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Responses to bottom-up manipulations, forest harvesting and fragmentation

Tropical ecosystems throughout the world are undergoing rapid changes due to human-induced activities. However, detailed understanding of how Arthropods which constitute the bulk of tropical biodiversity respond to these habitat changes are incompletely known. This thesis provides novel information about the responses of the poorly known tropical galling insects to experimental bottomup manipulations, forest harvesting and habitat fragmentation.

Publications of the University of Eastern Finland Dissertations in Forestry and Natural Sciences isbn: 978-952-61-1607-5 (printed) issnl: 1798-5668 issn: 1798-5668 isbn: 978-952-61-1608-2 (pdf) issnl: 1798-5668 issn: 1798-5676

dissertations | No 162 | Geoffrey Maxwell Malinga | Tropical galling insects in a changing environment

Geoffrey Maxwell Malinga Tropical galling insects in a changing environment:

Geoffrey Maxwell Malinga

Tropical galling insects in a changing environment: Responses to bottom-up manipulations, forest harvesting and fragmentation

Publications of the University of Eastern Finland Dissertations in Forestry and Natural Sciences No 162

GEOFFREY MAXWELL MALINGA

Tropical galling insects in a changing environment: Responses to bottom-up manipulations, forest harvesting and fragmentation

Publications of the University of Eastern Finland Dissertations in Forestry and Natural Sciences No 162

Academic Dissertation To be presented by permission of the Faculty of Science and Forestry for public examination in the Auditorium N106 in Natura Building at the University of Eastern Finland, Joensuu, on November , 14, 2014, at 12 o’clock noon. Department of Biology

Grano Oy Joensuu, 2014 Editors: Profs. Pertti Pasanen, Pekka Kilpeläinen, and Matti Vornanen Distribution: Eastern Finland University Library / Sales of publications [email protected] www.uef.fi/kirjasto ISBN: 978-952-61-1607-5 (printed) ISSNL: 1798-5668 ISSN: 1798-5668 ISBN: 978-952-61-1608-2 (PDF) ISSNL: 1798-5668 ISSN: 1798-5676

Author’s address:

University of Eastern Finland Department of Biology P.O.Box 1111 80101 JOENSUU FINLAND email: [email protected]

Supervisors:

Professor Heikki Roininen, Ph.D. University of Eastern Finland Department of Biology P.O.Box 111 80101 JOENSUU FINLAND email: [email protected] Dr. Anu Valtonen University of Eastern Finland Department of Biology P.O.Box 111 80101 JOENSUU FINLAND email: [email protected] Professor Philip Nyeko, Ph.D. Makerere University Department of Forestry, Biodiversity and Tourism P.O.Box 7062 KAMPALA UGANDA email: [email protected]

Reviewers:

Professor Derek Pomeroy, Ph.D Makerere University Institute of Environment and Natural Resources National Biodiversity Data Bank P.O.Box 7298 KAMPALA UGANDA email: [email protected]

Professor Geraldo Wilson Fernandes, Ph.D CP 486 ICB/Universidade Federal de Minas Gerais Ecologia Evolutiva & Biodiversidade 30161 901 Belo Horizonrte MG Brazil BELO HORIZONTE BRAZIL email: [email protected]

Opponent:

Professor Toomas Tammaru, PhD University of Tartu Department of Zoology Vanemuise 46, EE-51014 TARTU ESTONIA email: [email protected]

ABSTRACT

Tropical ecosystems throughout the world are undergoing rapid changes due to human-induced activities such as deforestation, fragmentation of natural habitats and changes in nutrient cycling. Understanding how different species respond to these habitat changes is essential for developing management strategies. However, how most arthropods, especially, endophytophages respond to these habitat changes is still incompletely known. In this study, galling insects associated with Neoboutonia macrocalyx (Euphorbiaceae) in Kibale National Park, Uganda were used as a model system to study the responses of tropical galling insects to bottom-up field experimental manipulations and anthropogenic habitat modifications. The first aim was to study how variations in host plant vigour (manipulated through fertilization), resource concentration (manipulated by host tree density) and their interactions, affect the population of a cecidomyiid leaf galler (Cecidomyiini sp. 1EJV) and its mortality by parasitoids and inquilines. Increasing fertilization and host density caused a trophic cascade on gallers and their parasitoid populations but the rate of parasitism did not change. Total leaf area correlated positively with galler density, but within galled replicates, galled leaves were larger than ungalled leaves. The results indicate that resource concentration is more important than plant vigour at the resource unit level, but when gallers are in the selected resource units, they select the most vigorous leaves as predicted by the plant vigour hypothesis. The second aim was to examine how variations in host plant vigour (fertilization), resource concentration (tree density) and their interactions influence the community structure of galling insects and within-species variation in gall-morphotype assemblages. Increasing fertilization and host tree density significantly changed the structures of galler communities and gall-morphotype assemblages. These results demonstrate the important role of bottom-up factors in structuring galler

communities and gall-morphotype assemblages. The observed changes could be linked to differential responses of galler species and gall morphs to plant quality and quantity changes. Furthermore, the change in the structure of gall-morphotype assemblages indicate the possible roles of bottom-up factors in driving adaptive radiations in galling insects. The third aim was to investigate whether and to what extent galling insects can cope with habitat changes due to selective and clear-cut logging. The results of the present study indicated for the first time that tropical galling insects might be highly resilient to selective and clear-cut logging at least when primary or secondary forests with established Neoboutonia populations are sufficiently near. The fourth aim was to study the influence of habitat fragmentation and fragment characteristics on communities of galling insects. Forest fragmentation caused negative effects on species richness, density and also changed the community structure of gallers. Continuous forest areas showed similar community characteristics but some fragments were similar to continuous forests and others differed from them. The species richness and overall density of gallers did not differ among all the continuous forests and four of the fragments but was significantly lower in two fragments, both surrounded by tea plantations, than in any continuous forests. The present results highlight the need to include fragments in management and conservation priorities to complement the conservation of galling insects in continuous forests. The studied fragment characteristics did not explain differences in communities of galling insects in fragments, suggesting that caution is required about generalisations on the use of easily measureable fragment characteristics (e.g., size and distance of isolation) when designing and planning conservation areas in all species groups. In conclusion, the results of this study indicate that bottomup effects are fundamental determinants of tropical galling insect populations, community structures and within-species variation in gall-morph assemblages. In addition, it demonstrates that tropical galling insects on pioneer host plants

