View metadata, citation and similar papers at core.ac.uk brought to you by CORE

provided by ScholarBank@NUS

ANT FUNCTIONAL GROUP SUCCESSION

DYNAMICS CORRELATES WITH THE AGE OF

VEGETATION SUCCESSION: DATA ANALYSIS

OF WORLDWIDE STUDIES AND A CASE STUDY

OF A SECONDARY TROPICAL RAIN FOREST IN

SINGAPORE

THAM KOON HUNG, ANDREW

(B.Sc. (Hons.), NUS)

A THESIS SUBMITTED FOR THE DEGREE OF MASTER OF

SCIENCE

DEPARTMENT OF BIOLOGICAL SCIENCES

NATIONAL UNIVERSITY OF SINGAPORE

2006

a 0 ACKNOWLEDGEMENTS

My deepest gratitude to Associate Professor Li Daiqin, who not only guided me and kept me focused on this project but also allowed me the freedom to think and play with ideas. I will look back many years from now and wonder where I would have gone without him. My heartfelt thanks to members of the Spider Lab, whose friendship kept me young-at-heart, especially Jeremy Woon for all the “lunge” sessions, Matthew Lim for the “tech support”, Olivia Tan for evaluating the standards of my jokes, Seah Wee

Khee for actually laughing at them, Chris Koh for the entertaining CDs. I thank Reuben

Clements and Kelvin Peh for their patience and enormous help with data analysis,

Darren Yeo for his initial advice on being an ant taxonomist, the National Parks Board,

Chew Ping Ting and Benjamin Lee for approving the research permit, supplying the

GIS data and guidance when I was lost in the jungle. To Faith, my precious daughter, for giving me the impetus to finish this thesis. To my ever-lovely, then-girlfriend and now wife, Geraldine, without whom I may never have had the belief in myself to do anything meaningful in life. Finally, to JC, my constant but silent friend: thanks for forgiving my nonsense.

“Go to the ant, thou sluggard; consider her ways, and be wise...”

- The Bible

i TABLE OF CONTENTS

Page

ACKNOWLEDGEMENTS i

TABLE OF CONTENTS ii

ABSTRACT iii

LIST OF TABLES iv

LIST OF FIGURES v

CHAPTER 1 GENERAL INTRODUCTION 1

CHAPTER 2 ANALYZING PUBLISHED DATA TO STUDY THE 10

SUCCESSION ECOLOGY OF ANTS

Introduction 10

Material and Methods 15

Results 20

Discussion 33

CHAPTER 3 ANT SUCCESSION DYNAMICS IN A SECONDARY 41

RAIN FOREST OF SINGAPORE

Introduction 41

Material and Methods 46

Results 55

Discussion 66

CHAPTER 4 GENERAL DISCUSSION 72

REFERENCES 81

APPENDIX 95

ii ABSTRACT

Many studies have shown that ant communities respond to changes in the environment but some questions remain unanswered. What functional groups dominate different types of ecosystems? What groups succeed one another? Are there trends in the succession of ant communities in relation to vegetation succession? To answer these questions, data analysis of existing studies from six terrestrial ecosystems, viz. tropical rain forest, montane forest, temperate forest, desert, subtropical grassland, tropical bushland, was performed. I showed that each habitat had different dominant functional group. In tropical rain forests, Opportunist and Tropical Climate Specialist functional groups were the pioneer community that established in young, disturbed vegetation.

These two groups were succeeded by Cryptic Species, Generalized Myrmicinae and

Specialized Predator groups during vegetation succession. Sigmoidal mathematical models best described the decline and growth of these two communities, respectively. I demonstrated this pattern of functional group succession by conducting a study of the ant community within a secondary tropical rain forest in Singapore. Using the mathematical models, the ages of different locations in this forest were estimated. This pattern of functional group succession implies that ants may be used as bioindicators during forest rehabilitation. Directed studies on specific groups may be conducted to assess their impact on forests at different stages of succession. The mathematical models represented a first step in developing tools for estimating forest age where historical records are lacking.

iii LIST OF TABLES

Page

Table 1. Summary table of studies on ants. 19

Table 2. Description of the typical vegetation found in each of the four Forest 52

Types in Singapore.

Table 3. Study site, forest type and environmental variables. 54

Table 4. Variance in species data (r2) represented by the three axes of 62

ordination and the coefficients of correlation of significant

environmental variables with axes two and three.

Table 5. MRPP Results of average within-group (Forest Type) distances and 63

pair-wise comparisons between groups.

iv LIST OF FIGURES

Page

Figure 1. Proportions of functional groups in tropical rain forest, 24

temperate forest and desert.

Figure 2. Proportions of functional groups in subtropical bushland, 25

montane forest and tropical grassland.

Figure 3. Relationships between proportions of functional groups and age 26

of forests.

Figure 4. Relationships between proportions of functional groups and age 27

of forests.

Figure 5. Correlations of proportions of Opportunist with Generalized 28

Myrmicinae, Cryptic Species and Specialized Predator ants.

Figure 6. Correlations of Cryptic Species with Tropical Climate Specialist, 29

Generalized Myrmicinae and Specialized Predator ants.

Figure 7. Correlations between proportions of functional groups with one 30

another.

Figure 8. Correlation between proportions of Tropical Climate Specialist 31

and Specialized Predator ants.

Figure 9. Relationship between proportions of Cold Climate Specialist and 31

age of temperate forests.

Figure 10. Sigmoid curves relating the proportions of functional groups and 32

the age of tropical rain forests.

Figure 11. Sketch map of Singapore main island. 45

v

Figure 12. Study sites and transects in the Central Catchment Nature 53

Reserve.

Figure 13. Correlation between proportions of functional groups and the 58

ranked age of Forest Type.

Figure 14. Correlation between proportions of functional groups and the 59

ranked age of Forest Type.

Figure 15. Correlations of proportions of Cryptic Species, Generalized 60

Myrmicinae and Specialized Predator groups with Opportunist

group.

Figure 16. Correlations of proportions of Cryptic Species, Generalized 61

Myrmicinae and Specialized Predator groups with Tropical

Climate Specialist group

Figure 17. NMS plots of species and site scores. 64

Figure 18. Estimated mean age of different Forest Types. 65

vi CHAPTER 1

GENERAL INTRODUCTION

Succession Ecology

Ecosystems are not static entities. Conditions within habitats vary widely and one group of these variations is ecological succession cycles. For example, large trees in primary rain forests often collapse, leaving gaps in the canopy and creating patches where secondary succession takes place (Whitmore, 1998). The gaps slowly return to the primary condition after many years, completing the cycle (Whitmore, 1998). There are similar cycles in other areas such as aquatic habitats (Wetzel, 1995).

The general trend seen in ecological succession is that of particular community structure and environmental conditions replacing another over time. There usually is a set of environmental conditions that allow a certain community to thrive. As this community ages, the conditions change and another set of community more suited to the new conditions gradually take over (McCook, 1994). Furthermore, it is not just the interactions between environment and community that play important roles. Interactions between different species are also important in determining the path of succession

(Farrell, 1991).

In addition, one of the most important determinants of whether an ecosystem recovers naturally is the disturbance caused by humans. The over-riding significance of the ecological footprints created by anthropogenic disturbance is clearly demonstrated

1 in large-scale landscape changes brought about through the advancement and development of human civilization (DeFries et al, 2005). The natural cycles are either altered or replaced by artificial cycles. For example, cultivated landscapes that were subsequently abandoned often do not have the conditions that are necessary for growth into its original uncultivated state (Roth, 1999).

The natural resources of this planet are limited but yet are being exploited at a high rate (DeFries et al, 2005). There is an urgent need to restore exploited ecosystems and bring it back from the brink of collapse. This is important because ecosystems provide numerous services (Bennett et al, 2005). Having a good understanding of succession ecology will enable stakeholders of the environment to effectively rehabilitate and conserve natural resources so that sustainable use is achieved for the long term (Leitao and Ahern, 2002).

Many ecologists try to grasp the complexity of succession by describing its individual components and making useful extrapolations in order to understand general trends (Underwood, 1997). Another challenge that ecologists deal with is to come up with reliable models of prediction from their observations. Predictive models in ecology are useful in that it allows researchers to work on a general level with fewer variables to estimate the responses of ecosystems (Brook et al, 2000). Such models could serve as an alert mechanism for possible impending ecological crisis, much like climate change and global warming models (Viner et al, 1995).

One of the components of succession is the animal community. The fauna of a habitat changes with the succession cycle (Done, 1992). Therefore, ecologists often study changes in populations and communities of animals that affect and are themselves affected by succession. For example, the community structure, species richness and

2 abundance are different at different stages of succession (Done, 1992). Ants are considered a useful group of organisms for the study of ecosystem succession. This is because of their relatively wide ecological range (Holldobler and Wilson, 1990) and the different responses of different species to changes in the habitats (Andersen, 1995).

Aspects of ant biology and their significance in ecosystems will be discussed shortly.

Biology of The Ants

“Ants are everywhere,” Holldobler and Wilson (1990) once commented. It is not surprising that such a statement was made. Ants are insects, which constitute over 75% of all estimated animal species on this planet (Ruppert and Barnes, 1994). There are more than 9,000 described species of ants in nearly 300 genera, forming the entire family Formicidae, within the order Hymenoptera (Bolton, 1994).

There are three anatomical features found in the ant that set it apart from other insects. First, ants have narrow proximal segments of the abdomen joining the thorax.

These narrow segments are known collectively as the petiole (Bolton, 1994). Second, the mandibles of an ant are elongated and highly modified for grasping and cutting

(Holldobler and Wilson, 1990). The ants use their mandibles for a variety of purposes, including manipulation of objects, defense and communication (Holldobler and Wilson,

1990). Third, ants have a pair of metapleural gland on the last segment of the thorax

(Holldobler and Wilson, 1990). These glands produce phenylacetic acid, which has antibiotic properties (Beattie et al, 1986). The metapleural gland is present only in ants and has been described as their defining characteristic (Holldobler and Wilson, 1990).

3 An interesting aspect of the ants is the social nature of their existence. Ants are eusocial insects, meaning they live and interact closely in a colony and only one or a minute portion of individuals in the entire colony reproduces while the rest are sterile

(Gadagkar, 1994). The study of this social nature of the ants’ existence has yielded great insights into the areas of animal communication and behavior. We now know that there are many classes of chemicals used in communication within and across species (Law and Regnier, 1971; Nordlund, 1981). The nature, quantity and stereochemistry of such chemicals differentiate the types of signals sent (Holldobler, 1983a). In addition to chemical signals, the ants use complex sequences of tactile signals and body movements to convey information regarding food source, recruitment needs and defense, among others (Holldobler and Wilson, 1978), much like the well-known waggle dance of honeybees (Judd, 1995).

The study of ant society has helped introduced the concept of altruism to the field of evolutionary biology (Wilson, 1975). Altruism may be defined as actions undertaken by an individual that benefit others at a detrimental cost to that individual performing these actions (Le Galliard et al, 2005). Altruistic actions by the ants include the worker caste foregoing its reproductive functions while tending to the welfare of the reproductive caste and older workers stationing themselves at the territorial boundaries of the colony where mortality rates are higher due to increased predation (Porter and

Jorgensen, 1981) and confrontation with other ant colonies (Holldobler, 1983b). The study of altruism has contributed many ideas to the fields of kin selection and sociobiology (Wilson, 1971; 1975). Wilson (1975) had even argued a Darwinian explanation for the existence and perpetuation of human culture based on altruism and kin selection.

4 Ants belong to different levels of the food pyramid. Seed harvester ant species of the genus Pogonomyrmex are primary consumers (Pol and Casenave, 2004) while certain species of Iridomyrmex are secondary or higher consumers that hunt and feed on other arthropods (Gibb and Hochuli, 2004). Still other species are parasites or detritivores. Ants are also important prey. For example, disturbances in ant populations have been known to affect the animals feeding on them (Suarez and Case, 2002).

Ants form symbiotic relationships with other insects. This include ants tending the larva of Riodinidae butterflies, protecting the latter from predators while feeding on the sugary secretion that these larva produce (Ross, 1966). Some butterfly species even spend their pupal stage within the nests of the ants (Holldobler and Wilson, 1990). In addition to animals, symbiotic relationships with plants are also common. For example, species of Crematogaster, which live within the Macaranga plant, reduce the damage from herbivory suffered by these plants (Murase et al, 2003). Holldobler and Wilson

(1990) gave a fascinating account of how a number of fungal species are obligately and asexually propagated by fungi-culturing ants. These fungi are not known to reproduce naturally without the help of the ants (Weber, 1957).

Human beings have both been affected by and taken advantage of ants. The fire ant, Solenopsis invicta, destroys human properties through its disruptive nesting activity

(Greenberg et al, 2003) and causes deadly anaphylactic reactions in people who are allergic to the venom found in the ants’ stings (Solley and Vanderwoude, 2004). There have been many instances of humans using ants as a form of pest management and records of ancient Chinese history showed that the leaf-weaver ant, Oecophylla smaragdina, was cultivated on fruit trees to deter or reduce pest damage and this method is still employed in parts of China as an alternative to chemical pesticides

5 (Huang and Yang, 1987). Way and Khoo (1992) has an excellent review on the subject of ants as bio-control agents.

The Ecology of Ants

The composition of ant species in different ecosystems, like temperate forests (Maeto and Sato, 2004), deserts (Nash et al, 2004), montane forests (Robertson, 2002) and lowland rain forests of the tropics (Yamane et al, 1996), differ from one another. It is also known that species composition within the same habitat is influenced by different environmental conditions (Vasconcelos, 1999) and competitive interactions (Andersen,

1995).

There has been much progress in the study of the distribution of ant communities in different habitats ever since Andersen (1995) proposed a functional group classification of Australian ants. Under this classification system, ants in

Australia were grouped based on their hypothesized community dynamics, niche requirements and evolutionary history (Andersen, 1995). Using this classification, King et al (1998) was able to show that the proportions of different functional groups sampled in primary, young and old secondary lowland tropical rain forests were different. Environmental conditions and community dynamics change as vegetation succession takes place (Whitmore, 1998) and it is, therefore, possible that functional groups of ants replace one another during the process. In other words, the proportions of functional groups that may be sampled could be different in secondary forests of different ages.

6 Another notable progress was made when Brown (2000) widened the concept of functional groups to cover most genera of ants around the world. The genera and matching functional groups are listed in Appendix A. It is now possible to study the distribution patterns of ants around the world in terms of functional groups. The use of the functional group concept for the purpose of studying ant ecology has two potential advantages over traditional species-based studies. First, traditional ant taxonomy is based largely on external morphology, fossil records (Bolton, 1994) and, increasingly in recent years, phylogenetics (Ohnishi et al, 2003) while it ignores the resource requirement of each species. Therefore the responses of functional groups to changes in the habitat could, in theory, be much easier to predict over that of a community of species (Andersen, 1995). Second, in trying to grapple with the numerous species while looking for meaningful patterns, many ecologists try to reduce as much data as possible while retaining useful information (McCune and Grace, 2002). Most described ants found in ecological samples may be classified into one of nine functional groups

(Brown, 2000). Hence it is possible to work with a relatively smaller data set compared to species-based records while retaining enough information about available niche and resource.

The classification of ants into functional groups has generated many interesting questions. For example the global pattern of distribution of these functional groups is unknown. Are certain groups dominant in certain landscapes? There is also scarce knowledge on how these groups would respond to anthropogenic disturbance of forests and the subsequent second growth process. Furthermore, it would be interesting to be able to relate the quantitative relationship, if any, between populations of functional groups and the maturity of vegetation succession.

7

Main Aim of The Project

The main aim of this project is to look at the distribution pattern and succession ecology of functional groups of ants in relation to forest succession and to try to explain these patterns in terms of changing environmental conditions in forests of different ages. I achieved this aim through two methods.

For the first method, mega data was collected from existing scientific literature on ant sampling studies throughout the world and analyzed. The abundance data of every species collected from each study was re-organized to show the proportions of each functional group with respect to the overall number of ant individuals collected.

