnmary forest of LLNP; 2) disturbed agicultural habitats; 3) "mixed" habitat; 4) cleanng with corn fields. November 9, 1998 Figure 8. Map of locations of food resources visited by A. cerana foragers, as inferred fiom waggle dances in an observation hive on November 1 1. 1998. 1) primary forest of LLNP; 2) disturbed agicultural habitats; 3) "mixed" habitat; 4) cleanng with corn fields.

Figure 9. Map of locations of food resources visited by A. cerana foragers. as inferred from waggle dances in an observation hive on November 13, 1998. 1) primary forest of LLNP; 2) disturbed agricultural habitats; 3) "mixed" habitat; 4) clearing with corn fields. November 13,1998 Figure 10. Proportion of foragers of A. cerana and A. nigrocincto in four different types of habitai at the northem edge of Lore Lindu National Park in Central Sulawesi, as inferred from waggle dances on November 9, 1 1 and 13, 1998 (A. cerana) and November 10, 12 and 14, 1998 (A. nigrocincta). n=number of dances observed. Apis cerana n=382

disturbed clearing mixed forest

0.6

Apis nigrocincta n=305

disturbed clearing mixed forest habitat for A. cerana and A. nigrocincta. A similar proportion of bees of each species foraged in the cleanng and in the mixed area. In the cleanng, most dances by A. cerana indicated the corn fields while most dances by A. nigrocinctu corresponded to nearby cassava bushes. The proportion of bees of each species foraging in the disturbed agricultural area (coklat) and in the forest are obviously different, and are opposite of what was predicted by the altemate hypothesis. A. cevana dances indicated the forest more than A. nigrocincta dances, and A. nigrocincta dances indicated the disturbed agricultural area more than A. cerana dances.

Distribution of a colony's forages certainly depends on the availability of food sources. Honey bees discover and exploit even small resources. and foragers of A. meilfera from very distant colonies are sometimes found foraging on plants (Gary et al.

1980). In Our study, the areas not foraged in may have been devoid of flowers, or they may have contained floral resources less attractive than those in the mixed area.

In a Nonh Amencan temperate deciduous forest, honey bees have been shown to focus their foraging on a few patches at a time and to rapidly switch between resource patches (Visscher and Seeley, 1982). Afncan bees in Botswana. too, continually redistribute to di fferent patches (Schneider, 1989) despite their relative1y small foraging ranges (Scheider and McNally, 1993). Our bees showed a similar pattern, concentrating on a few patches at a tirne but switching rapidly even throughout the course of one day.

Figure 1 1 shows dances by A. cerana foragers, plotted in two-hour intervals. The bees began foraging south of the hive, then switched to areas northwest (corn) and southwest of the hive. In the aftemoon they retumed to foraging south of the hive. Even though bees switched patches rapidly, foraging on al1 days of observation was concentrated in

37 Figure 1 1. Locations inferred fiom dances of A. cerana in an observation hive near the edge of Lore Lindu National Park in Central Sulawesi on November 13, 1998. Dance information is plotted in two-hour intervals to show the rapid turnover in foraging locations. Apis cerana -- November 13, 1998 /\ the same general areas West and south of the hive (Figures 4-9).

One rnust be carefùl when making comparisons between two different colonies of

honey bees. Even two matched colonies of A. rnellifera honey bees, when paired in a

suburban environment, showed very different locations of Foraging (Waddington et al.

1994). The authors suggested that perhaps in the suburban area with abundant small

patches of forage, recruitment via dancing played a reduced role in allocating foragers

among those patches (Waddington et al. 1994). Before general conclusions can be made

about foraging locations, one needs to look at replicate colonies and make observations in

different locations and dunng different times of the year.

2.3.3 Foraging Ranges

Figure 12 shows distance distributions inferred from the dances for each species.

Puring the days of observation, we observed A. nigrocincta to forage farther and over a

wider range than A. cerana. The mean distance indicated by dances of A. cerana was

260 k 1 14 rn (mean * s.e.), while the mean distance from dances of A. nigrocincta was

320 k 186 rn (mean s.e.). The difference between species in distances travelled is

significant (blocked Anova; F=56.40;df=l; P=0.0001). However. there was large

variation among days in mean distance travelled (Figure 13; F= 18.47; de5; P=0.0001 ),

which rneans that results shouid be interpreted cautiously because differences between

the two colonies may merely reflect variation from day to day. Even in the

aforementioned experiment using matched A. mellifera colonies, mean flight distances

differed both between colonies and among days. Maximum flight distances also vaned

(Waddington et al. 1994). Despite large variation in foraging distances from day to day,

A. nigrocincta bees foraged over a muc h wider range th&. cerana during the days of

39 Figure 12. Frequency distribution of flight distances inferred from dances of A. nigrocincta and A. cerana to natural food sources near the boundary of Lore Lindu National Park in Central Sulawesi. Dances were observed November 10, 12 and 14, 1998 (A. nigrocincta) and November 9, 1 1 and 13, 1998 (A. cerana). n=number of dances observed for each species. Apis nigrocincta mean = 324.4 n = 305

Apis cerana mean = 254.8 m n = 382

400 600 Distance (metres) Figure 13. Mean distances inferred from dances of A. nigrocincta and A. cerana near the boundary of Lore Lindu National Park. Each colony was observed for three days; November 10, 12 and 14, 1998 (A. nigrocincta) and November 9, 1 1 and 13, 1998 (A. cerana). Numbers above each bar show number of dances used to calculate each mean. Overall means are also plotted for each colony. Lines above each bar show standard errors of the means. Mean distances travelled

A. cerana A. nigrocincta Species observation; our interpretations indicated that the former danced for distances up to 920

m while the latter only indicated distances of 560 m. These results suggest that A.

nigrocincta has a larger foraging range than A. cerana.

Punchihewa et al. (1985) found A. cerana bees to have a preferred foraging range

of less than 400 m; 70% of dances observed indicated distances less than 400 m. 50% of

A. cerana bees foraged within 195 m in a study by Dyer and Seeley (199 1). while 95%

foraged within 905 m. In Our sîudy, 50% of A. cerana bees foraged within 250 m, and

95% foraged within 470 m (Table 1). No studies had previously been done to determine

the foraging range of A. nigrocincta bees, but Our data indicate that 50% foraged within

358 m and 95% foraged within 656 m (Table 1).

Foraging ranges within a particular race or species may depend in part on clirnatic

factors due to geographical location. In Japan, for example, which has a nonhem temperate climate, Sasaki et al. (1995) found A. cerana japonica to have a foraging range of 1.5 to 2.5 km fiom their hives. This range is larger than the one reported for A. cerana in tropical regions (Punchihewa et al. 1995; Dyer and Seeley. 199 1), but smaller than that for A. meiliferra in temperate regions (Visscher and Seeley, 1982).

We found similar dance dialects for A. cerana and A. nigrocincta in Sulawesi, and yet Our interpretations of dances suggest that A. nigrocincta has a wider foraging range than A. ceranu. The results have implications for Our understanding of the relationship of dance dialect and foraging range. Gould ( 1982) has suggested that the dance dialect of a honey bee species or race directly corresponds to its foraging range, so that a species with a short foraging range would have a steeper dance dialect curve than a species with a long foraging range. This idea is called the adaptive tuning hypothesis (Gould 1982).

42 Table 1. Parameters of distance distribution inferred from dances of Apis cerana and A. nigrocincta to natural foraging sites. Data are from the present study; from a study in Thailand (Dyer and Seeley, 199 1); and from a study in Sn Lanka (Punchihewa er al., 1985). Table shows distance (in metres) corresponding to 50% of inferred foraging range, distance corresponding to 95% of foraging range, and maximum distance inferred from dances. S~ecies 50% (m) 95% (m) Max (m)

A. cerana 250 A. cerand 195 A. ceranaO 140

A. nigrocincta 360

"From data of Dyer and Seeley, 199 1. "Estirnated fkom Punchihewa et al., 1985. However, earlier this decade, Dyer and Seeley (199 1) found three Asian honey bee species to have similar dialects but veiy different flight ranges. Our results are in agreement with their conclusion that the adaptive tuning hypothesis is not adequate to explain the variance among honey bee species both in foraging distance and in dance dialects.

2.3.4 PoHen Collection

Figures 14 and 15 show the relative proportion of pollen of different colours brought into the hives by A. nigrocincta and A. ceraim. The difference in distribution of pollen colours between these species is statistically significant when compared using a

Chi-Squared test (X2=692.26;d62; P=0.001). A. cerana and A. nigrocincta colonies had similar percentages of pollen collectors overall; 8.3% of the A. cerona dances we observed were by bees carrying pollen, and 5.9% of the A. nigrocincta dancers camed pollen. 3.5% of A. cerana bees entering the hive camed pollen, while 2.4% of A. nigrocincta bees observed entering the hive camed pollen. The bright yellow pollen show in Figure 15 corresponded to corn plants in the clearing; I saw A. cerana bees with bright yellow pollen on their legs foraging on corn, and dances by foragers carrying the same colour of pollen indicated the direction and distance to the corn in the clearing.

Although A. cerana regularly collected bright yellow pollen fiom the clearing, A. nigrocincta foragers were only rarely seen with bright yellow pollen, and A. nigrocinctu dances never indicated the corn fields. Why would one species collect this abundant resource while another species hardly seemed to notice it? How do bees decide which pollen to collect? We do not know, and in my studies 1 performed no expenments to address these questions. We do know that A. melliftera exhibits distinct preferences for

44 Figure 14. Relative proportion of pollen of different colours brought into the hive by A. nigrocincta foragers near the northem edge of Lore Lindu National Park in Central Sulawesi on November 10, 12 and 14, 1998. n=number of foragers observed entering the hive with pollen. 0pale yellow bright yellow orange Apis nigrocincta orange yellow Pollen collection E light orange yellow n=307 white bright orange Figure 15. Relative proportion of pollen of different colours brought into the hive by A. ceruna foragers near the northem edge of Lore Lindu National Park in Central Sulawesi on November 9, 1 1 and 13, 1998. n=number of foragers observed entering the hive with pollen. 0pale yellow bright yellow ESSI orange Apis cerana orange yellow E light orange Pollen collection yellow some types of pollen over others. Reasons for these preferences are not clear; they do not seem to be related to pH nor directly to the protein content of the pollen, but may be linked to an odour association. Whatever the case, honey bees, when given a choice between several different types of pollen, landed directly on the dish containing their

"preferred" type of pollen (Schmidt, 1982).