are resilient to the effects of selective and clear-cut logging when source populations, i.e., primary or secondary forests with established host plant populations are nearby. However, galling insects are negatively affected by habitat fragmentation when the surrounding matrix is not primary or secondary forest. The results of this study suggest that the management and conservation priorities for galling insects require maintenance of large continuous forested areas, but the inclusion of forest fragments and regenerating forests is necessary as a complementary strategy.

Universal Decimal Classification: 574.3, 591.553, 595.754, 595. CAB

Thesaurus:

insects;

Cecidomyiidae;

Psyllidae;

tropical

forests;

population structure; population dynamics; habitats; habitat fragmentation; modification; host plants; vigour; density; deforestation; clear felling; afforestation; regeneration; plant succession; national parks; Uganda; Africa Yleinen suomalainen asiasanasto: hyönteiset; sademetsät; trooppinen vyöhyke; populaatiot; populaatiodynamiikka; habitaatti; isäntäkasvit; elinvoimaisuus; tiheys; metsänkäsittely; hakkuut; metsitys; metsänuudistus; toipuminen; palautuminen; kansallispuistot; Uganda; Afrikka

Preface I would like to express my heartfelt thanks to my supervisors, Dr. Anu Valtonen and professors Heikki Roininen and Philip Nyeko, first, for inspiring me to study the fascinating tropical insect gallers, and secondly for their continued guidance throughout the process of developing this thesis. I sincerely thank you for the time you spent reading, editing and commenting on the various chapters of this thesis, which has greatly helped to improve its quality. I thank the preliminary examiners of this thesis, Professors Geraldo Wilson Fernandes and Derek Pomeroy for their constructive comments which improved the content of this work. I thank the administration of the department of Biology, Joensuu for providing a modest working environment. In addition, I wish to thank the office of the Ugandan President, the Uganda National Council of Science and Technology and the Uganda Wildlife Authority for permission to conduct this study in Kibale National Park. I am thankful to Eero. J. Vesterinen of the University of Turku for help with DNA barcoding of the specimen, Vilma Lehtovaara for map work, and John Koojo and Lord Balyega for their assistance in the field. I am also grateful to my colleagues, Margaret Nyafwono, Arthur Arnold Owiny, Pirita Latja, Sille Holm, Tiina Piiroinen and Kaisa Heimonen, with whom I shared this long journey for their wonderful cooperation and support. I wish to extend my warm thanks to my MSc supervisors, Dr. Eric Sande and Professor Derek Pomeroy for the solid foundation they laid that has enabled me to sail through this doctoral study. You were my source of inspiration and love for tropical forest biodiversity.

Words are short of me to express my deep sense of gratitude to Mirja Roininen for her hospitality during several visits to her home. You made us feel home and re-energized each time, Kiitos!. Also, I am grateful to Dr. Jaakko Haverinen for being such as a wonderful flatmate. Lastly, I thank my parents for their constant love and encouragements throughout my studies, especially during moments of low inspirations. I am grateful to my dear wife, Santa for her kind love, patience, and above all enduring to single-handedly take care of our beloved daughter during my long absence from home, without complaint. And our little one, Mercy Dinah, you made me ever smile and relaxed even when things were so serious, because of your many sweet songs and amazing passion for butterflies and flowers. Funding for this thesis was provided by the Finnish Academy of Sciences (SA 138899 to Heikki Roininen). Joensuu, November, 2014

Geoffrey Maxwell Malinga

LIST OF ORIGINAL PUBLICATIONS This thesis is based on the following articles, referred to in the text by their Roman numerals. I

Malinga G M, Valtonen A, Nyeko P, Vesterinen E J, and Roininen H. Bottom-up impact on the cecidomyiid leaf galler and its parasitism in a tropical rainforest. Oecologia 176: 511–520, 2014.

II

Malinga G M, Valtonen A, Nyeko P, and Roininen H. Bottom-up manipulations alter the community structures of galling insects and gall morphs on Neoboutonia macrocalyx trees in a moist tropical rainforest. Agricultural and Forest Entomology 16: 314–320, 2014.

III

Malinga G M, Valtonen A, Nyeko P, and Roininen H. High resilience of galling insect communities to selective and clear-cut logging in a tropical rainforest. International Journal of Tropical Insect Science, 2014. In press.

IV

Malinga G M, Valtonen A, Nyeko P, Vesterinen E J, and Roininen H. Communities of galling insects on Neoboutonia macrocalyx trees in continuous forests and remnants of forest fragments in Kibale, Uganda. African Entomology, 2014. In press.

Publications I-IV are reprinted with the kind permission from respective publishers. Copyright for Publication I by SpringerVerlag, II by John Wiley and sons, III by Cambridge University press and for IV by the Entomological Society of Southern Africa.

AUTHOR’S CONTRIBUTION I participated in the planning and designing of all studies (I-IV) together with my supervisors, and played a leading role in collecting the data for all papers (I-IV). I was also responsible for analyzing the data in all papers (I-IV) with the assistance of my supervisors. In addition, I wrote the first drafts of all the four papers with subsequent inputs from co-authors (I-IV). DNA barcoding of specimen was done by Eero. J. Vesterinen at University of Turku.