The first objective was to find out what were the most abundant functional groups in the different landscapes studied. A second objective was to detect changes in proportion of each ant functional group in the different landscapes at different ages or stages of vegetation succession. In addition, I wanted to see whether the proportions of functional groups were correlated with one another. A third objective was to develop a mathematical model that relates the proportional abundance of functional groups to the age of tropical rain forests. In the absence of accurate records, it is difficult to know the age of re-generating vegetation and stakeholders who intend to rehabilitate a disused landscape would need to know this information. This is because a recently disturbed habitat would be ecologically dissimilar to an older area. Knowing the age of a re- generating ecosystem would allow suitable rehabilitation measures to be instituted.

For the second method, I conducted an ant sampling study in a secondary rain forest in Singapore. The first objective of this study was to see whether the results of my

8 data analysis of existing studies (discussed above) could be replicated in a secondary rain forest. The second objective was to explore the role of environmental factors in shaping the distribution patterns of the different functional groups in forests of different ages. The final objective was to use the mathematical models, developed previously, to estimate the age of different areas of a secondary forest in Singapore.

9 CHAPTER 2

ANALYZING PUBLISHED DATA TO STUDY THE

SUCCESSION ECOLOGY OF ANTS

Introduction

The concept of functional groups was initially proposed by botanists who wanted to describe and predict the variations in relative abundances of plants in response to changes in the environment (Raunkier, 1934; Noble and Slatyer, 1980; Pokorny et al,

2005). Different species responding similarly to particular environmental stimuli were thus classified in the same ‘functional’ group (Andersen, 1995). Subsequently, many ecologists used this concept to study the responses of other organisms such as birds

(French and Picozzi, 2002), bats (Stevens et al, 2003) and aquatic invertebrates (Heino,

2005) to variations in the environment.

Andersen (1995) proposed a functional group classification of Australian ants where species were classified into nine groups. The objective was to provide a classification system for use in analyzing general responses of ant communities to environment stress and disturbance (Andersen, 1995). The basis of classification was the observation that ants and vascular plants have ecological parallels (Andersen, 1991).

Vascular plants generally have similar ecological requirements and strategies in that individuals are situated in a fixed place while having repeated modules or units

10 such as branching in-ground root systems for gathering nutrients and water as well as aerial shoot systems for gathering sunlight and gases (Harper, 1985). This similarity leads to intense competition within the plant community for resources (Grime, 1979).

An individual ant has relatively minimal ecological impact and the colony is regarded as the functional ecological unit or “super-organism” while individuals may be regarded as the cellular equivalent (Holldobler and Wilson, 1990). The nesting site of an ant colony is fixed for most species and groups of individuals foraging both in and above ground may be considered as modular root and shoot systems, respectively

(Harper, 1981). As a result of similar ecological strategies, the competition for resources among ants is also intense (Holldobler and Wilson, 1990).

Grime (1977) defined three broad factors that influenced distribution of plants.

These are:

(i) environmental stresses, such as sub-optimal temperatures and available

moisture;

(ii) disturbances, such as habitat destruction, and;

(iii) competitive but resource-rich environments.

Plants that are able to thrive in each of the above situation are known as stress- tolerators, ruderals and competitors, respectively (Grime, 1977). Andersen (1995) considered three major groups of Australian ants as having one of the three strategies each. These are:

(i) Dominant Dolichoderinae, which are stress-tolerators;

(ii) Opportunist, being ruderals, take advantage of habitat disturbances but

being poorly competitive means they are unable to perpetuate

themselves when other ant functional groups are gradually established;

11 (iii) Generalized Myrmicinae, which are good competitors and able to recruit

rapidly at resource-rich habitats.

Six other groups of ants, which have their own unique resource requirements, are also defined (Andersen, 1995). These are:

(i) Subordinate Camponotini, which are not as competitive as other ants

and are usually found in low numbers in any type of habitat;

(ii) Specialized Predator, which prey on other arthropods and being

predators, their numbers are usually low and dependent on the presence

of target prey items;

(iii) Cryptic Species, which nest underground and forage exclusively within

or on the ground;

(iv) Tropical Climate Specialists, which thrive in warm and humid

environments of the tropics, particularly in the canopies of rain forests;

(v) Hot Climate Specialists, which live in arid habitats like deserts and;

(vi) Cold Climate Specialists, which are found mainly in cooler, temperate

regions.

There have been many studies on the responses of ant functional groups since their introduction and land managers have been using the functional group classification effectively to monitor land management and rehabilitation in Australia (Andersen and

Majer, 2004).

King et al (1998) conducted a study to investigate ant community differences between primary and secondary tropical rain forests in Australia. They found that

Opportunist ants dominated young secondary forests while Generalized Myrmicinae

12 ants were the most abundant in primary forests and the other groups were relatively less abundant in either type of forest.

The succession of tropical rain forests is a complex process (Richards, 1996) and changes in biotic and abiotic factors within the forest take place over time (Whitmore,

1998). Two kinds of changes with respect to time periods may be described: environmental and diversity variations tend towards a primary state in tandem with vegetation succession over centuries while fluctuations in microclimate over periods of days and months are driven by short-term cycles of the physical environment (Longman and Jenik, 1987). Given this complexity, it is inappropriate to classify forests, and its accompanying assemblages of organisms, as purely secondary or primary (Whitmore,

1998). Succession is a continuum with different plants and animals taking on prominence of varying degrees, at various stages (Longman and Jenik, 1987).

Furthermore, diversity seldom has a positive relationship with maturity of habitat

(Connell, 1978).

There are several interesting but unanswered questions arising from the study by

King et al (1998). It is unknown whether the eventual succession of ant communities within secondary forests would lead to a community that reflects that of an original, primary forest (i.e. one dominated by Generalized Myrmicinae). Furthermore, it is unclear if other functional groups exist in substantial numbers in forests at different stages of succession, from younger to older and finally near-primary or primary stages.

Perhaps the most significant question was whether this system of classification could be applied to ants on a global scale. If applicable, then what functional groups would be found in dominant numbers in ecosystems other than tropical rain forests? Are there predictable trends of ant succession in these ecosystems?

13 A first attempt to answer these questions was made by Brown (2000) when he extended the concept of functional groups to include most ant genera of the world. This effort at widening the system of classification, although largely hypothetical, meant that ecologists all over the world would have a template not only to test the validity of the classification but also to study broad responses of the ant communities to changes in the environment. Predictive ecological models could also be generated from such responses

(Babovic, 2005).

The first objective of this chapter is to find out what are the most abundant functional groups of ants in various types of vegetation around the world. The second objective was to look for changes in the abundance of functional groups with the ages of these vegetations, to find correlations between the abundances of functional groups and to test three specific hypotheses.

From the results of the study by King et al (1998), it would seem that abundances of at least two functional groups (i.e. Opportunist and Generalized

Myrmicinae) changed during forest succession. Therefore, I hypothesized that there exists a negative linear relationship between the proportional abundance of Opportunist ants and the age of a tropical rain forest. Proportional abundance was defined as the ratio of number of ant individuals of a functional group to the total individuals collected in a sample.

A second hypothesis is that there exists a positive linear relationship between the proportional abundance of Generalized Myrmicinae ants and the age of a tropical rain forest. These hypotheses were based on the ecological strategies of the Opportunist and

Generalized Myrmicinae functional groups as ruderals and competitors respectively

(Andersen, 1995).

14 Furthermore, the pattern of functional group distribution seemed to show that

Generalized Myrmicinae ants replaced Opportunist ants as vegetation succession progressed (King et al, 1998). Therefore, my third hypothesis was that there exists a negative correlation between the proportional abundances of Opportunist and

Generalized Myrmicinae groups of ants in tropical rain forests of various ages.

The third objective was to develop mathematical models to relate the proportional abundances of functional groups to the age of the forest. These models would allow researchers to estimate or predict the age of a forest by sampling the ant fauna or vice versa.

Material and Methods

I conducted an analysis of published studies that involved sampling for ant community abundances. The following two criteria were used for selection of works for this mega data analysis:

(i) Studies had to be conducted in landscapes where the ages of the

vegetation were known. Ages were given by the authors and were based

on the number of years since the vegetation was last cleared and left to

re-generate.

(ii) Data from only the bait and pitfall traps was used for this analysis. For

studies that included other techniques (e.g. Berlese funnel), the data

from bait and pitfall traps was extracted. The type of data analyzed was

the total number of individual ants collected for each species. Some

authors provided data in the form of proportional abundance (i.e. the

15 proportion or percentage of each species out of the total number of

individuals collected). This proportion data was also used for my

analysis.

The studies that were selected are listed in Table 1. For each selected study, the total number of ant individuals was calculated for each replicate. A replicate was regarded as the total sampling effort in a single contiguous forest of a single age. For each replicate, species were grouped together by functional groups using Brown (2000) as the reference (Appendix A). The total individuals collected in each functional group was calculated and converted to percentage values of the total number of individuals for that replicate. Proportion values were arcsine-transformed and Kolmogorov-Smirnov goodness-of-fit analysis was done to test for normality (Zar, 1999).

The main emphasis was not placed on exact standardization of experiment designs across studies because this mega data analysis was concerned mainly with the quantity of ants collected. The quality or robustness of the various studies was of lesser concern. The rationale behind this inclusive approach was to maximize the number of studies available for the review, keeping in mind the main aim of detecting broad scale patterns in the responses of functional groups to vegetation succession. The need for inclusiveness was illustrated by the fact that ant sampling studies with quantitative data were only available for six landscapes or ecosystems and these were deserts, subtropical bushlands, tropical grasslands, temperate, montane and tropical lowland rain forests.

Out of these six ecosystems, only montane, temperate and tropical rain forests had information on the ages of study sites.

To find the dominant functional groups in each ecosystem, one-way ANOVA, followed by Tukey HSD post-hoc comparisons where applicable, was performed. In

16 order to test my hypotheses and explore the relationships between functional groups and ages of forests, linear regression equations were calculated using the age of forests as the independent variable and the proportions as the dependent variable. It is reasonable to assume that the age affects the proportions of functional groups sampled (King et al,

1998). Therefore linear regression was used instead of correlation (Zar, 1999).

For functional groups that had significant relationship with age of forest, their proportions were correlated with one another in a pair-wise manner using Pearson’s correlation (Zar, 1999). In this case of comparing proportions of different groups of ants, there was no indication to show that the abundance of one group of ants could affect any other group or vice versa, therefore correlation analysis was used instead of regression (Zar, 1999).

Finally, functional groups that had significant results in age-proportion regression were used to develop mathematical models that related proportional abundance with age. Two models, or equations, were developed using non-linear regression, to describe the growth or decline of functional group proportions with age.

For the growth model, the proportions of functional groups that increased with age were summed. The best sigmoid curve (i.e. highest r2 with p < 0.05) that related this summed proportion to age of forest was selected. The same procedure, using the proportions of functional groups that decreased with age, was repeated to select the best decline model.

This was because biological population dynamics are usually best described by sigmoid curves (Sibly and Hone, 2002; Tsoularis and Wallace, 2002). All statistical calculations were done with SPSS 11.5 (SPSS, Inc., Chicago, USA).

The reason for summing the proportions of these two broad groups of ants, and not using any one functional group, was because I wanted to see broad trends of ant

17 community dynamics in relation to vegetation succession. Summing or pooling the data for groups of ants that responded similarly to vegetation succession would increase the strength of my analysis. It would also allow further generalizations to be made about ant successions. For example, we could refer to the community of ants that increased in abundance with succession as the “late colonizers” while those that were found in abundance in young forests but declined subsequently could be referred to as the “early colonizers”. This generalization would serve as a useful reference tool for developing a package of sampling protocols to assess the status of a habitat.

18

Table 1. Summary table of studies on ants

Ecosystem Location Replicates Study Desert Chiricahua Mountains, USA 1 Andersen 1997 Great Basin Desert, USA 1 Nash et al 2001 Eastern Mojave Desert, USA 1 Nash et al 2004 Gobi Desert Mongolia 9 Pfeiffer et al 2003 Olympic Dam, Australia 1 Read & Andersen 2000 Montane forest Heredia Province, Costa Rica 2 Perfecto & Snelling 1995 Mkomazi Game Reserve, Tanzania 5 Robertson 2002 Subtropical bushland Mkomazi Game Reserve, Tanzania 5 Robertson 2002 Temperate forest Wilson's Promontory, Australia 1 Andersen 1986 Chiricahua Mountains, USA 1 Andersen 1997 Shimanto River Basin, Japan 12 Maeto & Sato 2004 Tropical grassland Mpumalanga Province, South Africa 6 Hamburg et al 2004 Tussen die Riviere Nature Reserve, South Africa 1 Lindsey & Skinner 2001 Tropical lowland rain forest Western Ghats, India 1 Basu, 1997 Kinabalu National Park, Borneo 1 Berghoff et al, 2003 Riviere Bleue, New Caledonia 2 Breton et al, 2003 Barro Colorado Island, Panama 1 Feener and Schupp, 1998 Barro Colorado Island, Panama 1 Kaspari and Weiser, 2000 Atherton Tablelands, Australia 5 King et al, 1998 Kununurra, Australia 1 Majer and Camer-Pesci, 1991 Vicosa, Brazil 1 Ribas et al, 2005 Mkomazi Game Reserve, Tanzania 2 Robertson, 2002 Popondetta, Papua New Guinea 2 Room, 1975 Sarapiqui, Costa Rica 11 Roth et al, 1994 Catanduanes Island, The Philippines 1 Samson et al, 1997 Dimona and Porto Alegre, Brazil 5 Vasconcelos, 1999 Lambir Hills National Park, Borneo 1 Yamane et al, 1996

19 Results

Dominant functional groups in different ecosystems

The most abundant functional groups in tropical rain forests were Opportunist and

Generalized Myrmicinae (Figure 1A). Cold Climate Specialist ants were significantly more abundant than others in temperate forests (Figure 1B). Hot and Cold Climate

Specialists were the most abundant groups in deserts (Figure 1C). Cryptic Species were abundant in subtropical bushlands (Figure 2A) and montane forests (Figure 2B). There was no difference in proportions of functional groups in tropical grasslands (Figure 2C).

Age-proportion regression and among-groups correlation

In tropical rain forests, regression analyses showed that there was significant positive linear relationship between the proportion of Generalized Myrmicinae ants and the age of forests (Figure 3A) while Opportunist ants decreased with the age of forests (Figure

3B). There were also positive linear relationships between the age of the forest and the proportions of both Cryptic Species (Figure 3C) and Specialized Predators (Figure 4A) groups while the Tropical Climate Species group was negatively related with forest age

(Figure 4B).

Among-groups correlation analyses of data from tropical rain forests showed that proportions of Opportunist were negatively correlated with those of Generalized

Myrmicinae (Figure 5A), Cryptic Species (Figure 5B) and Specialized Predator ants

(Figure 5C) while positively correlated with Tropical Climate Specialist ants (Figure

20 6A). Proportions of Cryptic Species were positively correlated with those of the

Generalized Myrmicinae (Figure 6B) and Specialized Predator (Figure 6C) groups and the proportion of the Generalized Myrmicinae was positively correlated with that of the

Specialized Predator group (Figure 7A). The proportions of Tropical Climate Specialist ants were negatively correlated with those of the Cryptic Species (Figure 7B),

Generalized Myrmicinae (Figure 7C) and Specialized Predator groups (Figure 8).

In temperate forests, only the proportions of Cold Climate Specialist ants had a linear and positive relationship with age of the forest (Figure 9). The proportions of other functional groups did not change significantly with age. There was no relationship between the proportions of any functional group with the age of montane forests.

Mathematical models relating proportions and age

To develop a model describing the growth in proportions of functional groups of ants with the age of tropical rain forests, the summed proportions of Cryptic Species,

Generalized Myrmicinae and Specialized Predator ants were used. The proportions of these groups of ants all showed significant increase with age of the forest.

The summed proportions of Opportunist and Tropical Climate Specialist ants were used to develop a model describing the decline in proportions of functional groups of ants with the age of tropical rain forests. The proportions of these groups of ants decreased with age.

Figure 10A shows the best-fit sigmoid curve and equation for the growth model.

Re-arranging

21 0.769 y = 24.242−x (Equation 1A) 1 + e 14.219 where y is the summed proportions of Cryptic Species, Generalized Myrmicinae and

Specialized Predator functional groups and x is the age of the forest, the following equation was obtained:

⎛ 0.769 ⎞ x = 24.242 −14.219 ln⎜ −1⎟ (Equation 1B) ⎝ y ⎠

Figure 10B shows the best-fit sigmoid curve and equation for the decline model.