Levels of pollen collection in a colony may be regulated to some extent by genetics. Afncan colonies have been shown to have more pollen foraging activity than hybrid Afncan-European colonies (Schneider and Hall, 1997). High and low pollen- hoarding honey bee colonies have been selected for (Hellmich er ai. 1985). Genetics may have influenced the amounts of pollen collected by my colonies.

Results from an experiment like mine cannot be used to estimate levels of pollen collection, because the amount of pollen collected by a colony of bees varies throughout the year. Pollen availability depends on which pollen-producing plants are in flower

(Kiew, 1995). Pollen collection is a!so related to a colony's interna1 status. For example, pollen collection, amount of stored pollen, and amount of brood in hives of A. cerana iadica were al1 highest during April in Bangalore, India (Reddy, 1980). The proportion of A. rnellifeu scutellato foragers collecting pollen was correlated to the proportion of brood comb in colonies in Botswana, Africa (Schneider and McNally, 1992). Although the colonies we used were of roughly equal size, we did not obtain estimates of the amount of young brood and both colonies were queenless. However, while the amount of young brood may have affecied the amount of pollen collected, it seems uniikely that it would affect the type of pollen collected.

Pollen analyses can reveal much about a colony'sforaging resources. In Surinam, analysis of 97 honey sarnples from 30 locations revealed that a wide range of

species are utilized by honey bees, including some nectarless plants such as Cecropia.

Cecropin and Cocos nucifeu were widely used sources, with pollen from the former

found in 92.8% of honey samples (Kerkvliet and Beerlink, 199 1). Though we did not

identiQ specific types of pollen, out- data shows that each colony seemed to concentrate activities on a different pollen source (Figures 13 and 15).

In the Yucaian, Mexico, 148 species of plants were identified from honey samples

from 22 European and 22 Africanized honey bee colonies. Many of the pollen samples

found in the hmey were from nectarless plants. A mean of 44% of the species were comrnon to both European and Afncanized honey bees. The number of plant species represented by this pollen analysis suggests that honey bees are generalists when it cornes to foraging, yet the data revealed that less than 50% of the plant species were shared between European and Afncanized bees, indicating that the geographical groups were using di fferent resources (Villanueva-G, 1994). Pollen resource partitioning also seems to be true of A. cerana and A. nigrocincta (Figures 14 and 15).

2.3.5 Temporal Resource Partitionhg

The temporal distribution of bees observed entering the hives throughout the day is shown in Figure 16. Each species showed peaks of foraging, with decreased activity in the afiemoon. A. nigrocincta bees were more active early in the moming, but A. cerana were more active in midrnorning. The distributions in Figure 16 are significantly different (D=0.091; Dc=0.0 194 at P=0.0 1) when compared with a Kolmogorov-Srnimov two-sample test. However, Figure 16 shows distributions based on six days of observation in total. Each day's distribution also diffen significantly from the other days

48 Figure 16. Distribution of bees observed entering observation hives throughout the day. Data are from ha1f-hour observations during eac h day light hour (6:OO- 1 8:OO) on three different days for each species: November 9, 1 1 and 13, 1998 (A. cerana) and November 10, 12 and 14, 1998 (A. nigrucincta). Time of day (hours) (P

(Schneider and Hall, 1997). Temporal activity seems to depend largely on factors which may Vary from day to day. The distribution of dances observed throughout the day is shown in Figure 17. A. cerana dancing peaked around 9:00, probably corresponding to the availability of corn pollen. The peak for A. nigrocincta at l3:OO included mostly dances which indicated nearby cassava bushes (Manihot sp.). Immediately after observing dances in the observation hive, 1 ran over and observed the bees foraging frantically in the bell-shaped flowen; they would retum to the hive with their thoraxes dusted with pollen, but they were not actively collecting pollen. Dances in both hives decreased in the aftemoon. The two distributions in Figure 17, compared with a

Kolmogorov-Smimov two-sample test, are significantl y di fferent (D=O. 1 5: Dc=O. 125 at

P=O.O 1). Distributions also differed significantly between some days.

Honey bees depend on plants for nectar and pollen, and plants ofien depend on bees for pollination. Because plants often secrete nectar and dehisce pollen at specific times of the day, it is not surprising to find that foraging activity coincides heavily with availability of pollen and nectar resources. On staghom sumac in Ontario, anthers on male inflorescences dehisce between 10:OO and 1 1:OO. Bees forage for pollen on male inflorescences in the moming, but forage for nectar on female inflorescences during the aftemoon (Greco et al. 1996). On sunflowers in Queensland, A. mellifèra bees collect nectar throughout the day but collect pollen during the morning at times of greatest

50 Figure 17. Distribution of dances observed throughout the day. Data are from dances observed during half an hour of each daylight hour (6:OO-18:OO)on three different days for each species: November 9, 1 1 and 13, 1998 (A. cernna) and November 10. 12 and 14, 1998 (A. nigrocinctn). -Apis ceruna ...... Apis nigrocincfa

11 13 15 Time of Day (hours) pollen availability (Rhodes, 1979). A similar pattern has been found for A. niellifera bees

on sunfiowers in the Transvaal, South Africa (du Toit and Holm, 1992).

Figure 18 illustrates the times during which foragers of A. nigrocincta and A.

cerana were noted entering the hive with pollen. The peak of pollen foraging for A.

cerana occurred between 9:00 and 10:OO am. and for A. nigrocinctcz between 8:00 and

9:00 am. The distributions are significantly different when compared with a

Kolmogorov-Srnimov two-sample test (D=O.ZJ; D~0.116at P=O.O 1). Despite a large

overlap in the time of pollen foraging, there was very little overlap in the coiours of

pollen which were collected.

Daily foraging patterns may be the result of changes in ambient ternperatures. In

apple orchards in India, il. cerana was the most abundant insect pollinator. Peak A.

cerana activity occurred between 1 1 :O0 and 1200 and between 2:00 and 3:OO. when the

temperature was around 22°C. In contrast. several fly species were most active &O0 and

9:00, when the temperature was around 17°C (Vema and Chauhan, 1985). On red

clover, A. mellifea forager numbers peaked in the middle of the day-the warmest part of

the day-when bumblebees were least active (Fussell, 1992). In another study, A. cerana

and A. mellifera also seemed to forage at different times and temperatures; the former

foraged in the moming when temperatures ranged from 16 to 2 1°C, and the latter foraged

at midday when temperatures were slightly higher, from 2 1 to 25°C.

In a study of A. cemna and A. dorsata on peach flowers in India, flight activity of

A. cerana was found to be most significantly correlated with light intensity, but also with

temperature, with solar radiation and (negatively) with relative humidity. Initiation of

foraging in the moming was found to be a function of both temperature and light

52 Figure 18. Distribution of foragers entering the hive with pollen throughout the day. Data are from counts made during half an hour of each daylight hour (6:OQ-18:OO) on three different days for each species: November 9, 11 and 13, 1998 (A. cerana) and November 10, 12 and 14, 1998 (A. nigrocimia). n=number of foragers observed entering the hive with pollen. Apis nigrocincra ipale yellow bright yellow ESSSl orange orange yellow 6 light orange [IIIIIIID yellow fE%iii white bright orange

Apis cerana n=556

14 Time fiours) intensity (Abrol, 1992). In my study (Figures 16, 17, and 18), A. nigrocincta showed

higher levels of activity early in the moming. A. cerana and A. nigrocincta may have

different thresholds for temperature and light intensity. Although we did not record

temperatures, the weather on al1 days of observations was similar. mainly cloudy and

around 25". Table 2 shows the weather information we collected.

In some locations, daily flight activity pattems may depend on the season. In the

summer rainy season in Ghana, A. niel[ifea adansonii foraging activity peaked in the

early moming. During the winter dry season, foraging activity peaked shortly after

sumise and again just before sunset (Woyke, 1992). A sirnilar situation was found in

Botswana, Africa, with A. meIlifera seutellata. Daily foraging activity patterns changed throughout the year, with rnoming and aftemoon peaks during the hot-dry season and more consistent foraging throughout the day during the hot-wet and cool-dry seasons

(Schneider and McNally, 1992). Peak times of flight activity for honey bees in Korea have also been found to differ from season to season. Dunng the spring and fall, activity peaked between 1 1 :O0 and 3:00, but during the summer bees were most active between

8:00 and 9:00 and between 4:00 and 5:00. Diumal foraging activities of these honey bees were more strongly correlated with solar energy than with meteorological factors such as temperature, relative humidity, and wind speed (Lee et al. 1989)

If seasonal variation corresponds in large part to extemal temperatures, as has been suggested (Woyke, 1992; Schneider and McNally, 1992), such seasonal variation in foraging patterns may not exist for A. cerana and A. nigrocincta in Central Sulawesi. In this location, just south of the equator, daily temperatures Vary more than seasonal temperatures (Coates et al. 1997).

54 Table 2. Summary of weather information dunng six days of hive observation near Lore Lindu National Park in Central Sulawesi. A. cerana were observed on November 9, 1 1 and 13. A. nigrocincta were observed on November 10, 12 and 14.

2.3.6 Possible Sources of Variation

Because observations for each of our colonies were made on different days. we must ask whether our results can be explained by day to day differences. Did colonies forage differently because of changes in weather patterns? We estimated wind speeds, noted whether or not rain was falling, and estimated the percent of cloud cover hourly during rach day of observation. We found the weather to be generally cloudy and cool, around 25" (see Table 2).

Another possibility to explain differences in each species' foraging is that availablc resources may have changed fiom day to day. We are confident that resources were not quite so ephemeral; sometimes we knew of a particular resource which we saw on al1 three days in one hive but which we rarely observed in the other hive. An example is corn in the case of A. ceranu; similar bright yellow pollen was oniy brought in by a handful of A. nigrocincta foragers.

In addition to the factors which have been discussed, foraging behaviour is likely to be influenced by many factors which were beyond the scope of this experiment. These factors ought to be mentioned simply because they may have influenced the foraging behaviour of the bees we studied. For example, genes can influence foraging behaviour.