Contents 1 Introduction ................................................................................... 13 1.1 Tropical forests and the changing environment ............................ 13 1.2 Bottom-up regulation of population and community structures of insect herbivores .................................................................................. 14 1.3 Tropical insect herbivore response to anthropogenic habitat modification ......................................................................................... 15 1.4. Aims of the present study ............................................................. 17 2 Materials and Methods ................................................................ 19 2.1 Study area ...................................................................................... 19 2.2 The study system ........................................................................... 20 2.3 The influence of host plant vigour and density on a cecidomyiid leaf galler and its parasitoids (I) .......................................................... 21 2.4 The influence of host plant vigour and density on the structures of galler communities and gall-morphotype assemblages (II) ................. 23 2.5 Resilience of galling insects to selective and clear-cut logging (III) ............................................................................................................. 23 2.6 Response of galling insects to habitat fragmentation (IV)............. 25 2.7. Statistical analyses ....................................................................... 25 3 Results and Discussion ................................................................ 29 3.1 Bottom-up trophic cascade on a cecidomyiid galler species and its parasitoids ............................................................................................ 29 3.2 Galler communities are structured by bottom-up factors.............. 31 3.3 Bottom-up factors trigger variation in gall morphology in a cecidomyiid leaf galler.......................................................................... 32 3.4 Galling insects on pioneer hosts are resilient to clear-cutting and selective logging................................................................................... 32 3.5 Strong seasonal variation in galling insect communities.............. 34 3.6 Galling insect communities are affected by habitat fragmentation35 4 Conclusions.................................................................................... 37 5 References ...................................................................................... 39

1 Introduction 1.1 TROPICAL FORESTS AND THE CHANGING ENVIRONMENT

In recent decades, tropical forest ecosystems which contain the majority of global species have witnessed high rates of environmental change, as a result of human activities (MEA, 2005; Lewis, 2006; Gardner et al., 2009; Morris 2010). These activities include the clearance of native vegetation, especially deforestation, the degradation of natural habitats, fragmentation, changes in nutrient cycling, and climate change (MEA, 2005). Today, most of the once pristine and continuous natural forests have either been cleared or replaced by a humandominated ‘mosaic’ of landscapes (Lewis, 2006; Tscharntke et al., 2012). Deforestation has also reduced local rainfall patterns and extended the length of the dry season and droughts (MEA, 2005), and increasing warming trends are predicted for most of the tropics (IPCC, 2014). Furthermore, certain forest harvesting methods (e.g., clear-cutting, burning) can lead to nutrient cascades into the surrounding environment (Chen et al., 2010). These changes show no indication of slowing, given the accelerating trends of human population growth and dependency on wood fuel as a source of energy in tropical countries, raising concerns for the persistence of biodiversity (MEA, 2005; Krupnick, 2013). Despite these apparent escalations, detailed understanding of how Arthropods, which constitute the bulk of tropical biodiversity (Ghazoul & Sheil, 2010), respond to these habitat changes are highly incomplete. This study explores how tropical galling insects respond to variations in host plant quantity and vigour following experimental soil fertilization (bottom-up factors), and to habitat modification after clear-cutting or selective logging and fragmentation. A clearer understanding of such responses is

13

needed for the prediction and mitigation of future consequences of environmental change on Arthropod biodiversity and to develop informed conservation plans.

1.2 BOTTOM-UP REGULATION OF POPULATION AND COMMUNITY STRUCTURES OF INSECT HERBIVORES

The quest for which factors regulate the population and community structures of insect herbivores is a major theme in ecology (Price et al., 2011). Such knowledge is required to understand how ecosystems function. It has been suggested that insect herbivore population and community structures are regulated by both bottom-up (resource availability) and topdown (natural enemies) forces (Hunter & Price, 1992; Bailey & Whitham, 2003; Nakamura & Ohgushi, 2003). Nevertheless, the importance of either force continues to be a subject of debate (Walker et al., 2008). Recently, several authors have provided increasing evidence for the importance of bottom-up over topdown factors (Roininen et al., 1996; Price & Hunter, 2005; Cornelissen & Stiling, 2006; Kos et al., 2011). However, it remains unclear which bottom-up factor; plant quality or quantity is more important (Stiling & Moon, 2005). Consequently, two hypotheses have been invoked to explain the importance of bottom-up factors: the plant vigour hypothesis (Price, 1991) argues that insect herbivores select and perform best on vigorously growing plants or plant modules and the resource concentration hypothesis (Root, 1973) argues that specialist insect herbivores are more likely to find suitable habitat, breed more successfully and increase in abundance where resources are concentrated. In multitrophic level communities, bottom-up effects manifest when organisms at each trophic level are limited by resource availability from the level below (White, 1978; Roininen et al., 1996). If bottom-up effects are strong, nutrient addition or the increased quantity of host plants (resources) will have positive effects on the producer level, for example by changing 14

the architectural complexity, biomass and productivity (Gruner et al., 2008; Chen et al., 2010). These effects can spread up the food chain, resulting in higher populations of herbivores and natural enemies at higher trophic levels, a scenario termed a “bottom-up cascade” (Hunter & Price, 1992). For example, Nakamura et al. (2005) found that enhanced foliage sprouting after a flood resulted in an increase in the abundance of leaf beetles and their natural enemies. Additionally, plant-mediated indirect bottom-up cascading effects can propagate to the community level, and alter herbivore or natural enemy community structures (Kagata & Ohgushi, 2006; Utsumi et al., 2009). Empirical tests that have investigated the importance of bottom-up vs. top-down forces in regulating the population and community structures of poorly studied tropical insect gallers are noticeably scarce (but see Cuevas-Reyes et al., 2011). In boreal and temperate systems, bottom-up effects might be more important for gallers than top-down effects (Roininen et al., 1996; Price & Hunter, 2005; Cornelissen & Stiling, 2006), although there is some indication that top-down effects, e.g., predation are important in tropical systems (Hawkins, 1997).

