The associations of the plant-ant Cladomyrma with plants in

403 Pages·2010·16.98 MB·English

by  Joachim Moog

The associations of the
plant-ant Cladomyrma
with plants in Southeast Asia

Dissertation
zur Erlangung des Doktorgrades
der Naturwissenschaften

vorgelegt beim
Fachbereich Biowissenschaften
der Johann Wolfgang Goethe-Universität
Frankfurt am Main

von
Joachim Moog
aus Frankfurt am Main

Frankfurt am Main 2009
Vom Fachbereich ............................................................................................................
der J. W. Goethe-Universität, Frankfurt am Main, als Dissertation angenommen.

Dekan: .............................................................................................................................

Gutachter: .......................................................................................................................

Datum der Disputation: ...................................................................................................

Contents i

Contents

1. Preface 1

2. Notes on terminology 4
2.1. Myrmecophyte 4
2.2. Domatium 6

3. Revision of the genus Cladomyrma 7
3.1. INTRODUCTION 7
3.2. MATERIAL AND METHODS 8
3.3. RESULTS AND DISCUSSION 9
3.3.1. Synopsis of species 13
3.3.2. Key to the queen caste 14
3.3.3. Species accounts 17
Cladomyrma andrei 17
Cladomyrma hobbyi 19
Cladomyrma maschwitzi 22
Cladomyrma nudidorsalis 23
Cladomyrma petalae 24
Cladomyrma yongi 27
Cladomyrma aurochaetae 29
Cladomyrma crypteroniae 31
Cladomyrma dianeae 33
Cladomyrma hewitti 35
Cladomyrma maryatiae 37
Cladomyrma sp. nov.? 39
3.3.4. Conclusion 40
3.3.5. Summary of the revision 44

4. Host plants of Cladomyrma 45
4.1. INTRODUCTION 45
4.2. MATERIAL AND METHODS 47
4.3. RESULTS 49
4.3.1. Fabaceae – Caesalpinioideae 49
Saraca thaipingensis 49
Saraca dives 58
4.3.2. Fabaceae – Papilionoideae 60
Callerya nieuwenhuisii 60
Spatholobus bracteolatus 65
Spatholobus oblongifolius 69
4.3.3. Loganiaceae 74
Strychnos vanprukii 74
4.3.4. Rutaceae 78
Luvunga sp. 78
4.3.5. Achariaceae 82
Ryparosa fasciculata 82
Ryparosa porcata 87
Ryparosa sp. nov. aff. calotricha 88
Ryparosa anterides 89
[Ryparosa amplifolia] 89
4.3.6. Crypteroniaceae 90
Crypteronia griffithii 90
Crypteronia macrophylla 97
4.3.7. Putranjivaceae 100
Drypetes longifolia 100
Drypetes fusiformis 105
ii Contents
4. Host plants of Cladomyrma (continued)

4.3.8. Rubiaceae 108
Neonauclea 108
Neonauclea artocarpoides 127
Neonauclea borneensis 127
Neonauclea calcarea 127
Neonauclea excelsioides 129
Neonauclea gigantea 129
Neonauclea longipedunculata 132
Neonauclea paracyrtopoda 132
Neonauclea pseudocalycina 135
Neonauclea sp. A 135
Neonauclea sp. B 138
Neonauclea sp. C 139
Neonauclea sp. D 139
Neonauclea sp. E 139
4.3.9. Summary of the results: host plants 143
4.4. DISCUSSION 144
4.4.1. Taxonomic diversity 146
4.4.2. Diversity in distribution 146
4.4.3. Diverse habitats 147
4.4.4. Diverse growth forms 150
4.4.5. Differences in ant-housing structures 150
4.4.6. Preadaptations for myrmecophytism 155
4.4.7. Evolutionary specialisation of ant-housing structures 158
4.4.8. The special case of Neonauclea and its sister taxon Myrmeconauclea 162

5. Host-choice 166
5.1. INTRODUCTION 166
5.2. MATERIAL AND METHODS 167
5.3. RESULTS 169
5.3.1. Summary of the results: host-choice 170
5.4. DISCUSSION 170