Genetic differences between groups of honey bees may mean that the individuals in each group will display different responses to the same situation.

Genetic differences between patrilines can influence the types of plant species which they utilize (Oldroyd et al. 1992a) or the distance from the hive at which they prefer to forage (Oldroyd et al. 1993). Genetic differences also exist in the arnount of pollen collected by a colony. Page et al. ( 1995) manipulated colonies and found striking

56 differences in pollen collection in the resultant strains of honey bees; high-strain colonies collected an average of six times more pollen than low-strain colonies. Interestingly, hybrid colonies stored more nectar than either the high- or low-strain pollen collecting colonies (Page ef al. 1995).

2.3.7 Resource Use and Resource Preferences

Cornparison of foraging data for A. cerona and A. nigrocincia reveals some subtie differences between the two. Yet patterns of resource use (i.e., ecology) are not necessarily correlated with resource preferences (i.e., behaviour) (Singer and Thomas,

1992). There are several reasons why this might be so. First, a certain pattem of resource use could be produced by more than one preference distnbution. For exarnple, a few individuals in a population may prefer a certain resource while the majonty have no preference. Second, variation in resource use may result from variation in the resources individuals encounter and perceive, rather than variation in preference. Third, other factors which may affect spatial distnbution of individuals could also affect their use of resources-regardless of preferences. And finally, preferences may be conditional and may change "in response to resource availability, population density, or resource use by other members of the population" (Singer and Thomas, 19%). These suggestions deserve closer inspection.

1) What pattem of resource use could have produced the distribution we observed? The foraging maps were constmcted based on dances observed in the hive.

Thousands of foragers were observed entering the hive throughout the day, but the nwnber of dances observed in a day was closer to a hundred. Even taking into account the fact that foragers make repeated trips during a day, it seems reasonable to assume that

57 not al1 of the foragen who retumed to the hive danced for their particular patch of forage.

It may be that only the bees on extremely profitable patches danced. Some bees from the hive may have been visiting patches of forage which they did not advertize using dances.

2) What kind of variation might individual honey bees encounter and perceive in foraging patches? Perhaps most of the flowers in bloorn, or at least the most profitable ones, were found in the area west and southwest of the hive where dances indicated the bees concentrated their activity. Or perhaps the wind patterns favoured that location; odor cues are very important to honey bees (Werner et al. 199 1 ). We estirnated wind speed each day and did not find it to be very strong, but we cannot discount the possibility that it may have influenced foraging (Table 2). A third possibility is that the bees were exhibiting flower fidelity, foraging on the same kinds of plants they had foraged on in the village before we moved them up to the station. Flower fidelity has been demonstrated for A. mellifea bees in a Wisconsin apple orchard. The bees collected more pollen from oak uees around the perimeter of the orchard than from the apple flowers within the orchard. The colonies were originally located in an area surrounded by oak trees (Severson and Parry, 198 1). Our colonies were originally located in the village of Kamarora several kilometres away, but we have no indication of what they foraged on in the village before being moved.

3) Cornpetition with other bees nesting in the area might have influenced the distribution of foragers. But in the forest, A. nigrocincta is abundant, as determined by honey baiting (G.W. Otis, persona1 observation). Besides, a large feral colony of A. nigrucincta was later found in a fallen log in the mixed area where most of our bees seemed to be foraging, and a managed colony of A. cerana bees was located in the

58 middle of the cleanng, so that cornpetitive exclusion seems very unlikely.

4) Preferences may indeed depend on resource availability, population density,

and resource use by other bees. Each of these parameters was beyond the scope of my

study. Funher studies in different locations could help begin to sort out these parameters.

2.3.8 Conclusion

The nul1 hypothesis that honey bees forage randomly among habitats was

rejected. The alternative hypotheses that A. cerana preferentially forages in disturbed

agricultural areas and that A. nigrocincta forages mainly in forested areas in zones of

sympatry were also rejected. Both species foraged in disturbed agricultural areas, forest,

mixed areas (between forest and disturbed agricultural land), and in a cleanng which

contained corn, scattered trees and shnibs. Both species foraged mainly in mixed area

and in the clearing near the hive. Results are in strong contradiction to expectations

based on the observed distribution of nests of these species (Hadisoesilo, 1997) and on

the results of honey baiting in the forest (G.W. Otis, persona1 observation). It is unclear

if the species were foraging in particular areas as a result of habitat preferences or if,

alternatively, the best plant resources available during the days of observation happened

to be in the mixed area and the ciearing.

We can see some differences in foraging between A. cerana and A. nigrocincta.

These differences must be interpreted with caution, and cornparisons will have to be

repeated with more colonies before fim conclusions cmbe drawn. The most strikrng

result of our foraging study, however, is the similarity in the locations where each species

foraged. The results of our foraging snidy do not help to explain the originally observed distribution of these bees, with A. cerana inhabiting disturbed agicultural land and A.

59 nigrocincta living in the forest. THE INFLUENCE OF HABITAT ON NEST SITE SCOUTING BY SWARMS OF APIS CERANA AND APIS N?GROCIIrVCTA

3.1 INTRODUCTION

3.1.1 Swarming Behaviour and Nest Site Selection

The selection of a new home by a honey bee swarm is unique in that it is a

decision involving the whole colony and the decision process can be observed directly.

Scouts locate up to several dozen potential nest sites and advertize them via waggle

dances on the surface of the swarm. Gradually one site gains in popularity, until finally

the colony collectively decides on a location and the dancing bees al1 indicate the same distance and direction (Lindauer, 1955). At this point, scout bees retum to the swarm cluster and some of them engage in excited "buuing mns" through the swarm (Seeley er al. 1979). Just before lift-off, a swarm seethes with activity. Seconds after the first bees take to flight, the entire swmis airborne and moves quickly in the direction of the new nest site (Seeley et al. 1979).

Somehow, a swarm composed of thousands of individual bees cornes io consensus on a location. Lindauer (1955) was one of the first people to describe the events preceding occupation of a cavity by a swarm. According to him, when more than one site was being "advertized", scout bees of a particular site were often persuaded by dancers to visit and subsequently to dance for an altemate site. Gradually al1 the scouts danced in agreement. According to Lindauer (1955), this direct evaluating behaviour by individual bees was confinned again and again in his experiments.

61 More recently, Camazine et al. (in press) have argued that a direct cornparison of nest sites by individual bees does not seem to be the mechanism by which consensus is reached. Rather, the process seems to include positive feedback within a colony by scouts who have found good nest sites and a corresponding gradua1 reduction in recniiting activity by scouts from poorer sites (Camazine et al. in press).

Honey bees sornetirnes travel several kilometres to a new nest site. How far a colony travels to a new nest site likely depends on several factors, including local availability of nest sites and particulars of the individual colony. Scouts from Ahcan and Ahcanized hybrid colonies in northwestem Costa Rica which were set up in artificial swarms recniited fellow bees to nest sites an average of 3.5 km away. Final destinations of the swarms averaged 4.7 km fiom the original location. The colonies recruited to nest sites over an even wider range of distances (Schneider, 1995). Although honey bees may have a preferred distance when selecting a new nest site, they may have different criteria for an acceptable distance; when honey bees in New York were induced to swarm and then given a choice of nest boxes either 20 or 400 m from the swarm cluster, the bees preferentially chose the near nest site four out of five times (Seeley and

Morse 1977).

Numerous studies have been performed to detemine cnteria for nest site selection in honey bees. Seeley and Morse (1978) showed that Apis meilfera honey bees in New York, when given a choice, had distinct preferences for certain nest heights, enûance areas, entrance positions, and entrance directions. These results were obtained for bees of mixed European ancestry in a temperate ciimate. Naturally occumng colonies of Apis mellifea scutelluta in the Okavango River Delta in Botswana chose top

62 entrances over bottom ones, in contrast to bees' preference for bottom entrances in Seeley and Morse's study (Schneider and Blyther, 1988). The honey bee popuiations in the bvo studies demonstrated different preferences for certain aspects of their nesting sites.

For A. mellijiera, we know of several cues which are important in terms of the actual nesting site. These include the size, location. and direction of the entrance; the volume of the cavity; the distance to the nest site; height off of the ground; and evidence of previous occupancy (e.g. cornbs) (Seeley and Morse, 1978). These preferences for aspects of the nest site differ among races of honey bees (Jaycox and Parise, 1980, 198 1) and no doubt also among honey bee species.

We have evidence suggesting that honey bees evaluate various attributes when inspecting a specific nesting site. But what about on a larger IeveI? Do honey bees also evaluate and select particular habitats before they select nest sites?

In the pages following, 1 briefly discuss habitat selection and give examples of studies which have been done to investigate habitat selection by various groups of insects. T'en 1 return to the topic of honey bees and habitat selection.

3.1.2 General Overview of Habitat Selection

Habitat selection occurs at many levels, by animals with differing levels of awareness about their environment. Most previous habitat selection studies have been done with relatively large vertebrates such as birds (e.g. Cody, 1985). However, some studies demonstrate that even insects seem "choosy" about what kind of habitat they [ive in (Whitham, 1980; Evans, 1982; Evans 1983; Howard and Harrison, 1984). How do insects select habitats? What cues do they use, and how do they recognize these cues?

Why do insects select specific habitats? More particularly, how do honey bees select

63 specific habitats?

Before 1 try to address these questions, 1 will try to clan@ a number of concepts and answer a more general question: what is habitat selection?

Habitat is a tem used to describe the area in which an lives. More specifically, habitat is "the conglomerate of physical and biotic factors which together make up the sort of place in which an animal lives" (Partridge, 1978). Fretwell and

Lucas (1 970) narrow the definition even more, defining habitat as an area "essentially homogeneous with respect to the physical and biological features which we believe to be rnost relevant to the behavior and survival of the species". Just what constitutes a relevant feature of a particular habitat rnay Vary widely from species to species. In addition, we can distinguish between levels of habitat, such as microhabitat and rnacrohabitat. Habitats rnay change over time, and time itself (time of day, for example) rnay be a critical feature of an organisrn's habitat (Partridge, 1978).

Habitat selection rnay be defined as "the process by which animais actively choose habitats in which they will conduct particular activities" (Stamps, 1994). Habitat preferences ca~otnecessarily be inferred from the observed distribution of a species among potential habitats (Fretwell and Lucas, 1970). Competition, for example, rnay greatly affect distibution (Paruidge, 1978). Competition and other factors will be examined in more detail later in this chapter.