1.3 TROPICAL INSECT HERBIVORE RESPONSE TO ANTHROPOGENIC HABITAT MODIFICATION

Understanding how tropical insect herbivores respond to anthropogenic habitat modifications such as the clearance of native vegetation and fragmentation has received much attention in recent years (e.g., Tylianakis et al., 2007; Savilaakso et al., 2009; Nyafwono et al., 2014). A key question for insect conservation at present, however, is whether communities in such human-modified sites can withstand habitat changes or whether they can recover to an approximation of a primary forest status. Generally as forest landscapes are logged or become increasingly fragmented, the distance to source populations increases so that dispersal and movement of a

15

species between remnant forests become increasingly difficult (Farig, 2003). To persist under such changed environmental conditions, species will have to align their resilience abilities with the changing environmental conditions. Two theories have been used to predict the dynamics of species occurrence and persistence in fragmented landscapes: the island biogeography and metapopulation theories (ArroyoRodríguez & Mandujano, 2009). According to the theory of island biogeography (MacArthur & Wilson, 1967), the species richness and abundance of organisms should decline in fragments that are smaller or more distant from the mainland due to increased extinction and decreased colonisation rates in small and isolated fragments. This theory has long been increasingly applied in planning and designing reserves. Lately, the emphasis has shifted to the metapopulation theory (Levins, 1969; Hanski, 1998; Hanski & Gilpin, 1991). The metapopulation concept argues that, species that inhabit fragmented landscapes form metapopulations consisting of local populations that are spatially separated but reciprocally linked by occasional migrations and gene flow. The probability of extinction will decrease as patch size increases, and the more distant the source population, the less likely it is that the patch will be colonised (Hanski, 1991; Hanski & Gilpin, 1991). Whereas a growing number of studies have examined the responses of different insect herbivore species to habitat modification, in contrast, our current understanding of the responses of tropical galling insects to habitat changes remain anecdotal (but see, Oyama et al., 2003; Julião et al., 2004; Araújo et al., 2011; Araújo & Espirito-Santo Filho, 2012). Due to their extreme specificity with their host plants (Cuevas-Reyes et al., 2007), galling insects might be highly sensitive to habitat changes (Oyama et al., 2003). Importantly, galling insects, constitute important links in terrestrial food-webs (Nyman et al., 2007), and thus their response to habitat alteration might be indicative of ecosystem stability and function (Paniagua et al., 2009; Fernandes et al., 2010).

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1.4. AIMS OF THE PRESENT STUDY

This thesis used galling insects associated with Neoboutonia macrocalyx Pax (Euphorbiaceae) as a model system to study how tropical galling insects respond to field experimental bottom-up manipulations and anthropogenic habitat modifications. The specific aims of this study were:  To assess the relative importance of host-plant vigour (manipulated by fertilization) and resource concentration (manipulated by host-tree density) in regulating the abundance of the cecidomyiid leaf galler (Cecidomyiini sp. 1EJV) and its mortality by parasitoids and inquilines, as well as to evaluate the relative importance of the plant vigour and resource concentration hypotheses in the trophic cascade on the cecidomyiid leaf galler and its parasitoid (I).  To examine how variations in the levels of fertilization (hostplant vigour), host-tree density (resource concentration) and their interactions influence the structure of galling insect communities and within-species variation in gall-morphotype assemblages (II).  To assess whether galling insects exhibit resilience to selective and clear-cut logging, and whether there is a directional recovery trend for communities of gallers along the successional gradient (III).  To evaluate how habitat fragmentation affects the communities of galling insects, and the importance of fragment properties in explaining their distributions (IV).

17

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2 Materials and Methods 2.1 STUDY AREA

This study was conducted in a medium-altitude moist evergreen tropical rainforest of Kibale National Park (KNP, 795 km2) located in central-western Uganda (0°13' to 0°41'N and 30°19' to 30°32'E) in the foothills of the Ruwenzori mountains (Strushaker, 1997; Dowhaniuk et al., 2014). The park is located within a matrix composed of tea plantations, grazing and agricultural land. The mean annual precipitation at KNP is 1,696 mm (1990−2011; C.A. Chapman and L. Chapman, unpubl. data), and the mean daily minimum and maximum temperatures are 14.9°C and 20.2°C, respectively (Chapman et al., 2005). The rainy season occurs from March to May and September to December, and the dry season from June to August (Strushaker, 1997; Kasenene & Roininen, 1999). The soils are classified as lixic ferralsols, although there are local variations among sites (Majaliwa et al., 2010). For example, valley bottoms are characterised by moderately deep, well-drained and dark clay soils with a low pH whereas hill slopes have a deep, red sandy loam (Lang-Brown & Harrop, 1962). Studies I and II were conducted in an experimental field of a former clear-cut Eucalyptus plantation near the Makerere University biological field station. The sites for study III included, four differently aged regenerating clear-cuts of former coniferous plantations (RACs for brevity) and three selectively logged (K13, K14 and K15) and two primary forest compartments (K30 and K31) representing a gradient of forest recovery as different successional stages (Table 1, Fig. 1, III). The boundaries of RACs were confirmed with Landsat images and by local residents who were present at the time of logging. The sites for study IV consisted of five continuous forest compartments within the park (K13, K14, K15, K30 and K31)

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and six fragments of native forest neighbouring the park on the north-western side, namely, Kiko 1, Kiko 2, Kiko 4, John’s forest, Lake Nkuruba forest and Mukwano’s forest (Table 1, Fig. 1, IV). The fragments ranged in size from 0.9 to 22.6 ha and were located between 0.05 and 5.1 km away from the park boundary. The vegetation matrix around the fragments was composed of tea plantations and isolated shade tree species (Kiko 1, Kiko 2, Kiko 4 and Mukwano’s forest), grazing land and subsistence agricultural fields (John’s forests and Lake Nkuruba fragments). Within the matrix, there were no Neoboutonia trees present (pers. obs). These fragments appear to have been connected with the park, but became isolated in about 1959 (Chapman et al., 2003).