6. Acquisition of scale insects 173
6.1. INTRODUCTION 173
6.2. MATERIAL AND METHODS 176
6.3. RESULTS 181
6.3.1. Dispersal flight 181
6.3.2. Colony founding 181
6.3.3. Experimental exclusion of trophobionts 185
6.3.4. Active entry of immature mealybugs into founding chambers 187
6.3.5. Primary hole 190
6.3.6. Summary of the results: acquisition of scale insects 191
6.4. DISCUSSION 192
6.4.1. Co-dispersal 192
6.4.2. Colony founding 195
6.4.3. Secondary slits 196
6.4.4. Primary hole 197
6.4.5. Experimental exclusion of trophobionts 198
6.4.6. Active entry of immature mealybugs into founding chambers 202
6.4.7. Scale insect dispersal 204
6.4.8. Conclusion 205
Contents iii

7. Flood control 207
7.1. INTRODUCTION 207
7.2. MATERIAL AND METHODS 208
7.3. RESULTS 209
7.3.1. Summary of the results: flood control 212
7.4. DISCUSSION 212

8. Ant activity 215
8.1. INTRODUCTION 215
8.2. MATERIAL AND METHODS 216
8.3. RESULTS 218
8.3.1. Food rewards on the plant surface? 218
8.3.2. Spatial and temporal distribution of ant activity 221
8.3.3. Activity on mature plant parts 228
8.3.4. Behaviour of the ants on young leaves 229
8.3.5. Response to disturbance of the host plant 229
8.3.6. Summary of the results: ant activity 230
8.4. DISCUSSION 231
8.4.1. Variation of ant activity and response to disturbance 231
8.4.2. Activity on mature plant parts 232
8.4.3. Preference for young plant parts 232
8.4.4. Does the host plant mediates the ant's behaviour by chemical signals? 233
8.4.5. What is the cue by which Cladomyrma ants can recognise young plant tissue? 235
8.4.6. Why do Cladomyrma species preferentially patrol young plant tissue? 236

9. Protection against herbivory 239
9.1. INTRODUCTION 239
9.2. MATERIAL AND METHODS 240
9.3. RESULTS 244
9.3.1. Ant response to insect herbivores 244
9.3.2. Field observations of unprovoked encounters with insect herbivores 250
9.3.3. Ant response to insect eggs (cleaning behaviour) 252
9.3.4. Ant protection of young leaves 253
9.3.5. Summary of the results: protection against herbivory 258
9.4. DISCUSSION 259
9.4.1. Protection against phytophagous insects 259
9.4.2. Cleaning behaviour 261
9.4.3. Does Cladomyrma provide protection against folivorous mammals? 263
9.4.4. Underestimation of the protective effect 265
9.4.5. Protection by a facultative ant, Crematogaster sp. 1 266
9.4.6. Is degree of folivory a good precursor of plant fitness? 268
9.4.7. Plant defence hypotheses 270
9.4.8. What is the role of biotic defences in relation to the plant's other defences? 273
9.4.9. Vulnerability of young plant tissue 274
9.4.10. The role of extrafloral nectaries 275
9.4.11. Biotic defence by Cladomyrma 278

10. Pruning of neighbouring plants 282
10.1. INTRODUCTION 282
10.2. MATERIAL AND METHODS 284
10.3. RESULTS 285
10.3.1. Summary of the results: pruning behaviour 290
10.4. DISCUSSION 291
10.4.1. Pruning intensity and climber toughness or age 291
10.4.2. The Cladomyrma maschwitzi case 293
10.4.3. Pruning in climber-inhabiting Cladomyrma species 294
10.4.4. Chemical 'warfare' 297
iv Contents
11. Concluding discussion 300
11.1. A plant’s perspective: benefits of being colonised by Cladomyrma 301
11.2. A plant’s perspective: costs of being colonised by Cladomyrma 304
11.3. Do host plants need Cladomyrma for their survival? 309
11.4. The ants’ point of view 315
11.5. Host specificity 317
11.6. Host range and specialisation in other plant-ant lineages 321
11.7. Evolution of host affiliation 323

12. Summary 329

13. Ausführliche Zusammenfassung 331
13.1. Einleitung 331
13.2. Revision der Gattung Cladomyrma 332
13.3. Das Wirtspflanzenspektrum 332
13.4. Unterschiede zwischen den Wirtpflanzen 333
13.5. Nutzen der Cladomyrma-Besiedlung für die Wirtspflanzen 336
13.6. Kosten der Cladomyrma-Besiedlung für die Wirtspflanzen 337
13.7. Brauchen Wirtspflanzen Cladomyrma für ihr Überleben? 338
13.8. Nutzen und Kosten aus Sicht der Ameisen 338
13.9. Wirtsspezifität 339
13.10. Evolution des Wirtsspektrums 339