Re-arranging

0.883 y = 1.916 (Equation 2A) ⎛ x ⎞ 1 + ⎜ ⎟ ⎝ 32.572 ⎠ where y is the summed proportions of Opportunist and Tropical Climate Specialist functional groups and x is the age of the forest, the following equation was obtained:

⎛ 0.883 ⎞ ⎜1.916 ⎟ x = 32.572⎜ −1⎟ (Equation 2B) ⎝ y ⎠

The 95% confidence interval of the curves showed that the maximum combined proportions of Opportunist and Tropical Climate Specialist ants was around 70-80% and this occurred at the very beginning of forest succession immediately after the cessation of human disturbance. This proportion decreased to the minimum of about 0-15% in a sigmoidal pattern as the vegetation reverted to a primary or near-primary condition. The proportions Cryptic Species, Generalized Myrmicinae and Specialist Predator showed a similar sigmoidal pattern of increase from about 5-15% in very young forests to about

65-70% in mature forests.

22 In temperate forests, only one functional group, the Cold Climate Specialist group, was significantly related to the age of the forest and non-linear regression did not produce any significant result. The linear equation was not developed further as a mathematical model because it cannot realistically represent biological population dynamics. For example, according to the linear equation, the proportions of Cold

Climate Specialist ants would increase indefinitely with the age of forest but this is clearly illogical.

23

A Tropical rain forest

0.6 a a a b a b a a a Between groups df = 8, Within groups df = 281, 0.3 F = 29.706, p < 0.01 Proportions 0.0 123456789

B Temperate forest 0.6 c b a b b b a,b a a Between groups df = 8, ons i Within groups df = 108, 0.3 F = 64.441, oport

r p < 0.01 P 0.0 123456789

C Desert 1.0 b a a a b a a a a Between groups df = 8, ons i Within groups df = 108, 0.5 F = 14.737, p < 0.01 Proport 0.0 123456789

Functional groups

Figure 1. Proportions of functional groups in tropical rain forest, temperate forest and desert. Small letters represent results of Tukey HSD post-hoc comparisons, ranked alphabetically in ascending order. 1 = Cold Climate Specialist, 2 = Cryptic Species, 3 = Dominant Dolichoderinae, 4 = Generalized Myrmicinae, 5 = Hot Climate Specialist, 6 = Opportunist, 7 = Subdominant Camponotini, 8 = Specialized Predator, 9 = Tropical Climate Specialist.

24

A Subtropical bushland 0.8 a d a,b c a c a b,c a Between groups df = 8, Within groups df = 36, ons 0.4 F = 42.092, p < 0.01 Proporti 0.0 123456789

B Montane forest 1.0 a b a a a a a a a Between groups df = 8, ons 0.5 Within groups df = 54, F = 74.902,

Proporti p < 0.01 0.0 123456789

C Tropical grassland 0.4 a,b,c c,d a d b,c,d b,c,d a,b,c a,b a,b,c Between groups df = 8,

ons Within groups df = 54, 0.2 F = 6.922, p < 0.01 Proporti

0.0 123456789

Functional groups

Figure 2. Proportions of functional groups in subtropical bushland, montane forest and tropical grassland. Small letters represent results of Tukey HSD post-hoc comparisons, ranked alphabetically in ascending order. 1 = Cold Climate Specialist, 2 = Cryptic Species, 3 = Dominant Dolichoderinae, 4 = Generalized Myrmicinae, 5 = Hot Climate Specialist, 6 = Opportunist, 7 = Subdominant Camponotini, 8 = Specialized Predator, 9 = Tropical Climate Specialist.

25

A

e 0.8 y = 0.165 + 0.003x ina

c 2 i r = 0.544

rm p < 0.01 y 0.4 d M e z i

General 0.0 0100200

B 1.4 y = 0.661 + 0.006x r2 = 0.595 st p < 0.01 uni 0.7 Opport

0.0 0 100 200

C 0.6 y = 0.041 + 0.001x r2 = 0.147 p = 0.02

0.3 tic Species p y Cr

0.0 0100200

Age of forests

Figure 3. Relationships between proportions of ant functional groups and age of forests. Vertical axes show proportions. Horizontal axes show age in years.

26

A

0.2 y = 0.039 + 0.001x r r2 = 0.473 ato p < 0.01

Pred 0.1 ecialized Sp 0.0 0100200

B

0.4 y = 0.123 - 0.001x r2 = 0.269 p < 0.01

ate Specialist 0.2

0.0 Tropical Clim 0 100 200

Age of forests

Figure 4. Relationships between proportions of ant functional groups and age of forests. Vertical axes show proportions. Horizontal axes show age in years.

27

A 0.8 ae r = -0.859 icin p < 0.01

Myrm 0.4 neralized e

G 0.0 0.0 0.7 1.4

Opportunist

B 0.2 r = -0.434 p < 0.01

0.1 Cryptic Species

0.0 0.0 0.7 1.4

Opportunist

C 0.2

or r = -0.785

edat p < 0.01 r d P

e 0.1 z i l a eci p S 0.0 0.0 0.5 1.0

Opportunist

Figure 5. Correlations of proportions of Opportunist with Generalized Myrmicinae, Cryptic Species and Specialized Predator ants.

28

A

0.2 r = 0.636 ecialist p < 0.01

ate Sp 0.1 ical Clim 0.0 Trop 0.0 0.5 1.0

Opportunist

B

0.6 ae r = 0.533

icin p < 0.01

0.3 ralized Myrm e n e

G 0.0 0.0 0.1 0.2

Cryptic Species

C

0.2 r = 0.775 p < 0.01

0.1 Specialized Predator 0.0 0.00 0.09 0.18

Cryptic Species

Figure 6. Correlations of Cryptic Species with Tropical Climate Specialist, Generalized Myrmicinae and Specialized Predator ants.

29

A 0.2 r = 0.545 p < 0.01

0.1 Specialized Predator 0.0 0.0 0.4 0.8

Generalized Myrmicinae

B 0.2 r = -0.588 p < 0.01 ecies 0.1 tic Sp yp Cr

0.0 0.0 0.1 0.2

Tropical Climate Specialist

C

0.8 r = -0.678 icinae p < 0.01

Myrm 0.4 ralized e n e

G 0.0 0.00 0.09 0.18

Tropical Climate Specialist

Figure 7. Correlations between proportions of functional groups with one another.

30

0.2 r = -0.630 p < 0.01 edator

0.1 Specialized Pr 0.0 0.0 0.1 0.2

Tropical Climate Specialist

Figure 8. Correlation between proportions of Tropical Climate Specialist and Specialized Predator ants.

1.0 y = 0.475 + 0.001x r2 = 0.260 p < 0.05 0.5 ate Specialist

Cold Clim 0.0 0125250

Age of forest

Figure 9. Relationship between the proportion of Cold Climate Specialist functional group and the age of temperate forests. Vertical axes show proportions. Horizontal axes show age in years.

31 A 1.0 0.769 y = 24.242−x 1 + e 14.219 2 ons

i r = 0.857 0.5 p < 0.01 oport r P

0.0 0 100 200

B 1.4 0.883 y = 1.916 ⎛ x ⎞ 1 + ⎜ ⎟ ⎝ 32.572 ⎠ ons r 2 = 0.791 0.7 p < 0.01 Proporti

0.0 0 100 200

Age of forest

Figure 10. Sigmoid curves relating the proportions of functional groups and the age of tropical rain forests. Solid lines represent regression curves and dotted lines represent 95% confidence interval of regression. Vertical axis of Graph A is summed proportions of Cryptic Species, Generalized Myrmicinae and Specialized Predator ants. Vertical axis of Graph B is summed proportions of Opportunist and Tropical Climate Specialist ants. Horizontal axes show age in years.

32 Discussion

Dominant functional groups in different ecosystems

My analysis showed that Generalized Myrmicinae and Opportunist functional groups were the dominant ants in tropical rain forests. This is consistent with the observation made by King et al (1998). Generalized Myrmicinae ants prefer the warm, humid and resource-rich shaded environment of the rain forest floor (Andersen, 1995). Opportunist ants were similarly abundant because they are able to establish themselves in disturbed habitats and are often the most abundant ants in large cleared areas of the forest

(Bestelmeyer and Wiens, 1996; King et al, 1998).

Ambient temperature seemed to be the main factor determining the community structure of ants in temperate forests and deserts. The cooler climate in temperate forests is probably responsible for the abundance of Cold Climate Specialist ants while Hot

Climate Specialist ants dominate the arid desert environment. The abundance of Cold

Climate Specialist ants in deserts could be explained by the drastic change in temperature between day and night in deserts (Goudie, 2002). Therefore, one would expect the Cold Climate Specialist ants to be active during the night while the Hot

Climate Specialist ants would be active during the day. It would be interesting to study how these two groups of ants share ecological niches by being active at different times.

Cryptic Species prefer to nest in the ground, within the leaf litter and soil

(Andersen, 1995) so they may be sampled by ground collection techniques. The use of bait and pitfall traps would allow Cryptic Species ants to be sampled. However, since subtropical bushlands and montane forests are less species-rich and diverse compared to

33 the rain forest (Connell, 1978), other functional groups of ants would probably be less abundantly collected. This possibly explains the dominance of Cryptic Species ants in samples from subtropical bushlands and montane forests.

The diversity and species-richness of ants in grasslands are generally lower than in forest habitats (Hamburg, 2004). This could be a possible explanation why no functional group was more abundant than others.

Age-proportion regression and among-groups correlation

(i) Tropical rain forest

My analysis showed two general patterns in how ants responded to vegetation succession in tropical rain forests around the world. First, the Generalized Myrmicinae,

Specialist Predator and Cryptic Species functional groups increased proportionally with forest succession. Second, Opportunist and Tropical Climate Specialist groups decreased proportionally with ages of forests.

There are changes in ecological niches immediately following destruction of rain forests and fluctuations in the physical environment are usually greater than in older or primary habitats (Connell, 1978; Longman and Jenik, 1987). The loss of large trees and accompanying vegetation often mean other species are corresponding lost (Turner, 1996;

Brook et al, 2003). This concurrent emptying of niche and fluctuations in environment conditions would allow Opportunist ants, which adopt the ruderal strategy (Andersen,

1995), to establish themselves in dominant numbers. As the effects of the initial disturbances fade with time, leading to stabilization of environment, the other groups of ants would gradually be able to establish themselves. Opportunist ants, being poorly

34 competitive (Andersen, 1995), would not be expected to dominate in numbers compared to other groups as the forests mature. Hence the proportions of Opportunist ants showed a decrease with increasing forest age.

Generalized Myrmicinae ants thrive in resource-rich and low environmental stress areas, such as the understorey of primary or mature secondary rain forests

(Andersen, 1995). Therefore, when a secondary forest matures Generalized Myrmicinae colonies would gradually establish themselves in parallel with the gradually stabilizing environmental conditions and increasing resources available to ants.

Cryptic Species ants were so named because of their preference in nesting underground and foraging in and on the surface of the ground (Andersen, 1995). When rain forests are cleared, there are concomitant changes in the properties of soil (Lemenih et al, 2005). Some of the characteristics affected include erosion of topsoil and changes in bulk density and pore space (Lal, 1996). It is possible that these changes in soil characteristics could affect the nesting and establishment of ground-dwelling colonies, resulting in lower proportions of Cryptic Species in samples of disturbed and young habitats. As the forest matures, soil characteristics would gradually return to those that existed in the original primary forest (Lavelle and Spain, 2001). Therefore the proportions of Cryptic Species ants increased with forest age.

Specialized Predator ants prey almost exclusively on other arthropods (Andersen,

1995). As discussed earlier, there is a general loss of biodiversity after deforestation and arthropods are similarly affected (McGeoch, 2002). The loss of prey would exert a strong negative pressure on the number of Specialized Predator ant colonies being able to sustain themselves. Similarly, arthropod richness tended to increase as forests

35 matured (Haddad et al, 2001). This in turn would have allowed Specialized Predator ants to re-establish as vegetation succession progressed.

The abundance of Tropical Climate Specialist ants in disturbed and young forests could be explained by the fact that these ants usually nest in tree canopies of primary forests and are not easily collected through methods that sample the ground level (Andersen, 1995). Felling of trees could possibly allow these ants to be sampled in greater proportions in disturbed habitats. In addition, the canopy heights of forests are usually negatively related to maturity (Whitmore, 1998), which would mean that the probability of canopy-dwelling ants being sampled on ground corresponds with the age of the forest.

A further interesting pattern of ant functional group distribution emerged when the among-groups correlations were taken into account. The negative correlations between Cryptic Species, Specialized Predator and Generalized Myrmicinae groups of ants on one hand and the Opportunist and Tropical Climate Specialist ants on the other seemed to indicate that the former three groups were replacing the latter two during vegetation succession.

It would also seem that vegetation succession in secondary rain forests did not affect the relative abundances of the Cold Climate Specialist, Dominant Dolichoderinae,

Hot Climate Specialist and Subordinate Componotini groups. The reason may be because ants of these four functional groups do not exist in large numbers in tropical rain forests and they would not be expected to feature significantly in collection efforts

(Andersen, 1995; King et al, 1998).

While my analysis had uncovered interesting relationships, it was not designed to specifically test the validity of such relationships. The scientific process dictates that

36 hypotheses be formulated before experiments and experiments must specifically address the hypotheses to be tested (Underwood, 1997). Only three hypotheses were formulated and tested by the mega data analysis (see above). Therefore, to validate the relationships that were discovered through the mega data analysis, relevant hypotheses should be generated and tested.

Furthermore, although interesting patterns of ant succession were discovered, no underlying cause for such patterns could be investigated by this analysis. The driving force for these relationships between ants and vegetation succession cannot be the age of forest per se. As stated earlier, long-term changes in environmental conditions are more progressive than short-term fluctuations (Longman and Jenik, 1987). The gradual progress of environmental conditions, such as light levels (Montgomery and Chazdon,

2001), temperature (Didham and Lawton, 1999) and humidity (Whitmore, 1998) among others, towards the original, primary state is closely related to vegetation succession.

Therefore it is possible that such long-term changes in conditions are the main driving force behind the observed relationships between functional groups and forest age.

(ii) Temperate forest

Only Cold Climate Specialist ants were positively related to the age of temperate forests and the regression coefficient had a relatively low value of 0.260. The other functional groups were also significantly less abundant than it. This observation may be because low temperatures generally affect the activities of ants (Holldobler and Wilson,

1990). There is also lower species richness and diversity in areas outside of the tropics

(Bolton, 1994). Therefore, ecological niches in temperate forests are only available to ants that are adapted to thrive in cooler climates. Disturbances in temperate forests

37 could cause a decrease in the abundance of Cold Climate Specialist ants but the other functional groups could not fill the ecological niches. As the forest re-generates, these ants would re-colonize their previous niches.

(iii) Montane forests

It is possible that disturbances to montane forests caused an overall decrease in abundance of ant populations and that these populations recovered simultaneously at an approximately equal rate such that no single functional group could occur in greater abundance than the rest during succession. This possible reason could explain why no functional groups showed any significant increase or decrease of proportional abundance with age.

Mathematical models relating proportions and age

The equations representing the growth and decline of proportions of the respective functional groups conformed very well to the sigmoid model. This mirrored the dynamics of many other biological populations (Sibly and Hone, 2002; Tsoularis and

Wallace, 2002). The results may be interpreted in terms of the general principles of population dynamics (Berryman, 2003) and the competitive interactions between functional groups.

It is believed that Opportunist ants are poorly competitive (Andersen, 1995). In addition, Tropical Climate Specialist ants, being more suited to live in forest canopies

(Andersen, 1995) instead of on the ground, would also compete poorly against ants that

38 live on the ground. Therefore, these two groups would not be expected to hold on to the ecological niches that were presented to them after the forest was disturbed.

As the forest re-generated, the original ant community, made up of functional groups like Cryptic Species, Generalized Myrmicinae and Specialized Predator ants could easily re-occupy those niches. Since the growth in populations of Cryptic Species,

Generalized Myrmicinae and Specialized Predator ants were not likely to be limited by competition, the rate of growth would be exponential after a short initial period of lag, as if empty niches were being filled (Berryman, 2003). Factors such as the carrying capacity of the habitat, ant colony dynamics and competition within these three groups would gradually limit the rate of growth, resulting in a sigmoid curve (Berryman, 2004).