2.2 THE STUDY SYSTEM

Neoboutonia macrocalyx Pax (Euphorbiaceae) is a native pioneer deciduous tree species of medium-altitude tropical rainforests (Chapman et al., 1999) which grows in partially logged, primary and secondary forests (Kasenene & Roininen, 1999) and in gaps in swamps and valley bottoms (Chapman et al., 1999) from 600 to 2500 m a.s.l. (Lovett, 1991; Fischer & Killmann, 2008).Trees are 10–25 m in height (Lovett et al., 2006), have a short trunk with an open crown and a canopy width of 7–12 m (Hamilton, 1991) and produce leaves continuously throughout the year (Kasenene & Roininen, 1999). Neoboutonia trees are attacked by highly host-specific galling insect species, previously recorded by Skippari et al. (2009) and Heimonen et al. (2013). In this study five undescribed multivoltine galling insect species were recorded. Morphological identification of the study species were confirmed by DNA barcoding (Ratnasingham & Hebert, 2007) by sequencing part of the mitochondrial Cytochrome c oxidase subunit I (COI) gene (Hebert et al., 2003) from a subset of the sampled gallers (1–6 individuals per morphospecies) using standard protocols (details in I, IV). To delimit galler morphospecies as a single species, a neighbour20

joining tree for the samples was constructed using the “taxon ID tree” function of BOLD; based on the Kimura 2 parameter as a distance model. Due to the lack of taxonomic studies for Afrotropical galling insects, the species were named based on the morphological features of their galls, the host-plant parts attacked and the insect family (Fernandes & Price, 1988) as follows; (i) cecidomyiid leaf galler that forms smooth hard galls on the underside of leaf blades, leaf petioles and midribs of host plants, (ii) cecidomyiid shoot galler that forms smooth hard galls on shoots, (iii) cecidomyiid hairy stone galler that forms extremely hard hairy galls on the underside of leaf blades, (iv) cecidomyiid flower-stalk galler that forms smooth hard galls on flower stalks, and (v) psyllid leaf galler, that forms, soft hairy elliptical galls on the upper side of leaf blades. Of the five species, cecidomyiid leaf galler (Cecidomyiini sp. 1EJV) forms three distinctive gall morphs, namely petiole gall, hard leaf gall and midrib gall. The original collected materials and voucher specimens have been deposited at the insect collection of the University of Eastern Finland.

2.3 THE INFLUENCE OF HOST PLANT VIGOUR AND DENSITY ON A CECIDOMYIID LEAF GALLER AND ITS PARASITOIDS (I)

Study I was performed in a field experiment using a 4 × 4 factorial manipulation with four levels of plant vigour (manipulated by fertilization) and resource concentration (manipulated by group size of trees), respectively. It evaluated the impacts of increasing fertilization and host-tree density on the density of a cecidomyiid leaf galler species and its mortality by parasitoids and inquilines, as well as the importance of the plant vigour and resource concentration hypotheses on the trophic cascade of the cecidomyiid leaf galler and its parasitoids. Host-plant vigour was manipulated by adding granulated NPK (nitrogen/phosphorous/potassium) fertilizer to trenches dug at a uniform radius of 15−20 cm and a depth of 5−10 cm around the

21

tree base of two-year-old Neoboutonia trees which ranged in height from 77.4−491.3 cm. Based on previous studies, high plant nutritional content is usually associated with rapid growth and plant vigour (De Bruyn et al., 2002; Price et al., 2011). Phosphorous and nitrogen are the most limiting nutrients in tropical rainforests, and are the minerals most likely to regulate plant growth and determine soil fertility (Tanner et al., 1998). Nine replicates of each combination of four levels of host-tree density (one, two, three and four trees per 1-m2 plot) and four levels of fertilization (ambient level, 100 g, 200 g and 400 g of NPK fertilizer added) were randomly assigned in May 2011, resulting in 144 independent replicates for this experimental design. The trees in group sizes two, three and four were on average 30–50 cm distant from each other. The vegetation between the treatments contained a thick undergrowth of shrubs and some early and mid-successional trees. To minimise the effects of non-target plant diversity on the treatments, all plants beneath the canopy and those touching the canopy of experimental trees in the surroundings were periodically removed. Before the treatments were applied, and five months following the treatments (in November 2011), the number of leaves per shoot, mid-rib lengths and the number of galls per leaf were measured for each tree. In the final sampling (November 2011), all galls were removed for dissection and rearing in the laboratory to identify and count the gallers, parasitoids and inquilines as well as to establish the cause of mortality for gallers. Neoboutonia macrocalyx leaf area (Y) is dependent on mid-rib length (x) and was estimated by the regression model, Y = 5.03x + 0.83x2 (Savilaakso et al., 2009). Plant vigour was measured as the mean leaf size (Price, 1991; De Bruyn et al., 2002; Santos et al., 2011) or growth rate of leaf area during the study period (Price et al., 1991; Auslander et al., 2003). The total leaf area in each experimental unit represented the resource quantity or the resource concentration hypothesis (Low et al., 2009). We chose these factors because they allow us to evaluate the plant vigour and resource concentration hypotheses independently. The 22

density of gallers was estimated as the total number of individuals per leaf area. Because cecidomyiid galls are known to remain on a host plant long after the insect has emerged from the gall or died, all galls with live or dead insect gallers and those where the galler had emerged were sampled. The number of emerged adult gallers was estimated by counting emergence holes or empty viable gall chambers.

2.4 THE INFLUENCE OF HOST PLANT VIGOUR AND DENSITY ON THE STRUCTURES OF GALLER COMMUNITIES AND GALLMORPHOTYPE ASSEMBLAGES (II)

Study II used the same field experiment as study I. The aim was to investigate the roles of increased fertilization (plant vigour) and host-tree density (resource concentration) or their interactions in structuring the galling insect communities and gall-morphotype assemblages on N. macrocalyx trees. After applying treatments, gallers were allowed to establish naturally on experimental replicates. Five months following the treatments (November 2011), all trees in each replicate were sampled for gallers. For each tree, the number of different galler species per leaf was measured, together with the gall morphs from which they originated and the mid-rib length of all leaves. Neoboutonia macrocalyx leaf area (Y) was estimated by the regression model as in study I. In the laboratory, all galls were dissected under a stereomicroscope, to confirm the species morphological identifications.