We might start out by asking what stimuli influence an animal's choice of a place to live. What kinds of cues does an animal use to "recognize" a certain habitat? Cues rnay be varied. They rnay be biotic or abiotic; direct or indirect; or some combination of these. For example, in a study of Bembidion obtusidens beetles near a saline lake in

64 west central Saskatchewan, the beetles used a specific but indirect biotic cue. These

beetles were attracted to volatiles fiom mats of blue-green algae. Apparently the beetles

relied on the presence of these organisms (in addition to temperature, humidity, and other

physical cues) to help them locate their habitat (Evans, 1982).

Another indirect cue may be the presence of conspecifics, because presumably

members of the same species have similar habitat requirements (Stamps, 1994). The

presence of conspecifics indicates that the species' most critical habitat requirements have

been met (Stamps, 1994).

Some environmental stimuli may provide direct cues about habitat to individuals.

In a study involving several species of carabid beetles in central Europe, Thiele ( 1 977)

demonstrated the importance of specific environmental cues in segregating the beetles.

Through a series of experiments measuring orientations of many species to different

gradients of temperature, humidity, and light, "preference indices" were detennined for

each species. A comparison of responses among many different species of carabids

showed that European forest-inhabiting carabids preferred cool temperatures, high

humidity, and low light intensities (Thiele, 1977). These results may seem intuitive when we consider that forests tend to be cool, damp, and dark, but a closer look leads to some

interesting conclusions. Field inhabiting carabids, in a similar comparison, moved toward warmer temperatures but were evenly disûibuted over a humidity gradient and were indifferent to light levels (Thiele, 1977). Thus we see that the latter carabids only responded to one factor (temperature), but forest carabids responded to al1 three.

Nicrophoms amerkanus, the Amencan burying beetle, may require a combination of specific environmental factors for maximum survival. The beetles were

65 found to have much lower breeding success in grasslands than in the forest, and yet prerequisites for breeding seemed to include deep soil in addition to forest. Burying beetles bury animai carcasses in which they lay eggs, and since N. americanus is the largest burying beetle, it requires large carcasses. Although it appears indiscriminate of both habitats and carcasses for feeding, breeding requirements may be much more specific (Lomolino and Creighton, 19%).

Even when several environmental stimuli are important to an insect, one of the stimuli may assume greater importance than the others. Agonum assimile is a carabid found in cool, moist forests. When given a choice between a cool, dry environment and a warrn, moist environment, A. assimile rnoved toward the cool and dry area, dernonstrating a higher preference for optimal temperature than for optimal humidity

(Thiele, 1977).

In addition to environrnental cues, behaviour can play a large role in segregating groups of insects so that their niches do not overlap. Two carabid beetles, Abax ater and

Abar parallelus, are morphologically nearly identical and have the sarne gradient responses to temperature and humidity. However, their brood care behaviour is markedly different and serves to segregate thern. Females of A. ater lay eggs in clay cocoons, then leave them. If clay is not present, eggs will not be laid; thus clay is an environmental necessity for this species. Females of A. parallelus, in contrast, lay eggs in the ground and guard them. For A. purallelus, uniform soil humidity is essential (Thiele, 1977).

1 know of no evidence to suggest what cues or environmental stimuli might attract honey bees to specific habitats. Does the presence of conspecifics play a role? Important habitat indicators could include temperature, hurnidity, light intensity, vegetation (e.g.

66 plant volatiles), or availability of resources.

We have briefly discussed the possible role of cues in habitat selection by insects.

A logical next question is: how do insects know what cues are important? How do they know what to look for?

The question leads us to consider the respective roles of leaming and of genetics.

In a senes of experiments using laboratory-reared and field-caught prairie deer mice

(Peromysm maniculatus bairdi) and woodland deer mice (Peromyscus maniculatus gracilis), Wecker (1964) demonstrated that the mice chose their environment as determined by their heredity. Early field experience could reinforce habitat selection, but it was not a prerequisite and it could not ovemde hereditary affinity (Wecker, 1964).

It seems clear that insects, too. have predispositions to certain types of habitat.

Howard and Hamson (1984) used two different species of ground crickets, Allonernobius allardi and A. fasciutus, to investigate habitat preferences. A. allardi was typically found in dry pastures, while A. fasciatus was found primarily in wet pastures. Reciprocal transplants showed that each species could swive and reproduce in either habitat.

Howard and Hamson collected large numbers of each species and released them into the centre of 1 112 m by 30 m runways which contained wet pasture on one end and dry pasture on the other end. A. allardi were released in two runways, A. fasciatus were introduced into two more, and both species were released simultaneously in a remaining two runways. In each treatment which included A. fasciatus, the crickets moved fiom the midpoint of the runway to the wetter area on one end, showing a distinct preference for wet pastures. A. allardi showed no tendency to move either towards the wet or the dry end of the runway; the majority of the crickets stayed in the middle, and some moved in

67 each direction toward the wet and dry ends. While the experiment showed a preference

by A. fasciams for moist areas, the experiment gave no evidence to indicate whether the

tendency was genetic in nature or a result of earlier conditioning (Howard and Harrison,

1984).

Some evidence of a genetic predisposition for nest site selection has been

presented by Jaycox and Panse (1 980, 198 1). They presented Italian honey bees (Apis

meIlfera ligustica) and black-bodied honey bees (A. melIfera caucasica and A. nieIlfera

camica) with nesting cavities of different sizes and found significant differences in the

size of cavities which the bees would accept (Jaycox and Parise, 1980, 198 1). ltalian

honey bees, given a choice berneen hives with volumes of 5.2. 13.3, and 24.4 litres,

chose cavities with a mean volume of 19 L (Jaycox and Parise, 1%O), while black-bodied

honey bees, given a choice between nest cavities with volumes of 13.3, 24.4.43.5, and

85.1 litres, chose cavities with a mean volume of 45 L (Jaycox and Parise, 198 1).

The question of why animals, and more specifically insects, choose certain

habitats is extremely difficult to answer. The factors involved in habitat selection are

varied and, in many cases. poorly understood. In addition, species Vary so much in their

natural histories that generalizations are bound to fa11 short. Nevertheless, in our attempt

to understand ecology, certain broad principles have become accepted. Sorne of these

principles invite a closer look. In asking why a certain species might select one type of

habitat over another, we briefly discuss the role of environmental factors and the role of

social factors.

In studying the relation of an organism to its environment, the dominant approach used has been an economic one, identifying activities in terms of costs and benefits. The

68 'quality' of a habitat is described in terms of the expected fitness of m individual in that habitat in the absence of conspecifics (Stamps, 1994). Costs, which may include the danger of predation and the energy expended searching for habitat, are weighed against benefits, such as access to food resources and to mates (Stamps, 1994).

The economic approach has permeated discussions of habitat selection. But

Stamps suggests that this was not aiways the case. Scientists have also discussed the concept of a "rnultidimensionality niche", a complex and diverse set of factors which are used to try to determine whether or not a species can survive in a particular habitat and what the relative fitnesses of individuals are in different microhabitats. The approach, with its emphasis on diverse and complex factors, does not translate well into testabie models of habitat selection and has been replaced by the economic mode1 (Stamps,

1994). But in Our attempt to simpliQ and elucidate what we study by using models, we have narrowed Our vision of the very world we seek to understand.

Within its particular habitat, an individual is almost certain to corne into contact with conspecifics and with individuals of other species. In each case, the most common way of analyzing the interrelationships of individuals (whether of the same or different species) has been in terms of competition (Stamps, 1994; Partndge, 1978). Rosenzweig

(198 1) defines interspecific (between species) competition in the following way: "Two species compete if and only if the sum of their equilibriurn densities is less than the sum of their carrying capacities, at least partially because each depresses the other's net per capita reproductive rate, at least at some density combinations". So even if competition is not dominant at every density, it will overall reduce each species' density (Rosenzwieg,

198 1).

69 What role does competition play in habitat selection? How important is

competition in relegating species to particular habitats? Contrary to much popular

theory, Shorrocks et al. (1984) argue that even when competition is present, it need not

be "a major organizing force in community structure". Their modelling of population

dynamics of wild Drosophila populations suggested that a spatial parameter was more

important in determining global coexistence than a competition coefficient; even when

intense competition was present and resources were not partitioned, Drosophila species

did not exclude one another.

"Habitat shifi" is the idea that competitor niches diverge as a result of

coevolution. Conne11 (1980) challenges this common theory about interspecific

competition. In order to conclusively illustrate this kind of habitat shift between two

species, he says. one must show several different things. 1 ) Show that two species have

diverged in their respective use of resources. This is difficult to show conclusively

because observations must be made both before and after the species corne in contact

with each other. Mere observations of allopatric and sympatric populations may be

confounded by differences in their respective environments. 2) Show that divergence

was caused by competition rather than some other event. This could be shown by

manipulating the distribution and abundance of one or both species and anaiyzing the

effect on each species. The challenge here is to detemine which resource dimension(s)

is/are affected by competition. And even if two species do utilize the same resource, they do not necessarily compete for that resource. The main problem, in a nutshell: "Can ecologists judge availability as the organisms do?" (ConneIl, 1980). 3) Divergence must be show to have a genetic basis, so that even if one competing species was removed, the 70 other wouid not completely take over the first's habitat. Field experirnents have not yet

answered these questions conclusively (Connell, 1980).

Although competition has been studied extensively and is regularly proposed as a

key means by which organisms settle into particular habitats, evidence suggests that

cornpetition in insects fùnctions on a much different level. In fact, cornpetition may play

no discemible role in certain insect species. In general, phytophagus species do not seem

to compete for food (Lawton and Hassell, 198 1).

In a study of habitat segregation in ground beetles, Howard and Harrison (1984)

found no evidence of interspecific cornpetition. However, they comment titat "in every

investigation involving social insects, convincing evidence of intenpecific competition

has been found" (Howard and Harrison, 1984). They suggest that in social insects,

interspecific competition rnay help regulate populations and may also be due in part to resource specialization (Howard and Hamson, 1984).