Therefore, the rate of decrease in proportions of Opportunist and Tropical Climate

Specialist ants should correspondingly be that of an initial lag followed by exponential decline to a stable level, resulting in a sigmoid decline curve.

The graphs also indicated that the succession process of these five functional groups of ants could take between 50 to 100 years, possibly more. This is rather similar to that of vegetation succession in rain forests (Longman and Jenik, 1987; Whitmore,

1998). The concurrent succession of ants and vegetation means that it is possible to gauge the progress of one community by knowing that of another. Therefore, we could either estimate the age of a forest from the proportions of functional groups or vice versa. This reinforces the view that ants are good bioindicators of the natural environment (Brown, 1997).

The predictive nature of the models is useful in conservation where stakeholders often need to find indicator organisms that are easy to study. This model is simple enough to be used without extensive training and results may be obtained quickly.

39 However, a limitation of the equations was seen when trying to calculate the age from proportion values (see Equations 1B and 2B). The calculations would break down when y values above or below certain limits returned undefined mathematical solutions.

The age of a habitat cannot be calculated if there were very high or low proportions of respective groups of ants. Furthermore, though the two equations had very high regression coefficients, 0.857 and 0.791 for the growth and decline equations respectively, their validity remains untested. An experiment could be conducted to sample for ants at locations of known ages. The calculated age, from sampling, could then be compared to the actual age to test if these models are valid.

It is clear that refinement to the models need to be made but this attempt at linking the proportions of functional groups of ants with the age of tropical rain forests represented a first step towards the development of more rigorous models relating different aspects of succession ecology, community and population dynamics to one another.

40 CHAPTER 3

ANT SUCCESSION DYNAMICS IN A SECONDARY

FOREST OF SINGAPORE

Introduction

The main island of Singapore is located off the southern tip of the Malay Peninsula and most of the island consisted of tropical lowland rain forest for much of the Holocene

(Corlett, 1992). It was not until A.D. 1819, when the British East India Company established a colonial settlement, that large-scaled and organized deforestation took place (Corlett, 1992). Modernization and urbanization has been rapid and continuous from that time.

The rain forest of Singapore was felled in stages from 1819, initially around the port area of the Singapore River and southern coastline, gradually moving inland and northward (Wong, 1968). Most of the primary vegetation was cleared by 1900 (Wong,

1968). The remaining primary forest was isolated to a single fragment of 71 hectares

(Corlett, 1988) in the Bukit Timah Nature Reserve, which came under legislative protection in 1883 (Polunin, 1981). The main crop that was cultivated in commercial and export quantity for most of the nineteenth century was Uncaria gambir, commonly known as gambir (Jackson, 1965). After the economic decline of the gambir market,

Hevea brasiliensis, or rubber, became the main commercial cultivation until the

41 outbreak of the Second World War, taking up as much as 40% of the total land area at its peak (Corlett, 1992). Subsistence farming took place in smaller scales compared to the planting of commercial crops and became the only form of agricultural farming after the War (Turnbull, 1989).

The Central Catchment Nature Reserve, abbreviated as CCNR for this thesis, is the largest contiguous fragment of secondary lowland rain forest in existence today in

Singapore (Figure 11). The CCNR, with a total surface area of approximately 1700 hectares, consists of vegetation communities at various stages of succession (Wong et al,

1994).

The checkered history of conservation protection is perhaps largely responsible for this fragmented succession pattern. Part of the present-day CCNR first came under protection as early as 1868, after the development of MacRitchie Reservoir, when the secondary forest surrounding the reservoir was named a water catchment reserve

(Anonymous, 2005a). It was not until 1910 that the extent of the water catchment reserve was enlarged north to include the forest surrounding the Peirce Reservoir

(Anonymous, 2005a). The remaining area of the present-day CCNR, north of Peirce

Reservoir, continued to be used for a mixture of small-scale commercial plantation and subsistence farming (Koninck, 1975). The present extent of the CCNR did not receive formal legislative protection until the Nature Reserves Ordinance was enacted in 1951

(Chew, personal communication).

Even with the entire CCNR under protection, it has been continually subjected to human disturbance, both documented and otherwise. For example, small-scale farming continued in various locations right up to the early 1970s when government resettlement of farmers and acquisition of land finally cleared human settlements from

42 the CCNR (Koninck, 1975). The area around Peirce Reservoir was developed extensively in 1975 when a dam and a recreation park were built (Anonymous, 2005a).

A 28-hectare area in the northern limit of the CCNR was cleared and turned into a zoo in 1973 (Anonymous, 2005b). The Singapore military has regularly used large parts of it for training (Chew, personal communication). Most recently, a treetop canopy walkway for the general public was built in an area between MacRitchie and Peirce reservoirs in 2003. Therefore, it is not surprising that vegetation succession at different parts of the CCNR was interrupted at different stages, resulting in a patchwork of habitats at different stages of maturity.

The patchwork of forest habitats in the CCNR represents a vegetation succession chronosequence that encompasses nearly two centuries. Furthermore, Singapore, although small in size, has an ant fauna that is comparable to other forests in this region.

For example, Chong (2003) found 68 morphospecies using baits placed along seven replicates of a 100-meter transect in the CCNR while Yamane et al (1996) collected 51 species in three replicates of a 300-meter transect in Borneo. Therefore, the fragmented nature of succession and the rich ant fauna in the CCNR makes it ideal for the study of ant succession dynamics in the tropics. I was able to use the results of the data analysis that I carried out in Chapter 2 to formulate objectives and hypotheses for my study in

Singapore.

The first objective of this part of the project was to test the relationships between the proportions of functional groups of ants and the ages of forest in Singapore, using various patches of forests at different stages of succession in the CCNR as the study sites. Some of the hypotheses generated on the basis of the mega data analysis in the last chapter were:

43 (i) The proportions of Cryptic Species, Generalized Myrmicinae and

Specialized Predator groups of ants were each positively correlated with

the age of the forest.

(ii) The proportions of Opportunist and Tropical Climate Specialist ants were

each negatively correlated with the age of forest.

(iii) The proportions of Cryptic Species, Generalized Myrmicinae and

Specialized Predator groups were each negatively correlated with that of

the Opportunist group.

(iv) The proportions of Cryptic Species, Generalized Myrmicinae and

Specialized Predator groups were each negatively correlated with that of

the Tropical Climate Specialist group.

The second objective was to explore the relationships between the different functional groups and environmental factors so as to uncover possible reasons for the succession patterns that were observed.

Even though it was known that a limited area around MacRitchie Reservoir had been protected since 1868, it was still difficult to date the age of any patch of forest in the CCNR. This was because there was a scarcity of historical records and the authorities restricted public access to information regarding any development works or disturbance. Therefore, the third and final objective was to use the mathematical models that were developed in Chapter 2 (refer to Equations 1B and 2B) to estimate the age of different parts of the CCNR.

44 ). ed shad tion of the island ( at the central por Nature Reserve located main island. Central Catchment etch map of Singapore k

Figure 11. S

45

Material and Methods

Twenty study sites in the CCNR were chosen to represent forest patches of different relative ages. The exact age of these patches could not be found from historical or geographical record. Therefore, the sites were ranked according to their relative maturity of vegetation succession. There is usually significant correlation between the age of a forest and its state of vegetation succession. For example, the average girth of trees has a strong relationship with the age of a forest (Whitmore, 1998) while species richness of the plant community is also related to the age (Richards, 1996) although diversity usually declines in a primary or near-primary forest (Connell, 1978). Other physical measures such as the extent of canopy cover, height of the main canopy and the thickness of undergrowth also give an indication of the maturity of the forest (Longman and Jenik, 1987).

Wong et al (1994) provided the most recent comprehensive survey of the tree community in the CCNR. Aerial photography and sample plot measurements of tree data was done and the forest classified into four major stages of maturity or succession

(Wong et al, 1994). The forest patches at different stages of succession were ranked as

Forest Types One to Four, with ascending numbers representing increasing maturity or relative age. The information from Wong et al (1994) was integrated into the

Geographical Information System (GIS) at the National Parks Board (NParks) of

Singapore (Chew, personal communication), providing park managers with a map overlay of the approximate stages of vegetation succession at all areas within the CCNR.

Table 2 provides a summary description of the types of vegetation community in each

Forest Type.

46 The National Parks Board provided the GIS information from Wong et al (1994) for this project. Five sites were chosen from each of the four Forest Types as defined by

Wong et al (1994), making a total of 20 study sites. The approximate locations of the study sites are shown in Figure 12. Table 3 lists the geographical co-ordinates of each site.

A reduced version of the ALL protocol was used to sample ants on the ground

(Agosti and Alonso, 2000). At each site, two parallel transects of 100 m, spaced 10 m apart, were marked out. If a site was accessible via a clearly defined forest trail, then the transects were laid at least 10 m away from and parallel to the trail. If there were no nearby trails, then the transects were laid in the general direction of the long axis of that patch of forest and at least 10 m away from the edge of the forest patch. The purpose of laying the transects in this manner was to avoid the edge effect from confounding the results of the samples (Didham and Lawton, 1999).

At each site, bait stations were laid at 10-m intervals along one transect and pitfall traps were placed at 10-m intervals on the other transect. Pitfall traps were cylindrical clear plastic containers with a diameter of 10 cm and a depth of 5 cm. The traps were placed in the ground with their opening flushed along the surface of the ground. Each trap was filled with 100 milliliters of 70% ethanol and 3 ml of glycerol to reduce the volatility of the ethanol (Bestelmeyer et al, 2000). Leaves from the surrounding litter were placed over the openings of each trap to further reduce the evaporation of the ethanol as well as to allow organisms to crawl over trap. Traps were operated for 48 hours at each site.

47 Hard, white plastic sheets of 15 cm square and 0.3 cm thickness were used as bait stations. A teaspoon each of sardine and honey was placed on every bait station, near the center. The bait stations were operated for 90 minutes.

All of the ants found along the stations and traps at the end of the operating times were transferred into 90% ethanol. The ants were identified to genera using

Bolton (1994) and sorted into morphospecies according to visible differences in external morphological features. Each genus was also assigned a functional group using Brown

(2000).

To measure environmental variables, a quadrat with sides of 10 m was marked out in an area bounded by the two transects, between the 45th and 55th meter marks of both transects. The following environmental variables within the quadrat were measured using the respective methods:

(i) Canopy cover

A Lemmon Model C Spherical Densiometer (Lemmon, 1957) was used

to measure the canopy cover at the center of the quadrat. As outlined by

Lemmon (1957), four readings were made at the same spot, each facing

North, South, East and West, and the average calculated.

(ii) Diameter of trees

The diameter of the trees within the quadrat was measured at a height of

1.3 meters above the ground. Only trees with diameters of more than 10

cm were recorded. The large number of smaller and younger tree

saplings were excluded from sampling because they would have made

the data set too large and these extra data would not have provided other

48 useful information pertinent to the project (Wong et al, 1994). The

average measurement was calculated.

(iii) Shrub cover over the ground

The quadrat was bisected on both sides into four smaller equal sub-

quadrats and a visual estimation of the proportion of ground covered by

shrub growth was made. The total shrub cover for the quadrat was

calculated from the recorded values for the four sub-quadrats.

(iv) Temperature and relative humidity

A wooden stake, 70 cm in length, was driven firmly into the ground at

the center of the quadrat. A data logger (HOBO Pro RH/Temp Data

Logger, Part No. H08-032-08. Onset Computer Corporation,

Massachusetts, USA) was secured to the wooden stake with the sensor at

a height of 5 cm above the surface of the leaf litter or ground. The logger

was operated for 48 hours, concurrently with the pitfall traps.

Temperature and relative humidity were recorded hourly. The fluctuation,

maximum, minimum and average values were calculated from the

recordings.

The geographical co-ordinates of each site were read from a Global Positioning

Satellite (GPS) handheld unit (GPSMAP 76S, Garmin Limited, Taipei). The reading was taken at the center of the quadrat. However if the canopy cover prevented readings to be taken, then readings from the nearest position where satellite reception was available were used.

For data analysis, the study sites were ranked by their relative ages according to the Forest Types defined by Wong et al (1994). The total number of ant individuals

49 collected at each site was recorded. The total number for each functional group was also calculated and expressed as a proportion of the total number of individuals. The proportions of Cryptic Species, Generalized Myrmicinae, Opportunist, Specialized

Predator and Tropical Climate Species ants were correlated with the ranked age of the

Forest Type using Spearman’s non-parametric correlation (Zar, 1999). Non-parametric correlation was used because the age of forest was a ranked variable (Zar, 1999). The proportions of Cryptic Species, Generalized Myrmicinae and Specialized Predator ants were each correlated with that of the Opportunist and Tropical Climate Specialist ants using Pearson’s correlation because the data conformed to those of a normal distribution

(Zar, 1999).

To explore the relationship between environmental variables and functional groups, the following procedure was performed:

(i) Non-metric Multidimensional Scaling (NMS) was done, after identifying

and excluding outlier species, to relate species and study sites to one

another in an ordination space, using Sorensen distances (McCune and

Grace, 2002). NMS is an ordination procedure that allows researchers to

express the degree of dissimilarity in the species composition of different

habitats or study sites (McCune and Grace, 2002).

(ii) The site scores of the two dimensions or axes that represented the highest

proportions of variance (r2) in the ordination space were correlated with

the sampled environmental data to identify the environmental variable that

significantly (p < 0.05 for both axes) affected distribution of ant species.

(iii) To test if the ant communities differ significantly among forest patches of

different ages, pair-wise comparisons of scores from each of the four

50 Forest Types were made using Multi-Response Permutation Procedures

(MRPP), a statistical method that compares the distances of different

groups of habitat in ordination space (Mielke and Berry, 2001).

(iv) A plot of species scores and correlation coefficients of significant

environmental variables in the two axes with the highest r2 was done to

show the relationship between species and environmental variables. A

second plot of site and correlation coefficients of significant environmental

variables was also done to show the relationship between forest patches at

different stages of succession and the associated environmental conditions.

Correlation analyses were performed with SPSS for Windows version 11.5 while NMS and MRPP were done using PC-ORD version 4.14 with the “autopilot, slow and thorough” option (McCune and Mefford, 1999).

Equations 1B and 2B from Chapter 2, were used to estimate the mean ages of the four Forest Types in the CCNR. The mean of summed proportions of Cryptic

Species, Generalized Myrmicinae and Specialized Predator functional groups in each

Forest Type were used to calculate the age with Equation 1B. The mean of summed proportions of Opportunist and Tropical Climate Specialist functional groups in each

Forest Type were used to calculate the age with Equation 2B.

51 Table 2. Description of the typical vegetation found in each of the four Forest Types in Singapore, based on Wong et al (1994).

Forest Type Description of vegetation 1 Early succession vegetation, mostly open ground with tall shrubs and grass. Dicranopteris and Smilax abundant.

2 Mixture of open shrub/grass with aggregates of trees 8 to 10 meters tall. Tree canopy present but sparse. Dicranopteris and Smilax are less abundant, secondary forest trees like Adinandra and Rhodamnia present.

3 Vegetation with larger trees 10 to 20 meters tall. Tree canopy continuous. Secondary trees abundant. Higher species diversity than Type 2.

4 Generally tallest trees of the entire CCNR exist here. Primary forest trees present (e.g. Dipterocarpaceae family). Multi-storey canopy structure with tall emergent trees visible above main canopy.

52

Figure 12. Study sites and transects in the Central Catchment Nature Reserve. Thin lines represent approximate route of forest trails. Forest trail routes were first obtained from National Parks Board, Singapore, and subsequently confirmed by hiking and mapping with a GPS handheld device. Darkened areas represent reservoirs. ‘MR’ = MacRitchie Reservoir, ‘UP’ = Upper Peirce Reservoir, ‘LP’ = Lower Peirce Reservoir and ‘US’ = Upper Seletar Reservoir. Study sites are marked with combination numerals and letters of the alphabet to denote Forest Types and replicate respectively, e.g. ‘2A’ = Forest Type 2, replicate A.