2.5 RESILIENCE OF GALLING INSECTS TO SELECTIVE AND CLEAR-CUT LOGGING (III)

The resilience of galling insects to selective and clear-cut logging was evaluated by comparing the species richness per tree

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(’species density’, see Gotelli & Colwell, 2011), the density and community structure of galling insects from four differently aged regenerating clear-cuts (RAC9, RAC11, RAC14 and RAC19) of former coniferous plantations (9–19 years), and three selectively logged (K13, K14 and K15) compartments (42–43 years) with two adjacent primary forests (K30 and K31). A total of 10 Neoboutonia trees were randomly sampled from each successional stage. Six apical branches were randomly cut from each tree using a tree pruner. The branches were cut from the middle canopy, 6–15 m high. From branch samples, the total number of leaves, midrib lengths, and the number of different galler species per leaf were assessed. In the laboratory, all galls were dissected under a stereomicroscope to confirm the morphological identifications. All the N. macrocalyx trees in each compartment were also mapped, and using the latitude and longitude of each tree, the Euclidean distance between trees for each sampled tree was calculated, as an approximate indication of host density at a landscape scale. In addition, the stem diameter at breast height (DBH) and the height (m) of each sampled tree, using a 1-m marked pole were estimated. Estimates of mean tree height and host-tree density were used as indicators of resource availability (Neves et al., 2014). Sampling was performed twice during the wet season and three times during the dry season. The same trees were studied in all samplings and each sampling lasted 2–3 weeks with successional stages visited in random order. Species density was measured as the number of species per tree (six branches per tree), and the density of gallers as the total number of individuals per leaf area. Leaf area (Y) is dependent on the midrib length (x) and was calculated as in study I.

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2.6 RESPONSE OF GALLING INSECTS TO HABITAT FRAGMENTATION (IV)

Study IV examined the effects of habitat fragmentation on galling insect communities and the importance of fragment properties in explaining their distributions. A similar sampling plan as in study III was used, but included six native fragments. In addition, the fragment area and the shortest distance to the park boundary and to the nearest neighbouring fragments were measured for each fragment. The density of Neoboutonia trees in each fragment was measured as the number of individuals per area of the fragment. The species richness was estimated as species density per tree, i.e., the number of species per tree in a standard sample size of leaves and shoots, and galler density was the total number of individuals per leaf area. Leaf area was estimated as in study I.

2.7. STATISTICAL ANALYSES

Analysis of covariance (ANCOVA, with the initial mean tree height as a covariate) was used to test the effects of fertilization, host-tree density and their interactions on the growth rate and the total leaf area of experimental units (I). If ANCOVA indicated significant effects in fixed factors, multiple comparisons were performed using Tukey’s pairwise tests for each response variable; natural log (x+1) transformations were applied to the response variables to improve normality. Pretreatment differences in the number of galls (per tree) among experimental units assigned to different treatments were studied using Kruskal–Wallis ANOVA and Mann–Whitney U tests, and differences were not significant (Kruskal–Wallis tests, fertilization: H = 0.22, df = 3, P = 0.99; tree density: H = 7.4, df = 3, P = 0.060). A generalised linear model with a negative binomial error distribution and a log-link function was used to analyse the

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effects of treatments on the densities of gallers and parasitoids at the end of the experiment. When density differences were significant, multiple pairwise comparisons with sequential Bonferroni corrections were conducted. Spearman’s rank correlations were used to determine the relationships between the density of gallers and the mean growth rate of leaf area (plant vigour hypothesis), or the total leaf area of host plants in each experimental unit (resource concentration hypothesis). To test whether leaf size predicted the probability of leaves being galled in the experimental replicates that were colonised during the experiment, the mean leaf area of galled and ungalled leaves in each colonised replicate were calculated. Differences in mean leaf area between galled and ungalled leaves in colonised replicates were assessed using the paired sample t-test. Kruskal–Wallis ANOVA and Mann–Whitney U tests were used to evaluate the effects of fertilization and hosttree density on galler species rates of parasitism and inquilinism. Permutational multivariate analysis of variance (PERMANOVA) run by PERMANOVA routine of Primer-E, version 6 (Anderson et al., 2008) based on Bray–Curtis similarity was used to test the differences in the structures of galler communities or gall-morph assemblages among levels of fertilization, host-tree density and their interactions (II). The Bray–Curtis similarity was computed from fourth-roottransformed abundance data. The P values were obtained with 999 permutations of residuals under a reduced model and type III sums of squares. A non-metric multidimensional scaling (NMDS; Clarke & Warwick, 2001) was used to illustrate the differences and similarities in the structures of galler communities or gallmorph assemblages among levels of fertilization, host-tree density and their interactions. The NMDS ordination was conducted using a Bray–Curtis similarity matrix computed from fourth-root-transformed abundance data in the program PRIMER-E (Clarke & Gorley, 2006). For clarity, the NMDS