Even if evidence for competition has been found among insects, the tendency is towards asymmetrical cornpetition, in which one species is affected and the other is apparently impervious to the other. In a review of field evidence for insect competition,

Lawton and Hassell (198 1) reported only five cases of reciprocal cornpetition, but listed

23 examples of asymmetrical competition. "For insects in natural conditions," they stated, "strongly asymmetrical competition ... is the nom rather than the exception by a ratio of at least 2: 1" (Lawton and Hassell, 1981). Asymmetrical competition would have a significantly different effect on the dynamics of species interactions than reciprocal competition.

An exarnple suggesting asymmetrical competition has been described for larvae

71 of two Rhyacophila species (Trichoptera: Rhyacophilidae) in southem Ontario streams.

The two species of caddisfly have asynchronous life cycles which make their

distributions non-overlapping throughout most of the year. But during a penod in which

the Iarvae of the two species were morphologically similar and were found in an area of

sympatry, Rhyacophila melita had a significant microhabitat shifi while R. fimula

showed no change in microhabitat use (Martin, 1985). Similar evidence of asymmetric

interspecific interference was presented for larvae of the riverine dragonfly

Onychogomphus uncatus in the presence of other dragonfly larvae (Suhling, 1996).

In a mountain stream in France, two other species of caddisfly (R. evoluta and R.

intermedia) each have fourth instar larvae which are nonnally found in fast currents. The

larvae are similar in size, behaviour, and diet. When the species were in the sarne

geographical area, however, the larvae of R. evoluta were found in slow currents instead

of fast currents. These results suggest that competition from R. intermedia changed the

distribution of R. evoluta (Lavandier and Cereghino, 1995), yet another example of

asymmetrical competition.

In a study of two species of bumble bees (Bornbusflavifons and B. tujocinctus)

in which the species' flower choices were compared in allopatric and syrnpatric

situations, evidence suggesting asyrnmetric competition was also found (Bowers, 1985).

Occasionally interspecific and intraspecific (within species) competition are

found in the same system. In a riverbed in the Namib desert, two species of diurnal tenebrionid beetles, Onymacris mgotipennîs rugatipennis and Physdesmia globosa, are

found in the same open sandy environment. The species are similar in size, food preference, and distribution. 0. r. rugatipennis is most often found in the open sand,

72 while P. globosa is most abundant in the shade under Acacia trees which are sparsely interspersed throughout the landscape. When P. globosa were removed from under the trees by pitfall trapping, they were replaced by more P. globosa, presumably from the open area. It seems that P. globosa beetles experience intraspecific competition for habitat under Acacia trees, and that P. globosa beetles which "lose" and are driven into the open engage in interspecific competition with O. r. nrgatipennis (Ward and Seely,

1996).

What conclusions can we make about habitat selection in insects? The safest generalization seems to be that it is nsky to generalize! Despite the diversity among insects, however, it does seem as though insects sometimes choose habitats.

Habitat preferences are often based upon specific environmental stimuli. Indirect cues, such as the volatiles from mats of blue-green algae for beetles (Evans, 1982), are of particular interest. Without an understanding of which indirect cues are important for a species, alteration of an apparently independent aspect of the environment could have a huge detrimental impact on that species.

Little is known about how insects recognize appropriate habitats, and studies similar to Wecker's mouse experiments (1964) to compare the role of leaming and the role of genetics would yield important information in this area. Because of the reiatively short life span of most insects, one might expect habitat preferences to be inherited raiher than leamed, but field experiments are needed to investigate the question in a concrete manner.

Habitat selection in insects does not necessarily coincide with curent general ideas about habitat selection. In particular, the role of competition in habitat selection by

73 insects has linle support in scientific literature except for in social insects and a few other insect species (Howard and Harrison, 1984). Thus the dynarnics in habitat selection among insect groups can be expected to differ significantly from the dynarnics of larger, more-studied animais. The role of cornpetition among social insects remains a topic of interest.

3.1.3 Honey Bees and Habitat Selection

In areas of syrnpatry in Sulawesi, A. cerana and A. nigrocincta seem to nest in different habitats, with A. cerana occupying nest cavities in disturbed agricultural areas and secondary areas, and A. nigrocincta found mainly in forests (Hadisoesilo, 1997). In

Peninsular Malaysia, a similar situation has been observed between A. koschevnikovi and

A. cerana, with the former located in wet pnmary forest and the latter found typically in secondary growth, agricultural areas, and urban locations (Otis, 19%).

In the Hindu-Kush Himalayan region of Nepal, A. ceruna is facing a serious decline in numbers. Verma (1 993) attributes this decline in part to habitat alteration; as land is deforested and converted for agricuiture, there is a conesponding vast reduction in the species diversity of the flora. At the same time, many of the main crops planted

(among them nce and wheat) do not produce nectar and are of little value to honey bees.

As more land is tilled for agriculture, honey bees may no longer be able to find suitable micro-habitats for nesting sites (Verma, 1993).

In Sulawesi, too, forested land is gradually being pianted with cash crops. The impact of these activities on A. cerana and A. nigrocincta may differ for each species if they do indeed preferentially choose nest sites in disturbed agricultural areas and in forested areas respectively. Our nul1 hypotheses are that colonies of A. cerana and A.

74 nigrocincta select nest sites in a random manner with respect to habitat. Our alternative hypotheses are that A. cerana preferentiaily selects nest sites in disturbed agicultural areas and A. nigrocincta chooses nest sites in the forest. 3.2 MATERIALS AND METHODS

Fieldwork was done with the help of Ar10 Bakker. Plural pronouns are therefore

used throughout the following Materials and Methods section.

Dunng several weeks at the end of November and begiming of December, 1998,

we set up individual swarms along the ecotone between forest and disturbed agricultural

land. On each occasion, we caged the colony's queen and hung the cage fiom a

clipboard tied to a large tree root. We shook the rest of the bees out of the hive; they

soon clustered around the caged queen. Typically within a few hours, we could see

dances on the surface of the swam.

Beginning several hours after the swarm was set up, we watched for dances on the

surface of the swarm for half an hour of every hour during daylight hours (6:00 to 18:OO).

We continued watching until agreement on a cavity had been reached and the swarrn

lified into the air. We scanned the top, middle, and bottom of the swarm systematically

from lefi to right, stopping when a dance was observed in progress. We measured the

angle from vertical of each dance using a compass with a level attached, and we timed

several circuits using a stopwatch. Once again, we used the stopwatch information and

our dance dialect graphs (Figure 3) to extrapolate the approximate distance

conesponding to each dance. To the angles we had measured, we added the angle of the

sun's azirnuth at the time of observations. Azimuths were calculated using the astronomy

program "Solar System Live" located on the web (htt~://foumilab.ch/solar).Maps were constructed following the method of Visscher and Seeley (1982).

We fed each colony a 1: 1 (by volume) sugar and-water solution for a period of

76 several hours to several days before we created an artificial swarm from it, so that the bees would be engorged with food. We assumed dances were by bees scouting for nest sites rather than by foragen, unless a bee was canying pollen or imrnediately engaged in trophallaxis upon retum to the swarm.

In total, we observed seven swarms of A. nigrocincta bees and five swarms of A. cerana bees; some of the swarms were From the same colony but each used bees which had not previously been hung as a swarm. We estimated the surface size of the swarms by measuring the height and width. Table 3 presents a summary of the swarms we used.

The fint two swarms we studied were placed in the open. Dances by bees which can see blue sky are oriented both with respect to gravity and to the actual location of the

Sun; polarization depends on the position of the Sun, and bees can discem the polarization of light from blue sky (von Frisch 1967). Our observations were made on days which were mainly overcast, but bees fiom these two swarms may have been able to see blue sky. Results for these two swarms must be interpreted with caution. For al1 succeeding swarms, we blocked the bees' vision of the sky using cloth and an umbrella so that dances would be oriented only with respect to gravity.

We set out ten trap hives at equidistant positions in a circle of radius 150 m around the swam location, so that even if there were no natural nesting sites, nest sites would still be available in al1 directions. The trap hives were made of reinforced wood pulp with molded lids which fit into the top, as described in Schmidt and Hurley (1995).

Each had a 3 cm diarneter entrance hole at the bottom and had an inner volume of 24 L

(Schmidt and Hurley, 1995). We hung each trap hive fiom the branches of a tree. To protect the trap hives fiom rain, we covered each with a square of plastic draped

77 Table 3. Summary of swarms used for swarming study near Lore Lindu National Park in Central Sulawesi, including swarm origin, date used, and surface area of swarm. Swarrn Summarv:

Apis nigrocimta Swarm Origin Date Surhce Size of Swarm (cm2) # 1 Hive bought by owner four months previously 1 1/17/98 #2 From same colony as # 1, but different workers and queen 1 1/23/98 600 #3 Hive from Bobo (25 km away) 12/05/98 225 #4 Hive from Rahniat* 12/09/98* 216 #5 Established colony from Rahmat 1 2/09/98 180 #6 Same colony as #5; same queen but di ffereiit bees 1 21 10198 196 #7 Same colony as #5; sarne queen but different bees 12/11i98 132

Apis ceratta Swarm Origin Date Surface Size of Swarm (cm2) #l Collected as swarni 1 1/18/98 600 #2 Collectcd as swami 1 1 120198 150 #3 Colony hived from wild nest tiiree weeks previously 1 1/25/98 400 #4 Established colony 1 1/28/98 50 #5 Colony hived from wild nest two days prior 12/04/98 180

*colony dequeened three months earlier, then inerged with a swami diagonally over the top so that the corners hung down and formed drip tips. We smeared petroleum jelly around the wires to deter ants. We inspected the pulp hives every second day to check for damage or occupancy (Table 4). Where ants had gotten in. we took the hive down, brushed it out, repositioned it. and then reapplied petroleum jelly.

A11 of our trap hives were placed in shaded areas, except for #9 (Table 4) which was hung in a clearing on the only available tree in the vicinity. While honey bees are able to regulate the temperature within a hive with arnazing precision (Seeley, 1985a), they seem to carefully select nest sites which have adequate sheiter From the hot Sun

(Seeiey and Morse, 1978). Table 4. Location of trap hives and comments on damage and/or occupancy of each hive during swarming experiment near Lore Lindu National Park in Central Sulawesi.