53 Table 3. Study site, forest type and environmental variables.

Study Forest GPS co- Canopy Tree Shrub Temperature (oC) Relative humidity site Type ordinates cover diameter cover (%) (%) (cm) (%) High Low Mean High Low Mean (SE) (SE) 1A 1 N 01o 20.941’ 0.0 0 100 35.3 25.7 30.6 93.8 79.9 87.9 E 103o 48.567’ (0.42) (0.82) 1B 1 N 01o 23.993’ 0.0 0 96 36.0 25.6 31.0 97.3 79.1 89.4 E 103o 48.106’ (0.51) (0.79) 1C 1 N 01o 23.619’ 6.2 0 80 36.3 24.3 32.8 91.4 76 84.3 E 103o 46.551’ (0.46) (0.84) 1D 1 N 01o 21.608’ 8.3 0 76 37.3 24.8 34.7 96.2 84.4 91.1 E 103o 48.742’ (0.42) (0.86) 1E 1 N 01o 22.757’ 12.5 0 66 37.7 24.0 34.3 93.7 81.5 88.9 E 103o 47.078’ (0.53) (0.88) 2A 2 N 01o 20.487’ 38.5 0 98 33.0 24.3 28.5 100 87.5 95.8 E 103o 48.932’ (0.44) (0.81) 2B 2 N 01o 22.895’ 48.9 0 89 33.1 24.1 28.1 99.4 77.7 89.6 E 103o 48.610’ (0.52) (0.76) 2C 2 N 01o 22.925’ 59.3 61 42 34.1 24.9 29.9 98.6 84 91.3 E 103o 48.436’ (0.39) (0.81) 2D 2 N 01o 22.901’ 62.4 77 81 34.9 23.5 30.3 100 80.7 91.4 E 103o 47.280’ (0.39) (0.77) 2E 2 N 01o 23.069’ 72.8 90 71 36.0 23.9 32.9 100 86.5 92.3 E 103o 46.671’ (0.41) (0.80) 3A 3 N 01o 21.109’ 63.4 132 85 28.9 22.6 26.1 100 81.6 90.4 E 103o 49.339’ (0.38) (0.76) 3B 3 N 01o 21.375’ 68.6 150 68 29.6 23.3 25.5 100 87.6 97.6 E 103o 48.401’ (0.41) (0.82) 3C 3 N 01o 21.268’ 83.2 198 22 29.2 22.2 26.0 100 90.7 96.7 E 103o 48.276’ (0.32) (0.71) 3D 3 N 01o 22.108’ 91.5 115 46 31.0 23.7 27.6 100 91.1 94.7 E 103o 47.280’ (0.40) (0.77) 3E 3 N 01o 22.848’ 95.7 181 32 31.1 23.7 27.6 100 89.1 91.6 E 103o 47.756’ (0.36) (0.73) 4A 4 N 01o 20.984’ 71.8 166 39 29.0 23.1 25.0 100 83.2 91.7 E 103o 48.850’ (0.38) (0.69) 4B 4 N 01o 21.003’ 79.0 209 33 29.5 23.3 26.6 100 90.4 95.3 E 103o 48.893’ (0.37) (0.62) 4C 4 N 01o 21.061’ 86.3 197 25 30.0 23.6 25.9 99.8 88.2 96.2 E 103o 48.734’ (0.31) (0.71) 4D 4 N 01o 23.153’ 91.5 203 17 30.6 23.7 26.5 100 89.1 95.9 E 103o 47.949’ (0.35) (0.63) 4E 4 N 01o 20.636’ 92.6 218 6 31.2 24.0 27.2 100 85.3 92.7 E 103o 49.536’ (0.34) (0.66)

54 Results

A total of 1442 individuals from 73 morphospecies in 40 genera were collected. The richest site yielded 33 morphospecies while 4 morphospecies were collected from the least rich site. The morphospecies, number of individuals collected and the functional groupings are listed in the Appendix B.

Age-proportion and between-proportions correlations

The proportions of Cryptic Species (Figure 13A), Generalized Myrmicinae (Figure

13B) and Specialized Predator (Figure 13C) ants were positively correlated with ranked age of forest patch while the proportions of Opportunist (Figure 14A) and Tropical

Climate Specialist ants (Figure 14B) were negatively correlated with ranked age.

The proportions of Cryptic Species (Figure 15A), Generalized Myrmicinae

(Figure 15B) and Specialized Predator (Figure 15C) ants were negatively correlated with the proportion of Opportunist ants. In addition, the proportions Cryptic Species

(Figure 16A), Generalized Myrmicinae (Figure 16B) and Specialized Predator (Figure

16C) ants were negatively correlated with the proportion of Tropical Climate Specialist ants.

Ant succession in relation to environmental conditions

NMS produced an ordination space of three significant dimensions and these three dimensions or axes represented 76.5% of the variance in species data (Table 4). The

55 second and third axes represented 27.2% and 32.6% of the variance respectively while the first axes had the lowest representation of 16.7%. The species scores had a stress value of 15.4, which falls within an acceptable range of 10 to 20 for most ecological community data (McCune and Grace, 2002). Four environmental variables, canopy cover, diameter of trees, relative humidity and fluctuation in temperature were significantly correlated with the site scores of the second and third axes (Table 4).

Pair-wise comparisons of distance scores between different Forest Types, using

MRPP, showed that the ant communities in the four Forest Types were significantly different (Table 5). Comparison between Forest Types 1 and 4 (i.e. greatest difference in relative age) yielded the most negative T value while comparisons between Forest

Types with the least difference in relative age (e.g. Forest Types 1 vs. 2, 2 vs. 3 or 3 vs.

4) had the least negative T value (Table 5). A greater negative value indicated greater distinctiveness or dissimilarity in community.

The species scores were plotted on the second and third axes, along with the correlation coefficients of significant environmental variables (Figure 17A). The

Opportunist and Tropical Climate Specialist functional groups were associated with environment conditions of high temperature fluctuation, with the former group having a stronger association than the latter. The Cryptic Species, Generalized Myrmicinae and

Specialized Predator groups were associated with environments with higher canopy cover, higher relative humidity and having trees with greater diameter.

Site scores, together with the correlation coefficients of the significant environmental variables, were also plotted on the second and third axes (Figure 17B).

Forest Type 1 was associated with the highest fluctuation in ambient temperature, followed by Forest Type 2. Forest Types 3 and 4 had environments with higher canopy

56 cover, greater tree diameter and higher relative humidity. It may also be clearly seen the scores for Forest Type 1 (i.e. youngest relative age) were clustered around the lower left quadrant of the plot (i.e. most negative scores along both axes) and Forest Types of increasing relative age (i.e. 2, 3 and 4) had increasing scores for both axes.

Estimating the ages of different patches of forest

The estimated mean ages of each Forest Type using the two equations were calculated and shown in Figure 18. The mean ages of Forest Type 1 calculated from both models were not significantly different (2-tailed independent t-test: t7 = -1.321, p = 0.203). In addition, there was no significant difference between the mean ages of Forest Type 2 calculated from the two models (2-tailed independent t-test: t8 = -0.264, p = 0.798).

The mean ages of Forest Types 3 and 4 were undefined for Equation 1B because the mean proportions of functional groups did not lie within the range of values permitted by the equation (i.e. the calculations involved finding the natural log of negative numbers, which is undefined).

57

A

0.4 r = 0.699 es p < 0.01 eci p 0.2 c S i t p y r C

0.0 1234

B 0.8 ae r = 0.535 p < 0.05 icin m

Myr 0.4 ralized e n e

G 0.0 1234

C 0.6 r o

at r = 0.738 ed

r p < 0.01

ed P 0.3 z i al eci p S 0.0 1234

Ranked age

Figure 13. Correlation between proportions of functional groups and the ranked age of Forest Type. Vertical axes show proportions of functional group in each sample. Horizontal axes show ranked ages.

58

A 0.4

r = -0.752 t s p < 0.01 uni 0.2 Opport

0.0 1234

B

0.6 r = -0.637 p < 0.01

ate Specialist 0.3

0.0 Tropical Clim 1234

Ranked age

Figure 14. Correlation between proportions of functional groups and the ranked age of Forest Type. Vertical axes show proportions of functional group in each sample. Horizontal axes show ranked ages.

59

A 0.4 r = -0.464 es p < 0.05 eci p

S 0.2 c i t p y r C

0.0 0.0 0.2 0.4

B

e 0.8

ina r = -0.618 ic

m p < 0.01 r y

M 0.4 d lize a r e n e

G 0.0 0.0 0.2 0.4

C 0.6

or r = -0.560

edat p < 0.05 r d P

e 0.3 z i l a eci p S 0.0 0.0 0.2 0.4

Opportunist

Figure 15. Correlations of proportions of Cryptic Species, Generalized Myrmicinae and Specialized Predator groups with Opportunist group.

60

A 0.4 r = -0.523 es p < 0.05 eci p 0.2 c S i t p y r C

0.0 0.0 0.3 0.6

B

e 0.8 a n i r = -0.448 c i p < 0.05 rm

0.4 d My e z i l ra ne

Ge 0.0 0.0 0.3 0.6

C 0.6 r o

at r = -0.446 ed

r p < 0.05

ed P 0.3 z i al eci p S 0.0 0.0 0.3 0.6

Tropical Climate Specialist

Figure 16. Correlations of proportions of Cryptic Species, Generalized Myrmicinae and Specialized Predator groups with Tropical Climate Specialist group.

61 Table 4. Variance in species data (r2) represented by the three axes of ordination and the coefficients of correlation of significant environmental variables with axes two and three (i.e. axes with the highest variances).

Axis 1 Axis 2 Axis 3

Variance represented (r2)

Incremental 0.167 0.272 0.326

Cumulative 0.167 0.439 0.765

Correlation co-efficient (r)

Canopy cover 0.560 0.644

Diameter of trees 0.493 0.562

Temperature (fluctuation over 48-hour period) -0.560 -0.490

Relative humidity (mean over 48-hour period) 0.517 0.561

62

Table 5: MRPP Results of average within-group (Forest Type) distances and pair-wise comparisons between groups.

Forest Type Average within-group distance

1 0.945

2 0.778

3 0.811

4 0.840

Pair-wise comparisons T A p

1 vs. 2 -2.815 0.034 < 0.01

1 vs. 3 -3.055 0.048 < 0.01

1 vs. 4 -3.057 0.031 < 0.01

2 vs. 3 -2.752 0.037 < 0.01

2 vs. 4 -3.049 0.037 < 0.01

3 vs. 4 -2.225 0.032 < 0.05

63

1.5

X X 1 X 2 X X X X 3 X 3 0.0 -1.5 0.0 1.5 Axis Dominant Dolichoderinae 4 Generalized Myrmicinae Opportunist Subdominant Camponotini Specialized Predator Tropical Climate Specialist -1.5 X Cryptic Species

1.5

1 2 3 3 0.0 -1.5 0.0 1.5 Axis

4 Forest Type 1 Forest Type 2 Forest Type 3 Forest Type 4 -1.5 Axis 2

Figure 17. NMS plot of (A) species and (B) site scores with significantly correlated environmental variables. Species are differentiated according to the functional groups. The angles and lengths of the four environmental variables indicate the direction and strength of relationships of the variables with the ordination scores. ‘1’ = canopy cover, ‘2’ = diameter of trees, ‘3’ = mean relative humidity over 48-hour period and ‘4’ = temperature fluctuation over 48-hour period.

64

180

Age estimates using Equation 1B 90 Age estimates Age using Equation 2B

0 1234

Forest Type

Figure 18. Estimated mean age of different Forest Types. Vertical axis shows age in years. Horizontal axis shows Forest Types. Error bars are 95% confidence intervals, which were calculated using the method outline by Zar (1999, p342).

65 Discussion

Age-proportion and between-proportions correlations

The proportions of Cryptic Species, Generalized Myrmicinae and Specialist Predator groups of ants increased with the age of a secondary rain forest while the proportions of

Opportunist and Tropical Climate Specialist functional groups decreased with age. This generalization is supported by the observation that the former three groups of ants were associated with forest patches that had trees of greater diameters while the latter two groups showed the reverse association. In addition, the site scores on the two ordination axes suggested that higher values on both axes were associated with older forest patches.

It seemed that these five groups of ants succeeded one another as the forest matured. The Opportunist group established itself in younger forest patches, followed by the Tropical Climate Specialist group. The Cryptic Species, Generalized Myrmicinae and Specialized Predator groups of ants replaced the earlier two groups as the forest matured. This is clearly seen by the species scores of the various groups. Opportunist and Tropical Climate Specialist groups had lower scores on both axes while Cryptic

Species, Generalized Myrmicinae and Specialist Predator groups had higher scores.

Ant succession in relation to environmental conditions

One of the reasons for the observed pattern of succession in the ant community appeared to be the preferential establishment of certain functional groups in specific environmental conditions. This is because Opportunist and Tropical Climate Species

66 ants were associated with habitats that had higher fluctuations in temperatures, lower relative humidity and lower canopy cover, all of which were conditions found in young and recently cleared forests (Whitmore, 1998). The Cryptic Species, Generalized

Myrmicinae and Specialist Predator groups were associated with habitats that had the opposite environmental conditions, which were usually found in older forests with relatively advanced stages of vegetation succession (Whitmore, 1998).

It would seem that Opportunist ants, which favor environments that were highly disturbed, are able to establish themselves in younger and recently disturbed areas whereas the other groups could not do so in large numbers. However as vegetation succession took place, the Cryptic Species, Generalized Myrmicinae and Specialized

Predator groups of ants seemed to be able to establish themselves concomitantly with the environmental conditions approximating those of a mature or primary forest. Being poorly competitive, the Opportunist ants would be ousted from their ecological niche.

A closer examination of the NMS plots (Figure 17) showed that Tropical

Climate Specialist ants were more strongly associated with Forest Type 2 than Type 1.

Forest Type 2 typically has trees of low stature and some degree of canopy cover. The relative low height of the tree canopy in Forest Type 2 meant that ants of the Tropical

Climate Specialist functional group, which usually nest in tree canopies (Andersen,

1995) and are seldom collected in large numbers by ground sampling techniques (Bruhl et al, 1998), had a greater tendency to reach the ground level during the course of foraging. This may explain the greater abundance of this group of ants in Forest Type 2 samples.

Cryptic Species ants nest and forage in and on the ground (Andersen, 1995). It is reasonable to expect changes in soil characteristics to affect the recruitment success of

67 this group of ants. Soil changes and recovery during the process of forest clearance and succession (Lavelle and Spain, 2001) could explain the low abundance of Cryptic

Species ants in younger forests and the rise in numbers together with soil property recovery and forest succession.

Generalized Myrmicinae ants are known to recruit rapidly at food sources and they prefer to nest in the leaf litter of forest where it is cooler and more humid than open spaces (Andersen, 1995). Therefore they would be expected to be collected in abundant numbers by ground sampling techniques in older forests.

A loss of prey species would affect the predator population, especially if the predator has a strong relationship with the affected prey species (Donald and Andersen,

2003). The loss and recovery of arthropod biodiversity (McGeoch, 2002) in a forest that is initially cleared and subsequently left to regenerate would mean that the population of

Specialized Predator ants, which prey on other arthropods (Andersen, 1995), would be affected in a similar manner.

This part of the project validated hypotheses about the changes in proportions of functional groups of ants in relation to the age of a forest and it demonstrated that certain functional groups of ants were associated with certain environmental conditions.

However it did not take other ecological factors into consideration. For example, it is known that there is an abundant insect fauna in the tree canopies of tropical rain forests

(Ellwood and Foster, 2004) while this project only considered ants that forage on the ground. The community dynamics and responses of canopy-dwelling ants to disturbances should be studied closely, especially their reactions to widespread clearance of trees.

68 The recruitment success of Opportunist ants in disturbed forests was thought to be dependent on the lack of competition from other functional groups. This inter-group dynamics needs to be examined to elucidate the exact mechanism that determines the hypothesized competitive failure of Opportunist ants against other groups. In addition, while the competitive nature of the Generalized Myrmicinae ants had been partly attributed to their ability to respond rapidly to available food sources (Andersen, 1995), it is not known how these ants are able to respond faster than others and how they exclude other ants from reaching the same food source. Studies into these aspects will yield interesting results and improve understanding of ant behavior and community interactions.