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ordination graph generated using distances among centroids of each treatment combination was shown. The similarity percentage routine (SIMPER, in PRIMER-E, Clarke & Warwick, 2001) was used to identify which galler species or gall morphs accounted for the observed differences in the structures of galler communities or gall-morph assemblages between pairs of each treatment (II). The distance-based linear model (DistLM, in PRIMER-E) was used to test whether the observed differences and similarities in the structures of galler communities or gall-morph assemblages were explained by changes in the quality or quantity of host plants resulting from the experimental manipulations. To perform DistLM, the Bray– Curtis similarity matrix was modelled with the mean leaf size or total leaf area as the predictor variable. A generalised linear model (GLM) with a negative binomial error distribution and a log-link function in IBM SPSS, version 19.0 was used to test for the effects of successional stage (III) or forest (IV), month and their interactions on the species richness per tree, i.e., species density (Gotelli & Colwell, 2011) and the overall density of gallers. To take into account the variation due to host-tree size among successional stages (III), the diameter at breast height (DBH) was included as a covariate in each model (Cuevas-Reyes et al., 2006), but the effect of the covariate was not significant in either model. When the GLM gave significant results, multiple pairwise comparisons with sequential Bonferroni adjustments were performed. Spearman’s rank correlations were used to test the directional patterns in the mean values of species richness per tree (i.e., species density) and the overall density of gallers along the successional gradient (III). The species that characterised forest types (IV) were identified using the Dufrêne and Legendre Indicator Species Analysis (Dufrêne & Legendre, 1997) in R (R Development core team, 2013). PERMANOVA run by PERMANOVA + package for Primer-E, based on Bray-Curtis similarity computed from square-roottransformed abundance data was used to assess the differences in the community structure of galling insects among

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successional stages (III) or forests (IV), months and their interactions. The P values were calculated from 999 permutations of residuals under a reduced model and type III sums of squares. The NMDS generated from square-roottransformed abundance data and a zero-adjusted Bray–Curtis similarity matrix between samples was used to illustrate the similarities in the community structure of galling insects among successional stages (III) or forests (IV) and months. For clarity, distances among centroids of successional stages (or forests) and months were shown. A DistLM model was used to test for a directional pattern in the community structure of galling insects along the successional gradient (III). To perform DistLM, a Bray–Curtis similarity matrix was modelled with the “order” of successional stages as the predictor variable. Spearman’s correlation tests were used to examine the relationships between mean leaf area, mean tree height, or distance to the nearest neighbouring tree, and the overall density of gallers of each successional stage (III). Pearson’s correlations were calculated to determine the associations between community variables of gallers and fragment characteristics (IV).

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3 Results and Discussion 3.1 BOTTOM-UP TROPHIC CASCADE ON A CECIDOMYIID GALLER SPECIES AND ITS PARASITOIDS

In a fully factorial experimental manipulation, it was shown in this study that fertilization and increasing host-tree density triggered a bottom-up trophic cascade from the Neoboutonia trees to the cecidomyiid leaf galler (Cecidomyiini sp. 1EJV) and to its parasitoids (I). An increasing fertilization and density of host trees significantly affected the total leaf area of host plants or growth rate of leaf area (fertilization). The densities of gallers and their parasitoids changed as a response to both fertilization and density of host trees. These results indicate that bottom-upinduced plant responses not only affect insect herbivores, but can transfer to their natural enemies through a bottom-up cascade effect (Ohgushi, 2005; Kagata & Ohgushi, 2006). Several studies have also indicated strong bottom-up effects on gallers (Roininen et al., 1996; Price & Hunter, 2005) and other herbivorous insects (Denno et al., 2002; Nakamura et al., 2005). The results of this study provided support for the resource concentration hypothesis (Root, 1973), which predicts that specialist herbivore insect populations increase with an increasing density of their host plants (I). Many previous studies that have investigated whether insect herbivores are more abundant in denser stands of their host plants have produced inconsistent results (Grez & González, 1995; Nichols et al., 1999; Caballero & Lorini, 2000; Rhainds & English-Loeb, 2003; Cuevas-Reyes et al., 2004; Tuller et al., 2013). This suggests that the relationship between host-plant density and herbivore abundance is not universal. Several mechanisms have been suggested to explain these inconsistent responses of herbivore insect attacks to variations in the density of their host plants, including differences in species-specific searching behaviours

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and dispersal abilities, as well as experimental limitations (Grez & González, 1995; Caballero & Lorini, 2000; Cuevas-Reyes et al., 2004; Tuller et al., 2013). In addition, the presence of non-host plants in the matrix vegetation, i.e., associational resistance (Sholes et al., 2008; Barbosa et al., 2009) might confound the effects of host-plant density on insect herbivore abundance (III). Additionally, the results of the present study agree with the predictions of the plant vigour hypothesis (Price, 1991), suggesting that higher growth rates of plant modules or module size favours the preference and larval performance of insect herbivores compared to slow-growing or smaller modules (I). However, because galler density positively correlated only with leaf area (a measure of resource concentration) and not with the growth rate of leaf area (a measure of plant vigour), indicate that during the colonisation of resource units, resource concentration is more important than plant vigour. Similarly in study III, galling insects were less responsive to the quality (or vigour) of host plants at a landscape scale. Nevertheless, at the host-plant level, gallers select vigorously growing modules (larger-sized leaves, I) as predicted by the plant vigour hypothesis (Price, 1991). Thus, colonisation comprises two steps: finding the resource unit (with larger resource units colonised first), followed by selection within the resource unit (with the most vigorous leaves selected first). The preference of galling insects for vigorously growing plants or plant modules has also been demonstrated in several previous studies (Craig et al., 1989; Kimberling et al., 1990; Price & Ohgushi, 1995; Vieira et al., 1996; Santos et al., 2008). Vigorously growing plant modules (e.g., larger leaf size) might provide more oviposition sites for gallers or effective refuges from predators than less vigorous and smaller modules (Price et al., 2011). The rates of mortality by parasitoids and overall parasitism were generally low and did not alter with increasing galler density and quality or quantity of host plants, with the exception of tree-density manipulations, which increased the rate of inquilinism but at a very low level (I). These results indicate that the rate of parasitism is not dependent on the 30

density of gallers, suggesting that top-down factors might have weaker impacts in regulating the abundance of tropical insect gallers than bottom-up factors (Araújo et al., 2006). These findings support the general prediction by Hawkins et al. (1997) that endophytic gallers suffer the least parasitoid-induced mortality compared to other feeding guilds (Hawkins et al., 1997).