3.3 RESULTS AND DISCUSSION

Figures 19 and 20 show the approxirnate locations of nest sites scouted by A.

cerana and A. nigrocincta, as inferred from waggle dances we observed on the surfaces

of swarms. A. cerana seemed to scout somewhat indiscriminately in both forest and

disturbed agricultural area. A. nigrocincta scouted for nest sites mostly in the disturbed

agncuitural area north of the swarm.

Figure 2 1 indicates the approximate distance and direction of the sites agreed

upon Dy A. cerana swarms. Six destinations are shown for A. cerana in Figure 2 1,

because we did not see a consensus among the bees from the second A. cerana swarm.

Dotted lines show the two locations which correspond to the final dances on this swarm

before the bees took to the air. In contmst to Figure 19, al1 the sites which were agreed

upon by A. cerana were in the disturbed agricdtural area. Sometime between the start of

scouting and the selection of a nest site, a decision seems to be made in tems of habitat.

Our nul1 hypothesis that A. cerana bees select nest sites in a random marner with respect to habitat was disproved; results are consistent with our altemate hypothesis that A. cerana preferentially select nest sites in disturbed rigricultural areas in this zone of syrnpatry with A. nigrocincta. Results are also consistent with previous observations of the location of A. cerana nests (Hadisoesilo, 1997).

Figure 22 indicates the approximate distance and direction of sites agreed upon by

A. nigrocincta swarms. Eight locations are shown in Figure 22 because scouts fiom the last A. nigrocincicl swmdanced for two different sites up until the swarm lifted off.

Both of these sites are ploaed with a dotted line. Results-from the A. nigrocincta swarms

8 1 Figure 19. Approximate locations of nest sites inspected, as inferred from dances of A. cerana scouts on swarms hung at the ecotone between forest and disturbed agncultural area. White circles indicate location of trap hives. A) Disturbed agricultural land. B) Forest of Lore Lindu National Park. Distances are in metres. Angles are standard compass angles of north, east, south and West. Distant points are indicated to the top right of the graph.

Figure 20. Approximate locations of nest sites inspected, as inferred from dances of A. nigrocincta scouts on swams hung at the ecotone between forest and disturbed agricultural area. White circles indicate location of trap hives. A) Disturbed agnculniral land. B) Forest of Lore Lindu National Park. Distances are in metres. Angles are standard compass angles of north, east, south and West. Distant points are indicated to the bonom nght of the graph. swarm 1 r swarm 2 Distant points: swarm3 2290 m, 140" swarm4 2200 m, 140" A swarm 5 2340 in, 145" 6 1780 in, 140" swarm 1655 m, 155" swarm 7 1780 m, 135" 0 trap hives 1910 m, 135" 1390 ni, 130" Figure 2 1. Map indicating approximate distance and direction of sites agreed upon by A. cerana swmscouts. White circles indicate location of trap hives. A) Disturbed agricultural land. B) Forest of Lore Lindu National Park. Mean distance450 m. Distances are in metres. Angles are standard compasç angles of north. east, south and West. Dotted lines indicate two Iocations inferred fiom dances of a swarm which was not unanimous when the bees took to the air. Apis cerana A I N Figure 22. Map indicating approximate distance and direction of sites agreed upon by A. nigrocincta swarm scouts. White circles indicate location of trap hives. A) Disturbed agricultural land. B) Forest of Lore Lindu National Park. Mean distance=290 m. Distances are in metres. Angles are standard compass angles of north, east, south and west. Dotted lines indicate two locations inferred from dances of one swarm which was not unanirnous when the bees took to the air. Apis nigrocincta do not support Our altemate hypothesis that these bees preferentially choose to nest in the forest. Most dances by A. nigrocincta scouts indicated disturbed agricultural land rather than forest, and five out of eight destinations indicated in Fig. 22 were in disturbed agricultural areas. Two others were located just inside the forest. The eighth destination was almost 2 km in the forest.

Most dances by A. nigrocinc~ascouts indicated disturbed agricultural areas, yet the number of agreed upon sites in this habitat was relatively low. Of the sites which were selected in the disturbed second-growth areas, most were close to the ecotone. In the original observations which prompted this study (Hadisoesilo, 1997), roughly 85% of

A. nigrocincfa nests were found in the forest. and about 15% were found in disturbed habitats. This observation, combined with the results of Our study, suggest that A. nigrocincta may be somewhat less specific in its choice of habitat in which to nest.

The graphs show wide variation in the distance swarms were prepared to travel; for A. cerana, dancing scouts indicated distances from 10 m to 1420 m, and the averaged dances for final destinations ranged from 99 m to 780 m. Dances of A. nigrocincta scouts ranged from 75 m to 2340 m, and final destinations averaged from 140 m to 1920 m. Mean distances for the two species are significantly different (t-test, P

Most dances observed on the swarms indicated directions north and east of the swarms; the majority of these locations correspond to disturbed agricultural areas. In 86 these areas, rnany trees have been cut down. The resultant logs, if they contain cavities, provide many potential nest sites.

No dances indicated locations in the area where colonies of both species had concentrated foraging several weeks earlier. It is not known whether honey bees are able to evaluate the available forage at the area around a possible nest site, in addition to evaluating the characteristics of individual nest sites (Seeley and Morse. 1978).

Most of our A. nigrocincta colonies were obtained from established hives in the village of Kamarora, and several beekeepers told us that the A. nigrocincta bees had corne of their own accord to an empty nest box. Thus A. nigrocincta do not seem to be restncted to the forest. A. cerana, on the other hand, do not appear to nest in the forest in this zone of sympatry.

What effect does the presence of other colonies have on nest site selection? We knew of several colonies in the area where we set up swarms, but we did not attempt to locate al1 of the ferai or managed coionies in the area. Geographical areas are likely to differ greatly in availability of nest sites. In some circumstances, the density of colonies is limited by the number of acceptable nest sites (Crane. 1997). In other cases, food availability may be a limiting factor. Higher nest densities in the tropics than in temperate areas, despite the presence of many possible nest sites in each area, may illustrate different levels of food availability in each area (Ratnieks et al. 199 1). In a temperate Forest near Ithaca, New York, nest density of feral colonies was close to 0.5 nest per km2. In Chiapas, Mexico, colony nest density of A. mellifera scutellata was determined to be around 6 nests per km2(Ratnieks et al., 199 1). Colonies in the

Okavango River Delta, Botswana, were found at a density of 7.8 nests per km2

87 (Schneider and Blyther, 1988). Density of A. cerana nests rnay be even greater than that

of A. rnellifra. Near Padang, Sumatra, a census of nests for Apis cerana indica revealed

22 nests per km2,with a mean nearest neighbour distance between nests of 104 rn (houe

et al. 1990).

We did not attempt to census colonies in the area where we hung Our swarms. so

we do not know how the presence of other colonies may have influenced the decisions

made by swarms. The presence of conspecifics may act as an indirect biotic cue for a

swmof honey bees, either indicating that the area meets habitat requirements or letting

scouts know that they must searcb in another location in order to avoid resource

depletion.

A. cerana and A. nigrocincta seem to have an asymmetrical distribution. In

Central Sulawesi, nests of A. cerana have only been found in disturbed agncultural areas

and villages. Nests of A. nigrocincta, while found primarily in the forest, also sornetimes

occur in disturbed agricultural areas and villages. The locations indicated by bees dancing on swarms once they had reached agreement on nest sites are consistent with

these observed distributions, suggesting that the distribution of nests results from a colony level decision-making process.

The bees from our swarms largely ignored the trap hives which we hung out in a radius around the swam site. The trap hives may have been ignored for several possible reasons. 1) Perhaps the pulp cavities were not far enough away frorn the swarm. This may have been mie for A. nigrocincta, since al1 but one swarm decided on areas more than 200 m fiom the swam. However, two of the inferred destinations for swarms of A. cerana indicated locations within 200 m of the swam site, suggesting bat distance was

88 not a detemng factor for this species. 2) The hive boxes may not have been an

appropnate size for A. cerana and A. nigrocincta honey bees. Different races of A.

mellifera bees have shown preferences for different sizes of nest cavities, when given a

range fiom 13.3 to 85.1 litres (Jaycox and Panse, 1980, 198 1). Afncanized honey bee

swarms displayed no size preference for cavities ranging fiom 13.5 to 3 1 litres, but the

majority of European honey bee swarms chose larger cavities (Schmidt and Hurley,

1995). Without similar studies on A. cerana and A. nigrocincta, we cannot Say what size

cavities they might prefer. 3) Scout bees of one species which visited the pulp cavities

may have left behind pheromones repellant to the other species. 1 had no way to test thk

Occasionally when we checked Our trap hives, they had been knocked down or occupied by other insects (Table 4). Ants may have deterred scouts from using our pulp hives. However, we checked the pulp hives every second day and generally found them

Free of ants. If ants were present, we removed them. Besides, in my experience, ants in

Sulawesi are ubiquitous and 1 do not know how honey bees could keep other potential nest cavities completely free of ants.

The one trap box in a clearing was warrn when we checked it on sunny days, and thus it may have been unsuitable to scout bees.

For reasons beyond our control, the dances which we were able to record were likely only a fraction of the actual dances which were happening on the swarm. Our observations were limited to dances which took place on the surface of the swarm, but many dances on the swmseemed to happen beneath a layer of bees and thus could not be seen very well. For one A. nigrocincta swarm, 1 was only able to record a single dance before the swarm took to flight. In general, dancing increased as the swarm began

89 to corne to agreement, so that even though 1 might not have seen dances for al1 of the

advertized locations, 1 am quite confident that 1 saw dances for the most "popular"

locations.

Another source of uncertainty in my experiment concems the identity of the

dancers on the swarm. We had no way to be completely sure that an individual dance

was done by a scout rather than a nectar forager. We fed the colonies sugar water before setting hem up as swarms so that the bees would be well fed, but even so, some of the dances we observed may have been by nectar foragen rather than scout bees.