It was suggested that Cryptic Species ants would establish themselves in the right soil condition (Andersen, 1995). It is known that soil characteristic such as bulk density, compaction, porosity and fertility change concurrently with vegetation succession (Lavelle and Spain, 2001). What is not known are the kinds of specific soil characteristics or dynamics that would allow this functional group to thrive. Studying the response of these ants to alterations in soil properties and processes would be helpful.

The relationship between predator and prey is complex and there are many factors affecting it in any ecosystem (Sih and Wooster, 1994). Community dynamics such as recruitment rates, the strength of the predator-prey link as well as interactions with other species all combine to influence the population ecology of both predator and prey species (Sih and Wooster, 1994; Donald and Andersen, 2003; Schenk et al, 2005).

It was hypothesized that the Specialist Predator group would need a certain capacity of prey species in a habitat before being able to establish itself (Andersen, 1995). While it

69 is had been shown that mature forests held a greater abundance of arthropod communities (Haddad et al, 2001), which would boost predator numbers, there is a need for further studies into the relationship between Specialist Predator and arthropod

(especially prey species) abundances.

Estimating the ages of different patches of forest

The estimated ages of Forest Types were in agreement with the given ranks of ages (i.e.

Forest Type 1 was the youngest and Type 4 the oldest). The ages of Forest Types 1 and

2 calculated from the two equations were similar to each other. The similarity in the estimated ages allows both equations to be used simultaneously when sampling. This helps in overcoming the limitations of each equation. For example, Equation 1B may not be used if the summed proportions of Cryptic Species, Generalized Myrmicinae and

Specialized Predator functional groups exceeded 0.769, which would result in calculating the natural log of a negative number, an undefined value. A similar limitation applies to Equation 2B, where the age of a forest cannot be calculated if the summed proportions of Opportunist and Tropical Climate Specialist functional groups exceed 0.883. Therefore, if the age of a forest could not be estimated from one equation, then the second equation could still be used. These limitations also emphasized the need to consider the ant community as a whole rather than rely on data from any single functional group or species when attempting any ecological studies.

It is known that rain forest succession is a complex process involving many predictable biotic and abiotic factors together with stochastic events. Therefore, one would expect an improved model to include many other community dynamics and

70 environmental variables. A more complex equation factoring other functional groups of ants and even other types of fauna and flora may better relate age with community abundance data.

The challenge in predictive ecology is managing and finding an acceptable compromise between developing precise models and reducing the complexity of such models. Models that have high fidelity usually involve complex expressions of variables and constants that do not have any significant meaning in terms of physical dimensions and, therefore, do not explain the underlying mechanisms very well (Babovic, 2005).

However, models that are simple to explain are often not as good in predicting outcomes (Babovic, 2005).

At the very least, however, the models have shown that certain groups of ants may be used to indicate the age of a forest. I have also demonstrated that the succession of ants, driven in part by environmental processes, involved replacement of defined species with others over a predictable period of time. In addition, the development of these simple mathematical models represented a first attempt at giving researchers a useful basis for comparing ages of different forests and for further research in the field of modeling and predicting natural processes.

71 CHAPTER 4

GENERAL DISCUSSION

The main aim of this project, which was to explore the distribution pattern and succession ecology of functional groups of ants in relation to forest succession, was fulfilled through studies conducted and reported in the previous chapters.

In Chapter 2, I analyzed abundance data from ant studies around the world. Data from studies of six different types of landscapes were analyzed and these were: tropical lowland rain forests, deserts, temperate forests, tropical grasslands, tropical bushlands and montane forests.

The most abundant functional groups of ants in tropical lowland rain forests were the Generalized Myrmicinae and Opportunist groups. King et al (1998) also showed this pattern of dominance in rain forests. Hot and Cold Climate Specialist functional groups were the most abundant in deserts and this was probably due to the severe daily changes in temperatures between days and nights (Goudie, 2002), limiting the species of ants that were able to establish itself in this environment. Climate requirements could also be the main reason behind the abundance of Cold Climate

Specialist ants in temperate forests. There was no functional group that was clearly abundant in tropical grasslands while the Cryptic Species group of ants was the most abundant in both tropical bushlands and montane forests. A possible reason for the dominance of Cryptic Species, which live exclusively in the ground, in bushlands and

72 montane forests could be that the vegetation in these ecosystems do not have the stature and complexity (Siebert, 2005) to support other groups of ants.

The studies in tropical rain forests, temperate forests and montane forests also included data from areas that were cleared for human development and subsequently abandoned and left to re-generate, so I analyzed the proportional abundances of the different functional groups in relation to the age of vegetation succession in these forests. Within tropical rain forests, three functional groups – Cryptic Species,

Generalized Myrmicinae and Specialized Predator, increased with the age of vegetation succession while two groups – Opportunist and Tropical Climate Specialist, decreased with age. In temperate forests, only the Cold Climate Specialist group showed an increase with the age of the forest. In montane forests, the proportions of all functional groups were not significantly related to the age of forest.

After identifying the functional groups with proportional abundances that changed significantly with the age of the forests, I described the relationship between the proportions of these different functional groups. This was done in order to detect any patterns of succession within the ant communities of re-generating forests. In tropical rain forests, the proportions of Cryptic Species, Generalized Myrmicinae and

Specialized Predator were negatively correlated with those of Opportunist and Tropical

Climate Specialist. In temperate forests, the proportions of functional groups were not significantly correlated with one another.

It may be seen from the results that a definite pattern of ant succession existed in secondary tropical rain forests, with one set of ant community replacing another. This phenomenon was not observed in temperate forests and it could be due to the low temperatures in the temperate region limiting the ecological release of other functional

73 groups when the abundance of the dominant group (i.e. Cold Climate Specialist) was affected by disturbance.

Using the abundance data from tropical studies, I was able to develop mathematical models to relate the population dynamics of different functional groups with the age of a forest. The sigmoidal growth and decline models (Otto and Whitlock,

1997) best described the respective increases and decreases in proportions of Cryptic

Species, Generalized Myrmicinae and Specialized Predator, Opportunist and Tropical

Climate Specialist functional groups with age. The sigmoid model is usually seen in the population dynamics of many biological species and has been well described in scientific literature (Sibly and Hone, 2002; Tsoularis and Wallace, 2002). In temperate forest, only the linear model best described the growth of Cold Climate Specialist proportions with age. These mathematical models were the first that enabled researchers to estimate the age of a forest by sampling the ant community.

In Chapter 3, I conducted ant sampling within a secondary tropical rain forest in

Singapore and validated the relationships between proportional abundances of functional groups and the age of tropical rain forest that were discovered through the data analysis in Chapter 2. The correlations in proportional abundances among the functional groups were also confirmed. In addition, I uncovered key environmental factors that may explain the succession dynamics of ants in tropical rain forests. Higher fluctuations in temperature, lower humidity and lower canopy cover, which were conditions found in young and recently disturbed forests were associated with functional groups that established themselves in the early stages of vegetation succession. The reverse conditions in mature forests were associated with functional groups that were dominant during the later stages of succession. Finally, the ages of

74 different patches of a secondary forest in Singapore were also estimated using the mathematical models that were developed in Chapter 2.

Succession is a complex process and ecologists usually try to explain changes in terms of general trends and patterns. Here I showed that the succession dynamics of ants in tropical rain forests could be explained on a very general level, in terms of a community of species that were the initial colonizers of a disturbed forest followed by the gradual replacement with another community of species that establish themselves as the forest matures. Therefore, it is reasonable to introduce the concept of “pioneer” and

“climax” species (Whitmore, 1998) to described the initial and subsequent ant communities, much like that of vegetation. This parallel between ants and plants is not surprising and had been proposed a number of times, notably by Andersen (1995), who first introduced the concept of functional groups based on the ecological niches and strategies of plants. This concept of pioneer and climax ant species is potentially a useful tool in conservation. For example, knowing the proportions of these two communities of ants in a maturing forest could possibly allow forest managers to gauge the stage of succession of a forest and initiate intervention measures to maintain the well-being of fragile areas where necessary.

The observed succession dynamics of ant in tropical rain forests has generated a few interesting questions that warrant further study. How environmental factors influence the recruitment and establishment of various species of ants is unknown.

Although the association of groups of species with certain sets of environmental conditions had been demonstrated, it would be interesting to study the real-time responses of ant colonies to changes in these conditions, especially changes that are brought about by habitat disturbances. The interactions between ants and other

75 organisms in a maturing forest should also be examined. It is known that ants form symbiotic relationships with many plants and animals and these relationships may be important determinants of the outcome of forest succession. This is because ants are known to be ecosystem engineers (Jones et al, 1994). Cherret (1989) estimated that leaf- cutter ants reduced the annual leaf production of tropical forests while Paton et al (1995) calculated that ground ants were responsible for the second highest rates of soil turbation after earthworms. Furthermore Lavelle and Spain (2001) reported that levels of mineralized nitrogen, phosphorus and potassium in the soil over the nests of ants were higher than that in adjacent areas. The sensitivity of these relationships to disturbances needs to be examined. For example, the changes in food web dynamics in response to habitat disturbance could be examined in the form of a food-preference study. While the ecosystem engineer role of ants had been documented, the existence, or otherwise, of keystone species remains a mystery. There have been studies describing the impact of exotic ant species on local communities (Breton et al, 2003) but a good way to identify possible keystone ant species is to conduct species removal experiments to monitor the impact of a controlled local extinction.

At a time when the rate of exploitation of forest resources is high (Achard et al,

2002), finding new knowledge in ecological succession is all the more important because it allows us to implement mitigation measures for the purposes of ecological restoration. One of the ways in which we can monitor ecosystems is to look for changes in the environment, usually by selecting factors or indicators that respond to changes in the ecosystem. These indicators may be biotic or non-biotic in nature. Biotic factors, usually a single or small group of species, are known as bioindicators (Cook, 1976).

Observing such responses in indicator organisms allows stakeholders of the

76 environment to detect and assess disturbances, which may not be obvious. For example, the presence of organohalogen in polar bears indicates a certain level of pollution within the Arctic Circle (Kirkegaard et al, 2005). Certain plant species are used as indicators of soil nitrogen content and depth of groundwater (Kovacs, 1992).

In essence, there are key features that make certain species suitable bioindicators.

Cook (1976) suggested that such species should have specific, predictable and measurable responses to the environmental changes under investigation. Indicator species should also occur in enough numbers or be easily sampled (Cook, 1976).

Insects are particularly useful for indicating levels of human disturbance in forests, due, in part, to their great diversity and abundance. Brown (1997) has a good review on the suitability of the different insect orders for the purpose of bioindication.

In the review, Brown (1997) considered ants, together with butterflies, as the most suitable type of insects to be used as bioindicators. That favorable assessment of the suitability of ants as bioindicators is not surprising because they are easily sampled at low cost (Bestelmeyer et al, 2000), occur in large numbers across different habitat types

(Holldobler and Wilson, 1990), taxonomic identification is relatively simple (Bolton,

1995) and, as I had demonstrated in this project, community structure and population dynamics changed predictably with changes in the habitat.

There have been some restoration and rehabilitation projects that used ants as bioindicators and these were done mostly in Australia. Andersen et al (2002) used changes in ant communities to monitor the level of sulphur dioxide pollution around lead and copper processing facilities. Ants have also been used to assess the effectiveness of bauxite mine rehabilitation in Western Australia (Majer, 1983). There is little known effort to use ants as bioindicators outside of the Australian continent. In this

77 project I showed that the community dynamics of ants reflected changes in vegetation succession and demonstrated that ants could be used as bioindicators in tropical rain forests around the world in a practical manner.

Perhaps the biggest challenge that has yet to be met is the establishment of long- term study sites in secondary forests to sample the ant fauna at regular intervals over many years (Folgarait, 1998). This is because, for chronosequential studies across different forests, any observed variation in communities could be attributed to biogeographical differences that may be inherent when comparing different sites

(Cornell and Lawton, 1992). Even though I attempted to overcome this by sampling in a contiguous forest over a relatively small area, the best way to overcome biogeographical difference as a confounding factor is to study an ant community within the same site over a time period.

In addition to uncovering a general pattern of ant community changes with the age of forests, I proposed a mathematical model that linked the proportional abundance of functional groups of ants to the age of vegetation succession in secondary tropical rain forests. One of the challenges of ecological studies is the development of predictive models (Brook et al, 2000). This is usually achieved from observing limited sets of variables in the ecosystems and using the information from these observations to make logical extrapolations about how ecosystems would change when certain conditions change. Much like bioindication, predictive models are important to conservation biology where such models could serve as early warning systems to avert possible future ecological crisis (Brook et al, 2000).

Without good historical records, it is difficult to date the age of a patch of rain forest. This is especially so in areas outside of reserves, where there is usually no

78 administrative mechanism for record keeping. In addition, there is uncontrolled deforestation and unsustainable exploitation of forests outside of reserves (DeFries et al,

2005). Therefore, there is an urgent need not only to conserve what remains but also to rehabilitate forests that had been exploited and subsequently abandoned when the commercial returns were exhausted. A forest that was recently disturbed would be ecologically different from one that had been maturing for a longer period (Whitmore,

1998). The ability to predict the age of a forest would allow appropriate restoration plans to be put in place. Forest managers could also use predictive models to monitor the progress of succession in rehabilitating forests.

There are many interesting questions that remain unanswered. For example, the mathematical models that I proposed reflected the process of forest succession using only one aspect of ant community dynamics. The simplicity of the proposed model is, at once, both its strength and weakness. A simple model offers a quick assessment that may be used by both trained and untrained surveyors. However, the complexity of ecological systems demands correspondingly more complex models factoring in many variables, in order to achieve higher fidelity (Babovic, 2005). It would be fascinating to assess the contribution of ant communities to ecosystems by incorporating their succession dynamics into Markov models (Tanner et al, 1996) to predict various outcomes in different habitats.

The roles of other functional groups, such as the Dominant Dolichoderinae and

Subordinate Camponotini groups, were not examined in detail because they did not contribute greatly in terms of the numbers sampled. However, this did not mean that the quality of their contribution to the ecosystem was any lesser. Their ecological roles should be examined in detail.

79 Perhaps one of the biggest mysteries is the succession dynamics of canopy ants.

Given that disturbances to forests often involved felling of trees, one would expect the community of canopy ants to undergo drastic changes during forest succession. The partitioning of discrete communities of ants between the ground level and the canopy had been demonstrated (Bruhl et al, 1998) and this point to a strong possibility that succession dynamics are different in these two different habitats. Further studies could be conducted to investigate the differences in communities of ants at different canopy heights as well as to explore the interactions between canopy and ground ants.

In summary, the succession ecology of ants is an important field with potential contributions to conservation biology and restoration ecology. Much is known about their ecological roles in forests over the world but much more remains to be discovered and explained.

80 REFERENCES

Achard, F., Eva, H. D., Stibig, H. J., Mayaux, P., Gallego, J., Richards, T. and

Malingreau, J. P. 2002. Determination of deforestation rates of the world's humid

tropical forests. Science 297: 999-1002.

Agosti, D. and Alonso, L. E. 2000. The ALL protocol: a standard protocol for the

collection of ground-dwelling ants. In: Agosti, D., Majer, J. D., Alonso, L. E. and

Schultz T. R. eds. Ants: standard methods for measuring and monitoring biodiversity

pp 204-26. Smithsonian Institution Press, Washington.

Andersen, A. N. 1986. Diversity, seasonality and community organization of ants in

adjacent heath and woodland sites in south-eastern Australia. Australian journal of

zoology 34: 53-64.

Andersen, A. N. 1991. Parallels between ants and plants: implications for community

ecology. In: Huxley, C. R. and Cutler, D. F., eds. Ant-plant interactions pp 539-558.

Oxford University Press, Oxford.

Andersen, A. N. 1995. A classification of Australian ant communities, based on functional

groups which parallel plant life-forms in relation to stress and disturbance. Journal of

biogeography 22: 15-29.

Andersen, A. N. 1997. Functional groups and patterns of organization in North America

ant communities: a comparison with Australia. Journal of biogeography 24: 433-460.