14. References 341

15. Appendix 378
15.1. Table index 378
15.2. Figure index 379
15.3. Deposit of Cladomyrma specimens in Malaysia 383
15.4. AntWeb field guide to Cladomyrma (www.antweb.org) 385

16. Acknowledgements 388

17. Publications 391

18. Lebenslauf 394

19. Erklärung 395
Preface 1

1. Preface

Ada gula ada semut
Malayan proverb

No plant can live in tropical regions without having personal contact with ants. What
happens when these two worlds come together? What follows is a treatise on a rather
extraordinary ant/plant complex. Specifically, this dissertation is about Cladomyrma
plant-ants and their extremely extensive host plant range. In a broad sweep this study
examines several aspects of the behavioural ecology of Cladomyrma, for example
colony founding, host plant selection, acquisition of trophobiotic mealybugs, protection
of their hosts against herbivorous insects, and effects of catastrophic events, such as
flooding of nest chambers. Another major part of this study explores Cladomyrma
taxonomy and host plant range in order to evaluate the degree of host specificity.

All these aspects touch some fundamental biological questions concerning
mechanism of maintenance of diversity, e.g. habitat and/or host selection, intra- and
interspecific competition and stochastic versus deterministic colonisation. Other major
subjects in biology that are touched by this study are plant anti-herbivore defence
systems and the evolution of interspecific mutualisms. Such mutualisms are
widespread, but how they evolve is not clear. What factors promote the intimate
interaction between unrelated organisms? Do these ant/plant associations show the
potential for reciprocal evolutionary change, i.e., for coevolution?

Naturally, these subjects, being of major importance to biological science, cannot be
treated here in depth. On the contrary, it is my intent to maintain a broad but rather
superficial course by highlighting various different aspects, thus providing a first
glance from different angles on this newly discovered ant/plant complex. The result is
a puzzle with widely separated pieces and many gaps. Still, I hope that a picture
emerges that serves as the framework for promising future research.
2 Preface

Let me say a few words regarding the so-called 'big science'. We presently live in a
time when molecular biology and other types of big science receive far more attention
by grant giving institutions than 'simple' field research. This trend will continue to
reduce interest in whole-organism biology and natural history in both universities and
the students they produce. But, as DEVRIES, CHACON & MURRAY (1992, p.123) have
stressed earlier, "without data from the real world, no matter how sophisticated
laboratory techniques or models become, in the absence of natural history they are
unlikely to broaden our understanding of the myriad interactions among organisms." In
my opinion, future insights into tropical biodiversity in general, and ant-plant mutualism
specifically will demand a great deal more field work. The study on Cladomyrma/plant
associations presented here illustrates this need.

The tropical rain forests display a biodiversity unparalleled by that of any other
vegetation type. However, over the past few years I experienced a dramatic loss of
tropical rainforest in some of my study areas. On the island of Borneo, for example,
the natural forest cover is disappearing at a fast rate. Sabah, a federal state of
Malaysia on Borneo, has almost depleted its primary forests outside conservation
areas (UEBELHÖR & VON DER HEYDE 1993, RAMAKERS 1999, CHUNG et al. 2000,
FITZHERBERT et al. 2008). Today, more than two thirds of the commercial forest
reserves have been turned into second growth forests.

Secondary growth and selective logging, in turn, greatly enhance fire danger and,
indeed, in the last two decades, fire has become one of the greatest threats to
Bornean tropical rainforests (SIEGERT & HOFFMANN 2000). For the Bornean province
East Kalimantan (Indonesia) alone it is estimated that during a severe drought caused
by the 1997/98 El Niño phenomena, some 3 million hectare of forest (700,000 ha of
protected forests and 2.3 million ha of natural forest concession areas), about 15% of
the entire province, were affected by fire (HOFFMANN, HINRICHS & SIEGERT 1999). As
yet there is no clear trend of a return to pre-disturbance conditions, which indicates
that the burned forest may remain in a severely degraded state for a prolonged period
of time (CLEARY & PRIDJATI 2005).

Certainly, several of the studied ant/plant associations will be strongly affected by
these intense logging activities and increased fire danger. Although a few ant
associations with pioneer host plant species seem to benefit - at least on a short-term
basis - by these activities, I fear that in the long run they will be diminished as well. My
observations suggest that the association with Cladomyrma is lost - even in pioneer
hosts - when the distance to rainforest sources increases. A recent study by TANAKA et
al. (2007) corroborates my assumption that deforestation can drastically decrease the