The locations agreed upon by the swarms in our study are basically in agreement with the previously observed distribution of feral nests (Hadisoesilo, 1997). The results

for A. cerana are especially clear in this regard; swarm scouts investigated potential nest sites in both forested and disturbed secondary growth areas, but decided upon nest sites only in the disturbed area. Ln this case, it seems that habitat preferences were exercised by the swarms during the decision-making process. A. cerana seems to act at a colony level to choose nest sites in a particular type of habitat. Data for A. nigrocincta are not as clear-cut; this species seems able to utilise a variety of habitats. CHAPTER 4

GENERAL DISCUSSION AND CONCLUSION

A. cerana and A. nigrocincta are different species, yet they are similar in both size and morphology (Hadisoesilo, 1997). Both of these honey bee species require nesting cavities for shelter and pollen and nectar for food. In the areas of Sulawesi where these species' distributions overlap, they show distinctly different distributions of feral nests, with A. cerana typically found at elevations below 400 m in disturbed agricultural areas and A. nigrocincta located primuily in the forest at higher elevations.

Hadisoesilo ( 1997) mentioned three possible factors which rnay influence the distribution of each species: climatic conditions; habitat preferences; and cornpetitive exclusion. Although climate undoubtedly influences honey bee distributions, in the zone of sympatry in Central Sulawesi these species live under the same climatic conditions.

Besides, in parts of Sulawesi in which A. cerana is not found, A. nigrocincta is found fiom higher elevations to sea level (Hadisoesilo, 1997).

1 specifically wanted to explore the role of habitat selection in the distribution of

A. cerana and A. nigrocincta. 1 looked at two aspects of habitat selection: location of foraging and location of nest sites scouted by swarms.

Foraging by colonies of A. cerana and A. nigrocincta was monitored for six days.

Our nul1 hypothesis that the species would forage indiscnminately among habitats was rejected. Our alternative hypothesis that each species would forage in its observed habitat of association was also rejected. Instead, each species foraged mainly in the mixed area southwest of the observation hives where cash crops are interspersed with ta11

9 1 forest trees.

Apparently food resource partitioning between these sympatric species does not happen at the level of habitats. However, during the days of observation of dancing foragers, A. cerana and A. nigrocincta concentrated on different pollen resources, suggesting that resource partitioning may be happening on a different level. 1 do not know what would cause foragers of each species to visit different species of flowering plants for pollen. Cornpetitive exclusion may be one explanation, but 1 think it unlikely because A. cerana foragers collected pollen fiom a huge field of corn from which I doubt they could have excluded A. nigrocincta. Each species might have preferences for different kinds of pollen for reasons which are as yet unknown.

A cornpanson of A. cerana and A. nigrocincta foraging activity throughout the day revealed large variation fiom day to day both among and between colonies.

Resources do not seem to be partitioned by differences in time of foraging; however, slight differences in time of foraging may result from each colony exploiting different resources (e.g. Figure 1 8).

In the swarming study (Chapter 3), A. cerana scouts investigated nest sites in al1 directions around the swarm. However, they decided on sites in disnirbed agricultural area. These resuits support the hypothesis that A. cerana swarms prefer to nest in non- forested areas. A. nigrocincta swmbees also scouted in both forest and disturbed agricultural areas. These swms decided on nest sites in both types of habitat, in contrast with Our hypothesis that A. nigrocincta swarms wculd preferentially select nest sites in the forest. The disproportionately long distances inferred fiom dances of one swarm which indicated a location deep in the woods suggest that suitable nesting sites

92 may not have been as abundant in the forest near the swarm, despite trap hives set out in a 150 m radius in all directions around the swarm site. Altematively, A. nigrocincta might be more of a generalist than A. cerana when it cornes to choosing a habitat within which to nest. Such a conclusion is suggested by the fact that we never saw an A. cerana colony in the forest but we did find several managed A. nigrocincta colonies in the village of Kamarora; the owners of a few A. nigrocincta hives cornmented that the bees had corne of their own accord to the empty hive boxes. This conclusion also agrees with the nest distribution obtained by Hadisoesilo (1997).

I found A. ceranu and A. nigrocincta to have dance curves with equal dopes, but

A. nigrocincta started doing a waggle dance at a farther distance from the hive (25 rn, compared to 10 m for A. cerana). A. nigrocincta also bad a wider flight range than A. cerana, both in distances travelled while foraging and distances of nest sites investigated by swann scouts, but both species had relatively short foraging ranges. Information on preferred foraging ranges is helpful when deciding where to place hives; ideally there ought to be abundant sources of food within the preferred range. A wider flight range could give A. nigrocincta an advantage over A. cerana, enabling the former to scout farther for food and for nesting sites.

The abundance of feral nest cavities is not uniform in a particular area. Disnirbed areas may have more nest sites available because trees have been cut clown.

Several published studies have investigated the factors which influence honey bees' selection of nest sites (reviewed in Winston, 1987; Seeley, 1985a). In fairly broad terms, niche associations have been spelled out for the three main groups of honey bees:

A. dorsata build large, open combs under the strong horizontal branches of emergent

93 trees; A. florea build small combs on branches in thick vegetation; and A. cerana often nest in tree trunk hollows (Appanah and Kevan, 1995). But in terms of broader habitat associations, I know of no previous studies which addressed the role of habitat in nest site selection, in particular by cavity-nesting honey bees. Honey bees are particularly suited for this type of study, because the decision-making process can be observed directly through observation of dancing scout bees. My study indicates that for some colonies, habitat may be a strong influencing factor. However, it is difficult to know to what extent habitat associations are the result of cornpetitive interactions between the two species or of nest site availability. In order to rule out cornpetition as a factor, swarms of each species could be tested separately along the ecotone in areas in which the species live in allopatry. Nest cavity availability could be a limiting factor in sorne locations; more nest cavities may be available in disturbed areas than in the forest, for exarnple, because of more felled trees in the former area. To determine the distribution of natural nest sites would be a difficult matter, but artificial nest sites can be placed in each habitat.

Pior to the swarming expenment described in Chapter 3, we had no information about the size of cavities or distance scouted by A. nigrocincta swarms. Perhaps smaller artificial nest cavities placed further from the swmwould be more attractive to A. cerana and A. nigrocincta. REFERENCES

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e time refers to the time of day, measured with a stopwatch and adjusted according to the "equation of time" by adding or subtracting minutes depending on the day of the year. Time here is expressed in angular time, where O"= 12:OO am and 180°=12:00 pm. Each degree corresponds to four minutes. Prior to analysis, it was not necessary to adjust data to solar zenith time, because near Lore Lindu National Park we were practically on the 120" meridian. Angles are measured in degrees, clockwise from vertical. Tirnekircuit is recorded in seconds.

A.1 Apis cerana

November 9, 1998 true time angle tirnekircuit true time angle tirnekircuit 128 128.25 128.5 128.75 129.35 129.5 129.75 130.25 130.5 131 13 1.25 131.5 139.25 139.75 140.25 140.5 140.75 140.75 141 142 142.5 142.75 143 143 .S5 143.5 143.75 144 144.25 144.5 true time angle tirnekircuit true time angle tirnekircuit 144.75 186.25 143 2.26 145 186.75 132 2.05 145 .X 186.75 135 3.62 145.5 187 9 1 1.48 145.75 187.25 78 1.43 146 187.25 143 1.63 146.5 187.5 80 1.84 154 187.5 88 1.3 154.25 187.75 112 1.74 154.5 188 79 1.17 153.75 188.25 103 1.69 155 188.5 18 1.96 155.25 188.75 79 1 -29 155.25 188.75 105 1.7 155.5 189 55 1.36 155.75 189.25 63 1 .69 156 189.5 84 1.48 156.25 189.75 9 1 1.4 156.5 190 45 1.43 157 190.25 59 1.4 157.5 190.5 94 2.09 158.25 191 45 1.74 159 191 -25 9 1 1.49 159.25 199.5 42 2.29 160 202.75 45 2.18 160.25 206 1 07 3.89 160.5 215 97 3 .O7 161 2 15.75 355 1.3 161 2 17.5 126 3.05 161.25 218.25 102 3.13 17 1 220.5 58 2.56 172 22 1 93 3 .O7 172.25 173.5 November 1 1, 1998 173.75 174.25 tnie time angle tirne/circuit 174.75 97 274 2.1 1 175 98 304 1.4 175.5 99.5 280 1.64 176.25 101.25 277 1.92 176.5 1 09 134 3 -47 184.75 109.25 136 3.2 1 185 185.25 109.75 165 3.55 tme time angle tirnekircuit tnie time angle tirnekircuit 110 58 3.1 129.25 114 3.38 110.75 230 1.4 129.25 186 2.15 111 50 2.86 129.5 129 3.39 111 134 3 .O2 129.75 115 3.24 111.5 131 3.17 130 180 4.33 11 1.5 157 3.52 130 155 4.12 11 1.75 56 3.38 130.25 132 2.7 1 12.25 121 3.57 130.75 133 2.95 1 12.5 140 3 -96 139.75 159 4.45 113 140.5 161 3.99 113 140.75 155 3.77 113.25 141 164 4.07 113.5 14 1.25 175 2.45 113.75 141.75 170 3.89 1 14.5 142 107 3.13 115.25 142.75 152 3.3 8 1 15.5 143.75 110 3.8 1 15.75 144.75 172 3.62 116 145 170 4.16 1 16.5 154.5 176 3.01 124.25 154.75 158 3 .O5 124.25 155.25 168 4.25 124.5 156.75 143 4.25 124.75 157.75 263 1.76 125 158.5 151 3.6 125.25 159.75 135 3 ,97 125.5 160 124 4.27 125.75 160.5 136 3.66 126 160.75 128 3.42 126.25 169.25 95 3 .O8 126.5 169.5 95 2.86 126.75 169.75 90 3.12 127 169.75 89 2.83 127.25 170 92 2.58 127.5 170.25 9 1 3.18 127.75 170.25 9 1 2.88 128 170.5 9 1 2.43 128.25 170.75 90 2.52 128.75 172.5 340 1.22 129 2 14.25 184 3 .28 true time angle tirnekircuit true time angle tirnekircuit 2 13.75 199 3.63 125.5 2 15.25 20 1 3.87 125.75 2 15.25 200 3.72 126 2 15.75 199 3.29 126.25 2 16.75 204 3.63 126.5 229.5 286 3.85 127 230 110 4.5 1 127.25 230.25 292 3.44 127.5 230.5 139 4.27 127.75 332.75 127 3.66 128 248 125 4.37 128.25 248.5 117 4.79 128.75 25 1.25 118 4.37 129 25 1.5 108 4.44 129.25 129.25 Novernber 13, 1998 129.75 130 inie time angle tirnekircuit 131 99.75 3.24 13 1.5 100.75 3.47 139 109.5 2.85 139.25 109.75 2.76 141 109.75 2.69 14 1.25 110 2.83 142 110.5 2.68 142.5 1 10.75 2.82 142.75 1 1 1.25 2.66 143 111.25 3 *O3 143 11 1.5 2.72 143.75 112 2.97 144 112.25 2.92 144.5 113.25 2.87 144.75 145.5 145.75 146 146 146.25 1 54.5 1 54.75 155 tme time angle tirnekircuit true time angle tirnekircuit 155.25 2 15.75 155.75 2 16-25 156 2 16.75 156.25 217 156.75 2 17.25 157 2 i 7.75 157.25 218 157.5 2 18.25 157.75 2 18.5 158 219 158.25 2 19.25 159 2 19.25 159.25 2 19.5 160 220 160.75 220.25 161.5 220.5 169 220.75 169.25 22 1 171.5 22 1.25 172.75 229 173.25 229.25 173.5 229.75 1 74 230 174.5 230.25 175 230.5 175.25 23 1.5 175.5 233 175.75 233.25 176 233.5 176.25 234.25 184.75 234.5 186 235 186 235.75 187 236 204.25 236.25 214 24425 2 14.25 245 2 14.5 246.75 215 247.5 2 15.25 248 ûue time angle tirnekircuit 248.75 275 2.67 249.5 283 2.96 250.25 276 2.5 25 1.25 278 3.18