Andersen, A. N., Hoffman, B. D., Muller, W. J. & Griffiths, A. D. 2002. Using ants as

bioindicators in land management: simplifying assessment of ant community

81 responses. Journal of applied ecology 39: 8-17.

Andersen, A. N. and Majer, J. D. 2004. Ants show the way Down Under: invertebrates as

bioindicators in land management. Frontiers in ecology and the environment 2: 291-

298.

Anonymous. 2005a. Bukit Timah Nature Reserve and Central Catchment Nature Reserve:

History & Attractions. 1st December 2005.

http://www.nparks.gov.sg/nparks_cms/display_level2.asp?parkid=8&catid=2#central

Anonymous. 2005b. Singapore Zoo: Fast Facts. 1st December 2005.

http://www.zoo.com.sg/about/fastfacts.htm

Babovic, V. 2005. Data mining in hydrology. Hydrological processes 19: 1511-1515.

Basu, P. 1997. Seasonal and spatial patterns in ground foraging ants in a rain forest in the

Western Ghats, India. Biotropica 29: 489-500.

Beattie, A. J., Turnbull, C. L. Hough, T. and Knox, R. B. 1986. Antibiotic production: a

possible function for the metapleural glands of ants (Hymenoptera: Formicidae).

Annals of the Entomological Society of America 79: 448-450.

Bennett, E. M., Peterson, G. D. and Levitt, E. A. 2005. Looking to the future of ecosystem

services. Ecosystems 8: 125-132.

Berghoff, S. M., Maschwitz, U. & Linsenmair, K. E. 2003. Influence of the hypogaeic

army ants Dorylus laevigatus on tropical arthropod communities. Oecologia 135:149-

157.

Berryman, A. A. 2003. On principles, laws and theory in population ecology. Oikos 103:

695-701.

Berryman, A. A. 2004. Limiting factors and population regulation. Oikos 105: 667-670.

Bestelmeyer, B., Agosti, D., Alonso, L. E., Brandao, C. R. F., Brown, W. L., Delabie, J.

82 H. C. and Silvestre, R. 2000. Field techniques for the study of ground-dwelling ants:

an overview, description and evaluation. In: Agosti, D., Majer, J. D., Alonso, L. E. and

Schultz T. R. eds. Ants: standard methods for measuring and monitoring biodiversity

pp 122-144. Smithsonian Institution Press, Washington.

Bestelmeyer, B. T. and Wiens, J. A. 1996. The effects of land use on the structure of

ground-foraging ant communities in the Argentine chaco. Ecological applications

6:1225-1240.

Bolton, B. 1994. Identification guide to the ant genera of the world. Harvard University

Press, Cambridge, Massachusetts.

Bolton, B. 1995. A new general catalogue of the ants of the world. Harvard University

Press. Cambridge, Massachusetts.

Breton, J., Chazeau, J. and Jourdan, H. 2003. Immediate impacts of invasion by

Wasmannia auropunctata (Hymenoptera: Formicidae) on native litter ant fauna in a

New Caledonian rainforest. Austral Ecology 28: 204–209.

Brook, B. W., O'Grady, J. J., Chapman, A. P., Burgman, M. A., Akcakaya, H. R. and

Frankham, R. 2000. Predictive accuracy of population viability analysis in

conservation biology. Nature 404: 385-387.

Brook, B. W., Sodhi, N. S., Ng, P. K. L. 2003. Catastrophic extinctions follow

deforestation in Singapore. Nature 424: 420-423.

Brown, K. S. 1997. Diversity, disturbance and sustainable use of Neotropical forests:

insects as indicators for conservation monitoring. Journal of insect conservation 1: 25-

42.

Brown, W. L. 2000. Diversity of ants. In: Agosti, D., Majer, J. D., Alonso, L. E. and

Schultz, T. R. eds. Ants: standard methods for measuring and monitoring biodiversity

83 pp 45-79. Smithsonian Institution Press, Washington.

Bruhl, C. A., Gunsalam, G. & Linsenmair K. E. 1998. Stratification of ants in a primary

rain forest in Sabah, Borneo. Journal of tropical ecology 14: 285-297.

Cherret, J. M. 1989. Leaf-cutting ants. Biogeographical and ecological studies. In: Leith,

H. and Werger, M. J., eds. Ecosystem of the world, tropical rain forest ecosystem, pp

473-488. Elsevier, New York.

Chong, C. S. 2003. Ant diversity along a rural-urban gradient. BSc. (Hons.) thesis.

National University of Singapore.

Connell, J. H. 1978. Diversity in tropical rain forests and coral reefs. Science 199: 1302-

1310.

Cook, S. E. 1976. Quest for an index of community structure sensitive to water pollution.

Environmental pollution 11: 269-288.

Corlett, R. T. 1988. Bukit Timah: the history and significance of a small rain-forest

reserve. Environmental Conservation 15: 37-44.

Corlett, R. T. 1992. The ecological transformation of Singapore, 1819-1990. Journal of

biogeography 19: 411-420.

Cornell, H. V. and Lawton, J. H. 1992. Species interactions, local and regional processes,

and limits to the richness of ecological communities - a theoretical perspective.

Journal of animal ecology 61: 1-12.

DeFries, R., Hansen, A., Newton, A. C. and Hansen, M. C. 2005. Increasing isolation of

protected areas in tropical forests over the past twenty years. Ecological applications

15: 19-26.

Didham, R. K. and Lawton, J. H. 1999. Edge structure determines the magnitude of

changes in microclimate and vegetation structure in tropical forest fragments.

84 Biotropica 31: 17-30.

Donald, D. B. and Anderson, R. S. 2003. Resistance of the prey-to-predator ratio to

environmental gradients and to biomanipulations. Ecology 84: 2387-2394.

Done, T. J. 1992. Phase-shifts in coral reef communities and their ecological significance.

Hydrobiologia 247: 121-132.

Ellwood, M. D. F. and Foster, W. A. 2004. Doubling the estimate of invertebrate biomass

in a rainforest canopy. Nature 429, 549-551.

Farrell, T. M. 1991. Models and mechanisms of succession - an example from a rocky

intertidal community. Ecological monographs 61: 95-113.

Feener, D. H. Jr. & Schupp, E. W. 1998. Effect of treefall gaps on the patchiness and

species richness of Neotropical ant assemblages. Oecologia 116: 191-201.

Folgarait, P. J. 1998. Ant biodiversity and its relationship to ecosystem functioning: a

review. Biodiversity and conservation 7: 1221-1244.

French, D. D. and Picozzi, N. 2002. Functional groups' of bird species, biodiversity and

landscapes in Scotland. Journal of biogeography 29: 231-259.

Gadagkar, R. 1994. Why the definition of eusociality is not helpful to understand its

evolution and what should we do about it. Oikos 70: 485-488.

Gibb, H. and Hochuli, D. F. 2004. Removal experiment reveals limited effects of a

behaviorally dominant species on ant assemblages. Ecology 85: 648-657.

Goudie, A. 2002. Great warm deserts of the world: landscapes and evolution. Oxford

University Press, New York.

Greenberg, L., Reierson, D., Rust, M. K. 2003. Fipronil trials in California against the red

imported fire ant, Solenopsis invicta Buren, using sugar water consumption and

mound counts as measures of ant abundance. Journal of agricultural and urban

85 entomology 20: 221-233.

Grime, J. P. 1977. Evidence for the existence of three primary strategies in plants and its

relevance to ecological and evolutionary theory. American naturalist 111: 1169-1194.

Grime, J. P. 1979. Plant strategies and vegetation processes. John Wiley, New York.

Haddad, N. M., Tilman, D., Haarstad, J., Ritchie, M. and Knops, J. M. H. 2001.

Contrasting effects of plant richness and composition on insect communities: a field

experiment. American naturalist 158: 17-35.

Hamburg, H., Andersen, A. N., Meyer, W. J. and Robertson, H. G. 2004. Ant community

development on rehabilitated ash dams in the South African Highveld. Restoration

ecology 12: 552-558.

Harper, J. L. 1981. The concept of population in modular organisms. In: May, R. H., ed.

Theoretical ecology (2nd edition) pp 53-77. Blackwell Scientific Publications, Oxford.

Harper, J. L. 1985. Modules, branches and the capture of resources. In: Jackson, J. B. C.,

Buss, L. W. and Cook, R. E., eds. Population biology and the evolution of clonal

organisms pp 1-33. Yale University Press, New Haven.

Heino, J. 2005. Functional biodiversity of macroinvertebrate assemblages along major

ecological gradients of boreal headwater streams. Freshwater biology 50: 1578-1587.

Holldobler, B. 1983a. Ethological aspects of chemical communication in ants. Advances

in the study of behavior 8: 75-115.

Holldobler, B. 1983b. Territorial behavior in the green tree ant, Oecophylla smaragdina.

Biotropica 15: 241-250.

Holldobler, B. and Wilson, E. O. 1978. The multiple recruitment systems of the African

weaver ant Oecophylla longinoda (Latreille) (Hymenoptera: Formicidae). Behavioral

ecology and sociobiology 3: 19-60.

86 Holldobler, B. and Wilson, E. O. 1990. The ants. Belknap Press, Cambridge,

Massachusetts.

Huang, H. T. and Yang, P. 1987. The ancient cultured citrus ants. Bioscience 37: 665-671.

Jackson, J. C. 1965. Chinese agricultural pioneering in Singapore and Johore, 1800-1917.

Journal of the Malayan Branch of the Royal Asiatic Society 38: 77-105.

Jones, C. G., Lawton, J. H. and Shachak, M. 1994. Organisms as ecosystem engineers.

Oikos 69: 373-386.

Judd, T. M. 1995. The waggle dance of the honey-bee - which bees following a dancer

successfully acquire the information. Journal of insect behavior 8: 343-354.

Kaspari, M. and Weiser, M. D. 2000. Ant activity along moisture gradients in a

neotropical forest. Biotropica 32: 703-711.

King, J. R., Andersen, A. N. & Cutter, A. D. 1998. Ants as bioindicators of habitat

disturbance: validation of the functional group model for Australia’s humid tropics.

Biodiversity and conservation 7: 1627-1638.

Kirkegaard, M., Sonne, C., Leifsson, P. S., Dietz, R., Born, E. W., Muir, D. C. G. and

Letcher, R. J. 2005. Histology of selected immunological organs in polar bear (Ursus

maritimus) from East Greenland in relation to concentrations of organohalogen

contaminants. Science of the total environment 341: 119–132.

Koninck, R. 1975. Farmers of a city state: the Chinese smallholders of Singapore.

Canadian Sociology and Anthropology Association, Montreal.

Kovacs, M. 1992. Biological indicators of environmental pollution. In: Kovacs, M. ed.

Biological indicators in environmental protection pp 7-11. Ellis Horwood Limited,

West Sussex, England.

Lal, R. 1996. Deforestation and land-use effects on soil degradation and rehabilitation in

87 western Nigeria. Land degradation & development 7: 19-45.

Lavelle, P. and Spain, A. V. 2001. Soil ecology. Kluwer Academic Publishers, Boston.

Law, J. H. & Regnier, F. E. 1971. Pheromones. Annual review of biochemistry 40: 533-

548.

Le Galliard, J. F., Ferriere, R. and Dieckmann, U. 2005. Adaptive evolution of social

traits: origin, trajectories and correlations of altruism and mobility. The American

naturalist 165: 206-224.

Leitao, A. B. and Ahern, J. 2002. Applying landscape ecological concepts and metrics in

sustainable landscape planning. Landscape and urban planning 59: 65-93.

Lemenih, M., Karltun, E. and Olsson, M. 2005. Assessing soil chemical and physical

property responses to deforestation and subsequent cultivation in smallholders farming

system in Ethiopia. Agriculture, ecosystems and environment 105: 373-386.

Lemmon, P. E. 1957. A new instrument for measuring forest overstory density. Journal of

Forestry 55: 667-668.

Lindsey, P. A. and Skinner, J. D. 2001. Ant comparison and activity patterns as

determined by pitfall trapping and other methods in three habitats in the semi-arid

Karoo. Journal of arid environments 48: 551-568.

Longman, K. A. and Jenik, J. 1987. Tropical forest and its environment (2nd edition).

Longman Scientific and Technical, New York.

Maeto, K. and Sato, S. 2004. Impacts of forestry on ant species richness and composition

in warm-temperate forests of Japan. Forest ecology and management 187: 213-223.

Majer, J. D. 1983. Ants: bioindicators of minesite rehabilitation, land-use and land

conservation. Environmental management 7: 375-383.

Majer, J. D. and Camer-Pesci, P. 1991. Ant species in tropical Australia tree crops and

88 native ecosystems – is there a mosaic? Biotropica 23: 173-181.

McCook, L. J. 1994. Understanding ecological community succession – causal models

and theories, a review. Vegetatio 110: 115-147.

McCune, B. and Grace, J. 2002. Analysis of ecological communities. Mjm Software

Design, Oregon.

McCune, B. and Mefford, M. J. 1999. Multivariate analysis of ecological data. MjM

Software, Oregon.

McGeoch, M. A. 2002. Insect conservation in South Africa: an overview. African

entomology 10: 1-10.

Mielke, P. W. and Berry, K. J. 2001. Permutation methods: a distance function approach. Springer Series in Statistics. Springer, New York.

Montgomery, R.A. and Chazdon, R. L. 2001. Forest structure, canopy architecture, and

light transmittance in tropical wet forests. Ecology 82: 2707-2718.

Murase K., Itioka T., Nomura M. and Yamane S. 2003. Intraspecific variation in the status

of ant symbiosis on a myrmecophyte, Macaranga bancana, between primary and

secondary forests in Borneo. Population ecology 45: 221-226.

Nash, M. S., Bradford, D. F., Franson, S. E., Neale, A. C., Whitford, W. G. and Heggem,

D. T. 2004. Livestock grazing effects on ant communities in the eastern Mojave

Desert, USA. Ecological indicators 4: 199–213.

Nash, M. S., Whitford, W. G., Bradford, D. F., Franson, S. E., Neale, A. C. and Heggem,

D. T. 2001. Ant communities and livestock grazing in the Great Basin, U.S.A. Journal

of arid environments 49: 695-710.

Noble, I. R. and Slatyer, R. O. 1980. The use of vital attributes to predict successional

changes in plant communities subject to recurrent disturbances. Vegetatio 43: 5-21.

89 Nordlund, D. A. 1981. Semiochemicals: a review of the terminology. In: Nordlund, D.A.,

Jones, R. L. and Lewis, W. J., eds. Semiochemicals pp 13-27. John Wiley, New York.

Ohnishi H., Imai, H. T. and Yamamoto, M. T. 2003. Molecular phylogenetic analysis of

ant subfamily relationship inferred from rDNA sequences. Genes & genetic systems

78 (6): 419-425.

Otto, S. P. and Whitlock, M. C. 1997. The probability of fixation in populations of

changing size. Genetics 146: 723-733.

Paton, T. R., Humphreys, G. S. and Mitchell, P. B. 1995. Soils: a new global review. Yale

University Press, New Haven.

Perfecto, I. and Snelling, R. 1995. Biodiversity and the transformation of a tropical

agroecosystem: ants in coffee plantations. Ecological applications 5: 1084-1097.

Pfeiffer, M., Chimedregzen, L. and Ulykpan, K. 2003. Community organization and

species richness of ants (Hymenoptera/Fromicidae) in Mongolia along an ecological

gradient from steppe to Gobi desert. Journal of biogeography 30: 1921-1935.

Pokorny, M. L., Sheley, R. L., Zabinski, C. A., Engel, R. E., Svejcar, T. J. and Borkowski,

J. J. 2005. Plant functional group diversity as a mechanism for invasion resistance.

Restoration ecology 13: 448-459.

Pol, R. and Casenave, J. L. 2004. Activity patterns of harvester ants Pogonomyrmex

pronotalis and Pogonomyrmex rastratus in the Central Monte Desert,

Argentina. Journal of insect behavior 17 (5): 647-661.

Polunin, N. 1981. Bukit Timah Nature Reserve, Singapore. Environmental conservation 8:

274.

Porter, S. D. & Jorgensen, C. D. 1981. Foragers of the harvester ants, Pogonomyrmex

owyheei: a disposable caste? Behavioral ecology and sociobiology 9: 247-256.

90 Raunkier, C. 1934. The life-forms of plants and statistical plant geography. Clarendon

Press, Oxford.