A.2 Apis nigrocincta

November 10, 1998 true time angle tirnekircuit 146 146.25 154 155 157 158.25 16 1-25 161.5 170.25 170.5 173 174.25 175.5 176 184 184.25 184.5 184.75 185.25 185.75 186 186.25 186.75 186.75 187.25 l87.75 188.25 188.5 188.75 189.25 189.5 true time angle tirnekircuit true time angle tirnekircuit 189.75 234.5 144 2.19 190.25 235.75 130 3.67 190.75 236.25 O 4.84 191 244 349 4.24 191 245 1O6 2.53 191.25 245.25 359 4.69 191.5 247 358 4.19 199 247 358 4.08 199.75 248 6 3.95 200 238.5 130 2.55 200.75 249.5 10 4.52 20 1.5 250.75 137 3.9 202 25 !.25 115 3.5 204.25 260 350 1.9 1 205 260.25 350 2.19 2 14 26 1 97 3.36 2 14.25 2 15.25 November 12, 1998 2 15.5 216 me time angle tirnekircuit 2 16.75 2 17 2 17.5 2 18.25 2 18.75 219 2 1 9.25 2 19.5 2 19.75 220 220.25 220.5 220.75 22 1.25 229.5 229.75 230.75 23 1 232.5 233 tme time angle tirnekircuit true time angle tirnekircuit 101.5 188.25 109.25 188.5 109.5 188.75 109.75 189 1 10.25 189.25 1 1 1.25 189.25 Il4 189.5 125.25 189.75 126.25 190 130.75 190.35 13 1.25 190.5 139 190.75 139 190.75 142 191 142.75 i91.5 143 236 143.25 244.25 143.75 244.75 144 245.5 144.25 246 144.5 246.75 144.75 247.5 145.25 250.5 146.25 25 1 146.25 154.25 November 13, 1998 154.5 154.75 true time angle tirnekircuit 154.75 95.25 164 7.45 156.25 96.5 163 6.76 156.5 97.75 158 6.18 157 98.75 156 6.49 160 99.75 358 2.82 185.25 100.25 154 8.03 185.75 100.5 356 2.03 186.25 109.25 89 5.28 186.5 109.75 256 3.37 186.75 110 66 3.67 187 110.25 174 5.88 187.25 110.75 158 6.43 angle tirnekircuit 3 1*44 15 1.42 3 1.62 6 1.69 353 1.34 3 1-44 335 1.54 5 1.43 11 1.54 4 1.89 359 1.38 6 1.33 O 4.18 APPENDIX B: DANCE DATA FROM SWARMING STUDY

True time refers to the time of day, measured with a stopwatch and adjusted according to the "equation of time" by adding or subtracting minutes depending on the day of the year. Time here is expressed in angular time, where 0°= 12:OO am and 180°=12:00 pm. Each degree corresponds to four minutes. Pnor to analysis, it was not necessary to adjust data to solar zenith time, because near Lore Lindu National Park we were practically on the 120° meridian. Data in boldface indicate dances observed when bees on the swarm may have been able to see blue sb Angles are measured in degrees, clockwise from vertical. Tirnekircuit is recorded in seconds.

Swarm # 1 date true time angle tirnekircuit 156.75 date true time angle tirnekircuit 160.25 18/11/98173.25 88 2.4 160.75 174.75 215 10 161.25 175 95 2.36 169.5 175.5 212 9.52 174.5 185.25 96 3 -26 176.25 185.5 18 1 5.96 183.75 186 180 6 184.25 199.25 113 7.03 185.25 201.5 93 5.46 185.5 203.5 89 4.54 188.5 3.82 204 25 189 2 14.5 126 5.96 191 -25 2 15.75 126 6.2 199 16.25 126 6.1 1 2 199.75 2 16.75 126 6.02 200.5 20 1 202.25 date true time angle tirnekircuit 204 20/11/98 140.5 33 1 5.82 204.5 142.25 317 3.6 204.75 146 170 1.43 205.5 146.25 270 2.48 213.75 154.75 243 2.32 215 155.25 120 1.65 2 15.75 date true time angle tirnekircuit date tnie time angle tirnekircuit 2 16.75 187 3.57 198.5 176 2.97 2 17.5 140 3 .O2 199.25 175 3.12 2 19.75 28 1 2.86 200.25 92 2.48 220.5 180 3.35 200.75 175 2.58 220.7 5 183 3.29 20 1 162 2.98 233.5 157 4.2 203 155 2.73 234.5 129 3.3 203.25 173 2.8 235.5 112 2.39 205.25 172 3.16 246 132 4.15 213.25 145 2.6 1 247.5 124 -.7 93 213.75 157 2.55 213.75 157 2.64 Swarm #3 2 14.5 148 2.02 2 14.75 152 2.47 date tnie time angle tirnekircuit 215 159 2.45 25/11/98140 2 15.5 170 2.27 142.25 2 15.75 165 2.16 155.25 216 165 2.18 156.5 157.75 Swarm #4 158.25 158.75 date tnie time angle tirnekircuit 159.5 28/11/98 123.5 32 1 1.59 160 126 343 1.97 168.75 128.25 337 2.48 170.75 128.5 338 2.43 171.25 128.75 334 1.68 171.5 129.25 302 2.13 172.75 129.5 302 1.66 173 138.25 342 2.85 184.5 139.5 34 1 2.13 1 85.25 139.75 340 1.18 185.75 140.5 289 1.75 186 141.25 343 1.28 186.25 142.75 287 2.44 186.5 143 357 2.23 187 143.75 354 1.81 187.5 144 353 1.45 189.25 153.75 O 1.45 189.75 154.5 355 2.7 190.25 155 O 2.2 date me time angle tirnekircuit 155.5 17 1.99 156.75 1 3.23 157.75 357 2.07 158 9 2.O6 158.5 42 1.87 159.75 14 2.28 168.5 310 1.84 169 310 1.61 169.25 303 1.37 171.25 284 1.97 171.5 293 1.84 174.5 274 1.9 183.25 170 1.66 183.5 172 1.6 185.25 172 1.36 185.5 175 1.26 188.75 157 1.82 189.5 150 1.9

204 115 b341 204.25 114 2.06

date true tirne angle tirnekircuit 4/ 12/98 139.25 180 4.85 141.75 180 4.9 1 143.5 188 4.85 1 44 177 4.59 144.25 180 4.66 153.25 174 4.76

B.2 Apis nigrocincta

Swarm # 1 date true time angle tirnekircuit 136.5 185 7.24 date tme time angle timelcircuit 137 186 6.8 16/1 1/98246.25 285 2.28 138.75 185 6.72 17/11/98107.25 250 3.53 139.5 222 4.14 108.25 3 3.32 140.5 192 6.67 124.25 O 2.92 140.75 183 6.36 date true tirne angle tirnekircuit date tme time angle time/circuit 142 180 6.4 1 204.75 95 3.35 209 102 4.04 Swann #2 214 70 3.87 2 14.25 78 4.02 date tme time angle tirnekircuit 2 14.5 80 3.57 2311 1/98138.5 264 4.35 2 15.75 76 3.57 139 265 5 .O9 2 17.75 76 3.27 140.5 353 4.08 140.75 345 3.3 5 141.25 26 1 3 -49 142.25 345 4.2 1 date tmetime angle tirnekircuit 143.25 20 1 4.2 8/12/98 136 143.5 28 1 3.68 177.75 145.5 315 3 .O9 9/ 12/98 1 1OS 153.5 283 3.74 113.25 i 53.75 270 3.68 L 14.5 154.25 283 3.43 124.25 154.75 103 4.13 125.25 156.25 27 1 3.1 125.5 1 56.75 27 1 3.17 126.75 157.25 90 5.7 1 127 158.25 90 3.74 127.5 158.75 185 4.95 127.75 160 278 2.73 128.25 160.5 278 3.5 1 129 161 212 3.52 130.5 168.75 259 1.99 130.75 170 264 2.38 170.25 263 1.81 171.75 26 1 2.49 172.75 164 2.79 date tnie time angle timelcircuit 173 258 2.08 91 l2I982O9 122 2.92 220.25 174 258 2.95 180 5 -77 174.5 238 2.3 222 124 3.67 175 248 2.57 222.25 115 3.59 222.5 115 3.66 Swarrn #3 223 113 3.76 235 102 3.13 date tnie time angle timelcircuit 235.75 108 3.74 5/12/98 198 85 3.45 236.5 101 3.13 204.5 175 3.97 238 105 3.42 date tme time angle tirnekircuit date true time angle tirnekircuit 23 8.25 98 4.19 1 54.5 234 3 -7 239.25 101 3.37 154.75 242 2.86 340.25 101 3.39 155.25 358 11.5 242 1 03 4.26

date ûue time angle tirnekircuit 10/12/98155 35 1 3 .O8

Swam #7