Read, J. L. and Andersen, A. N. 2000. The value of ants as early warning bioindicators:

responses to pulsed cattle grazing at an Australian arid zone locality. Journal of arid

environments 45: 231-251.

Ribas, C. R., Sobrinho, T. G., Schoereder, J. H., Sperber, C.F., Lopes-Andrade, C. and

Soares, S.M. 2005. How large is large enough for insects? Forest fragmentation effects

at three spatial scales. Acta oecologica 27: 31-41.

Richards, P. W. 1996. The tropical rain forest: an ecological study (2nd edition).

Cambridge University Press, Cambridge.

Robertson, H. G. 2002. Comparison of leaf litter ant communities in woodlands, lowland

forests and montane forests of north-eastern Tanzania. Biodiversity and conservation

11: 1637-1652.

Room, P. M. 1975. Diversity and organization of the ground foraging ant faunas of forest,

grassland and tree crops in Papua New Guinea. Australian journal of zoology 23: 71-

89.

Ross, G. N. 1966. Life-history studies on Mexican butterflies, IV: The ecology and

ethology of Anatole rossi, a myrmecophilous metalmark (Lepidoptera: Riodinidae).

Annals of the Entomological Society of America 59: 985-1004.

Roth, D. S., Perfecto, I. & Rathcke, B. 1994. The effects of management systems on

ground-foraging ant diversity in Costa Rica. Ecological Applications 4: 423-436.

Roth, L. C. 1999. Anthropogenic change in subtropical dry forest during a century of

settlement in Jaiqui Picado, Santiago Province, Dominican Republic. Journal of

biogeography 26: 739-759.

91 Ruppert, E. E. and Barnes, R. D. 1994. Invertebrate zoology (6th ed). Saunders College

Publishing, Fort Worth.

Samson, D. A., Rickart, E. A. & Gonzales P. C. 1997. Ant diversity and abundance along

an elevational gradient in The Philippines. Biotropica 29: 349-363.

Schenk, D., Bersier, L. F. and Bacher, S. 2005. An experimental test of the nature of

predation: neither prey- nor ratio-dependent. Journal of animal ecology 74: 86-91.

Sibly, R. M. and Hone, J. 2002. Population growth rate and its determinants: an overview.

Philosophical transactions of the Royal Society of London Series B -biological

sciences 357: 1153-1170.

Siebert, S. F. 2005. The abundance and distribution of rattan over an elevation gradient in

Sulawesi, Indonesia. Forest ecology and management 210: 143-158.

Sih, A. and Wooster, D. E. 1994. Prey behavior, prey dispersal, and predator impacts on

stream prey. Ecology 75: 1199-1207.

Solley, G. O. and Vanderwoude, C. 2004. Fire ant sting anaphylaxis in Australia. Journal

of allergy and clinical immunology 113(Supplement 1): 75.

Stevens, R. D., Cox, S. B., Strauss, R. E. and Wilig, M. R. 2003. Patterns of functional

diversity across an extensive environmental gradient: vertebrate consumers, hidden

treatments and latitudinal trends. Ecology letters 6: 1099-1108.

Suarez, A. V. and Case, T. J. 2002. Bottom-up effects on persistence of a specialist

predator: ant invasions and horned lizards. Ecological applications 12: 291-298.

Tanner, J. E., Hughes, T. P. and Connell, J. H. 1996. The role of history in community

dynamics: A modeling approach. Ecology 77: 108-117.

Tsoularis, A. and Wallace, J. 2002. Analysis of logistic growth models. Mathematical

biosciences 179: 21-55.

92 Turnbull, C. M. 1989. A history of Singapore, 1819-1988 (2nd edition). Oxford University

Press, Singapore.

Turner, I. M. 1996. Species loss in tropical rain forest: a review of the evidence. Journal

of applied ecology 33: 200-209.

Underwood, A. J. 1997. Experiments in ecology: their logical design and interpretation

using analysis of variance. Cambridge University Press, New York.

Vasconcelos, H. L. 1999. Effects of forest disturbance on the structure of ground-foraging

ant communities in central Amazonia. Biodiversity and conservation 8: 409-420.

Viner, D., Hulme, M. and Raper, S. C. B. 1995. Climate-change scenarios for the

assessments of the climate-change on regional ecosystems. Journal of thermal biology

20: 175-190.

Way, M. J. and Khoo, K. C. 1992. Role of ants in pest-management. Annual review of

entomology 37: 479-503.

Weber, N. A. 1957. Fungus-growing ants and their fungi: Cyphomyrmex costatus.

Ecology 38: 480-494.

Wetzel, R. G. 1995. Death, detritus, and energy-flow in aquatic ecosystems. Freshwater

biology 33: 83-89.

Whitmore, T. C. 1998. An introduction to tropical rain forests, 2nd ed. Oxford University

Press, Oxford.

Wilson, E. O. 1971. The insect societies. Harvard University Press, Cambridge,

Massachusetts.

Wilson, E. O. 1975. Sociobiology: the new synthesis. Harvard University Press,

Cambridge, Massachusetts.

Wong, P. P. 1968. Some aspects of the surface configuration of Singapore island. M.A.

93 thesis, National University of Singapore.

Wong, Y. K., Chew, P. T. and Ali, I. 1994. The tree communities of the Central

Catchment Nature Reserve, Singapore. Gardens’ Bulletin Singapore 46: 37-78.

Yamane, S., Itino, T. & Nona, A. R. 1996. Ground ant fauna in a Bornean dipterocarp

forest. The Raffles bulletin of zoology 44: 253-262.

Zar, J. H. 1999. Biostatistical analysis (4th edition). Prentice Hall, New Jersey.

94 APPENDIX A

List of ant genera with functional group classification (from Brown, 2000). CCS = Cold Climate Specialist, CS = Cryptic Species, DD = Dominant Dolichoderinae, GM = Generalized Myrmicinae, HCS = Hot Climate Specialist, OP = Opportunist, SC = Subdominant Camponotini, SP = Specialized Predator, TCS = Tropical Climate Specialist.

Genus Functional group Acanthognathus SP Acanthomyops CS Acanthomyrmex TCS Acanthoponera TCS Acanthostichus CS Acromyrmex TCS Acropyga CS Adelomyrmex TCS Adlerzia CS Aenictogiton TCS Aenictus TCS Afroxyridris CS Allomerus CS Amblyopone CS Anillomyrma CS Anisopheidole CS Ankylomyrma TCS Anochetus SP Anomalomyrma CS Anonychomyrma DD Anoplolepis CS Aphaenogaster OP Aphomomyrmex TCS Apomyrma CS Apterostigma TCS Asphinctanillodes CS Asphinctopone CS Atopomyrmex TCS Atta TCS Azteca DD Baracidris CS Basiceros CS Belonopelta CS Blepheridatta TCS

95 Bondriotia CS Bothriomyrmex CCS Bracymyrmex TCS Calomyrmex CS Calyptomyrmex CS Camponotus SC Cardiocondyla OP Carebara CS Carebarella CS Cataglyphis HCS Cataulacus TCS Centromyrmex CS Cephalotes TCS Cerapachys CS Chalepoxenus CCS Cheliomyrmex TCS Chimaeridris TCS Cladomyrma TCS Colobostruma SP Concotio CS Creightonidris CS Crematogaster GM Cryptopone CS Cylindromyrmex SP Cyphoidris TCS Cyphomyrmex TCS Dacetinops CS Daceton SP Dendromyrmex SC Diacamma OP Dicroaspis CS Dilobocondyla TCS Dinoponera SP Discothyrea CS Doleromyrma OP Dolichoderus TCS Doronomyrmex CCS Dorylus TCS Dorymyrmex OP Dysedrognathus CS Echinopla SC Eciton TCS Ectatomma OP Emerypone CS Epelysidris TCS Epimyrma CCS Epitrius CS Epopostruma SP

96 Eucryptocerus TCS Euprenolepis TCS Eurhopalothrix CS Forelius DD Forelophilus SC Formica CCS Formicoxenus CCS Froggetella DD Gesomyrmex TCS Gigantiops TCS Glamyromyrmex CS Gnamptogenys TCS Goniomma HCS Gymnomyrmex CS Harpagoxenus CCS Harpegnathos SP Heteroponera CCS Huberia CCS Hylomyrma TCS Hypoponera CS Indomyrma CS Ireneopone TCS Iridomyrmex DD Ishakidris CS Kartidris TCS Kyidris CS Labidus TCS Lachnomyrmex TCS Lasiophanes CCS Lasius CCS Leptanilla CS Leptanilloides CS Leptogenys SP Leptomyrmex TCS Leptothorax TCS Linepithema DD Liometopum DD Liomyrmex TCS Lophomyrmex TCS Lordomyrma TCS Lordomyrmex TCS Loweriella TCS Machomyrma CS Manica CCS Mayriella CS Megalomyrmex TCS Melophorus HCS Meranoplus HCS

97 Mesostruma SP Messor HCS Metapone TCS Metapone TCS Microdaceton CS Monomorium GM Mycetarotes TCS Mycetophylax TCS Mycetosoritis TCS Mycocepurus TCS Myopias CS Myopopone CS Myrcidris TCS Myrmecia SP Myrmecina TCS Myrmecocystus HCS Myrmecorhynchus CCS Myrmelachista CS Myrmica OP Myrmicaria TCS Myrmicaria TCS Myrmicocrypta TCS Myrmoteras SP Mystrium CS Neivamyrmex TCS Neostruma CS Nomamyrmex TCS Noonilla CS Nothidris CCS Nothomyrmecia SP Notoncus CCS Notostigma SC Ochetellus OP Ochetomyrmex TCS Octostruma CS Ocymyrmex HCS Odontomachus OP Odontoponera SP Oecophylla TCS Oligomyrmex CS Onychomyrmex TCS Opisthopsis SC Orectognathus SP Overbeckia SC Oxyepoecus TCS Oxyopomyrmex HCS Pachycondyla SP Paedalgus CS

98 Papyrius DD Paratopula TCS Paratrechina OP Pentastruma CS Perissiomyrmex TCS Peronomyrmex TCS Petalomyrmex TCS Phasmomyrmex SC Phaulomyrma CS Pheidole GM Pheidologeton CS Philidris DD Phrynoponera SP Plagiolepis CS Platythyrea SP Plectroctena SP Podomyrma TCS Poecilimyrma TCS Pogonomyrmex HCS Polyergus SP Polyrhachis SC Ponera CS Prenolepis CCS Prionopelta CS Pristomyrmex TCS Proatta TCS Probolomyrmex CS Proceratium CS Procryptocerus TCS Prolasius CCS Protalaridris CS Protanilla CS Protomognathus CCS Psalidomyrmex CS Pseudaphomomyrmex TCS Pseudoatta TCS Pseudolasius TCS Pseudomyrmex TCS Pseudonotoncus CCS Quadristruma CS Recurvidris CS Rhopalothrix CS Rhytidoponera OP Rogeria TCS Romblonella TCS Rotastruma TCS Santschiella TCS Scyphodon CS

99 Sericomyrmex TCS Serrastruma CS Simopelta CS Simopone SP Smithstruma CS Solenopsis CS Sphinctomyrmex CS Stegomyrmex CS Stenamma CCS Stereomyrmex TCS Stigmacros CCS Streblognathus SP Strumigenys CS Talaridris CS Tapinoma OP Tatudris CS Technomyrmex OP Terataner TCS Teratomyrmex TCS Tetramorium OP Tetraponera TCS Tetraponera TCS Thaumatomyrmex SP Tingimyrmex CS Trachymyrmex TCS Tranopelta CS Trichoscapa CS Tricytarus TCS Turneria TCS Typhlomyrmex CS Vollenhovia TCS Vombisidris TCS Wasmannia TCS Xenomyrmex TCS Yavnella CS Zacryotocerus TCS

100 APPENDIX B

List of the number of ant individuals collected in the four Forest Types in Singapore. CCS = Cold Climate Specialist, CS = Cryptic Species, DD = Dominant Dolichoderinae, GM = Generalized Myrmicinae, HCS = Hot Climate Specialist, OP = Opportunist, SC = Subdominant Camponotini, SP = Specialized Predator, TCS = Tropical Climate Specialist.

Species Forest Type Functional Group 1 2 3 4 Acanthomyrmex sp. 1 0 8 1 1 TCS Acropyga sp. 1 0 1 3 58 CS Aenictus sp. 2 4 3 1 1 TCS Anochetus sp. 1 0 2 1 12 SP Anoplolepis sp. 1 1 4 8 0 CS Aphaenogaster sp. 1 2 6 3 1 OP Camponotus gigas 2 11 13 4 SC Camponotus sp. 1 0 12 1 3 SC Camponotus sp. 2 1 3 2 5 SC Camponotus sp. 5 4 1 14 0 SC Cardiocondyla sp. 1 1 5 1 2 OP Cerapachys sp. 1 0 9 6 11 CS Crematogaster sp. 1 0 5 5 2 GM Crematogaster sp. 2 2 2 6 9 GM Diacamma sp. 1 2 4 3 6 OP Dolichoderus sp. 1 0 0 1 1 TCS Dolichoderus sp. 2 3 14 1 1 TCS Dolichoderus sp. 3 1 12 1 1 TCS Euprenolepis sp. 1 3 12 1 1 TCS Gnamptogenys sp. 1 2 0 5 0 TCS Hypoponera sp. 1 0 0 1 10 CS Hypoponera sp. 2 1 3 10 18 CS Iridomyrmex sp. 1 6 3 6 3 DD Leptogenys sp. 2 0 5 29 8 SP Leptogenys sp. 3 1 3 12 17 SP Leptogenys sp. 4 0 2 6 1 SP Lophomyrmex sp. 1 0 11 3 1 TCS Meranoplus sp .1 0 1 0 0 HCS Metapone sp. 1 1 4 1 3 TCS Monomorium sp. 1 1 8 0 3 GM Myrmicaria sp. 1 0 9 1 0 TCS Ochetellus sp. 1 2 9 0 2 OP Odontomachus sp. 1 29 7 4 3 OP

101 Odontomachus sp. 2 0 1 1 0 OP Odontoponera sp. 1 1 0 35 12 SP Odontoponera sp. 2 1 0 10 20 SP Opisthopsis sp. 1 0 12 2 1 SC Pachycondyla sp. 1 0 7 1 22 SP Paratopula sp. 1 3 3 1 0 TCS Paratrechina sp. 1 1 3 1 1 OP Pheidole sp. 1 1 1 11 2 GM Pheidole sp. 2 1 3 35 3 GM Pheidole sp. 3 5 4 1 3 GM Pheidole sp. 4 4 3 2 34 GM Pheidole sp. 5 0 4 2 15 GM Pheidole sp. 6 3 0 0 13 GM Pheidole sp. 7 0 4 1 6 GM Pheidole sp. 9 0 20 4 6 GM Pheidole sp. 10 0 9 1 42 GM Pheidole sp. 11 1 3 0 10 GM Pheidole sp. 12 0 4 2 27 GM Pheidole sp. 13 0 10 1 7 GM Pheidole sp. 14 0 3 23 1 GM Pheidole sp. 15 0 13 10 9 GM Pheidole sp. 16 0 12 51 1 GM Pheidole sp. 17 1 10 3 13 GM Pheidologeton sp. 1 0 8 39 4 CS Pheidologeton sp. 2 0 1 19 6 CS Philidris sp. 1 2 1 0 1 DD Poecilimyrma sp. 1 0 11 1 1 TCS Polyrhachis sp. 1 0 2 2 0 SC Prenolepis sp. 1 0 0 0 3 CCS Proatta sp. 1 4 7 1 1 TCS Pseudolasius sp. 1 0 9 16 1 TCS Strumigenys sp. 2 1 7 8 0 CS Technomyrmex sp. 1 0 3 15 6 OP Tetramorium sp. 1 2 8 2 1 OP Tetramorium sp. 2 2 4 6 0 OP Tetramorium sp. 3 0 14 1 3 OP Tetramorium sp. 4 1 19 1 0 OP Tetraponera sp. 1 2 3 1 0 TCS Vollenhovia sp. 1 0 2 1 1 TCS Wasmannia sp. 1 0 4 1 0 TCS Total 105 441 462 464

102