3.2 GALLER COMMUNITIES ARE STRUCTURED BY BOTTOM-UP FACTORS

Both fertilization and increasing host-density manipulations significantly affected the community structure of gallers (II). A fertilization × tree density interaction effect on the community structure of gallers was also found, implying that increasing fertilization caused different changes in the community structure of gallers at higher than at lower tree densities (Fig. 1, II). The change in galler community structure was probably a response to the increased quality and quantity of host plants, because measures of plant vigour (mean leaf size) and resource concentration (total leaf area) explained significant proportions of the variation in the community structure of gallers (II). This indicates that bottom-up factors are fundamentally important in structuring communities of tropical galling insects (Araújo et al., 2006). Bottom-up factors (e.g., plant vigour) are important to explain the community structures of arthropods in other systems (Wimp et al., 2010). The mechanisms by which these changes in community structure are brought about are unclear. One highly probable explanation is that the different galler species differ in their resource ratio requirements and responses to plant quality changes. In study I, for example, the density of one of the three species that accounted for the differences in the community structure of gallers (cecidomyiid leaf galler) was positively affected by increasing fertilization and host-tree density.

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3.3 BOTTOM-UP FACTORS TRIGGER VARIATION IN GALL MORPHOLOGY IN A CECIDOMYIID LEAF GALLER

Using a manipulative experiment, it was shown that fertilization and increasing host-tree density as well as their interactions, significantly changed the structure of a cecidomyiid leaf-gall morphotype assemblage (II), and this change corresponded to a gradient of host-plant quality or quantity. This indicates that bottom-up factors can promote radiation in gall morphologies formed by tropical insect gallers, and consequently the emergence of new species. The possible underlying ecological forces causing this observed divergence in gall morphologies are unclear. It has been indicated in other systems that the morphological divergence in gall structures formed by one species within a host might be a response to an enlarged surface area for feeding (Stone & Schönrogge, 2003), or to intraspecific competition for gall sites (Inbar et al., 2004). Thus, the availability of resources and free space (adaptive zones) appear to be the key factors that trigger gall morphological diversification (Price, 2005; Hardy & Cook, 2010; Litsios et al., 2012). The experimental increase in nutrient levels and host density probably increases the number of vacant ecological niches for colonisation and leads to a higher rate of gall morphological diversification (McLeish et al., 2007; Price et al., 2011). These within-species radiations in gall morphologies on a single host have been demonstrated in several previous studies (Inbar et al., 2004; Joy & Crespi, 2007; Stireman et al., 2008), but the underlying mechanisms require future research.

3.4 GALLING INSECTS ON PIONEER HOSTS ARE RESILIENT TO CLEAR-CUTTING AND SELECTIVE LOGGING

There were no significant differences in the species richness per tree, i.e., species density and overall density of gallers between any regenerating and primary forests, 9–19 or 42–43 years after 32

clear-cutting and selective logging, respectively (III). These and those from Oyama et al. (2003) indicate that specialist galling insect species on tropical pioneer host plants might be highly resilient to habitat modification. The reasons for the high resilience of galling insects to forest harvesting in Kibale National Park are unclear but, probably relate to two potential causes. Firstly, the existence of source populations (primary forests or secondary forests with an established host plant population) within a relatively short distance from the regenerating forests, appeared to have facilitated species dispersion (Bengtsson, 2002), allowing re-colonisation to occur immediately following the re-establishment of host trees. Secondly, N. macrocalyx is an early successional tree with a patchy spatial distribution. This ephemeral and unpredictable existence of the host tree might have caused the adaptation of the efficient colonisation of host-specific gallers on Neoboutonia trees. These findings are particularly relevant in management decisions regarding the prioritisation of different habitats for protection. In contrast, a previous study on the same host-plant system in Kibale forest (Savilaakso et al., 2009), found significantly different densities of lepidopteran species between selectively logged and primary forests. This indicates that different insect taxa exhibit different resilience to habitat disturbances, and that they therefore can have different colonisation abilities, preference or performance on their host plants in different habitats. Despite the high resilience of galler species density and overall density to habitat modification, there was no predictable directional recovery trend in the patterns of galler community structure along the successional gradient and no existence of “climax” galler community (III). These patterns might be explained by the stochastic processes of recolonisation and extinction of successional stages due to the patchiness of Neoboutonia trees (Wool, 2012), or to differences in the speciesspecific traits, for example, the recolonisation efficiency of individual species which is greatly affected by dispersal abilities and the matrix vegetation, or to differences in the degree of past

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disturbances among successional stages (Cole et al., 2014). Furthermore, the results confirm the findings of Dunn (2004) suggesting that whereas the species richness of tropical fauna recovers relatively rapidly, a substantially longer period is needed for the complete recovery of community composition.

3.5 STRONG SEASONAL VARIATION IN GALLING INSECT COMMUNITIES

The seasonality of tropical insect gallers is less well understood than for other tropical insects. This study showed that the species richness per tree (species density), overall density and community structure of galling insects were strongly affected by seasonal variations (III, IV). Peak abundance was observed in the wettest months as also indicated by several previous tropical studies (Kasenene & Roininen, 1999; Cuevas-Reyes et al., 2006; Araújo & Dos Santos, 2009; Nyeko, 2009; Skippari et al., 2009; Valtonen et al., 2013; Nyafwono et al., 2014). These and other studies (Cuevas-Reyes et al., 2006; Araújo & Dos Santos, 2009) suggest that seasonality is a fundamental determinant of galling insect communities in tropical forests. The reasons for the galler abundance peak observed in the wet season in this study are unclear. It might be related to synchronization with the period of active growth of the host plant during which young, less toxic and highly nutritious leaves are produced (Neves et al., 2014). However, this is less likely, given that N. macrocalyx trees produce leaves continuously and therefore resources are available throughout the year (Kasenene & Roininen, 1999). Another possible reason is that seasonal changes in rainfall and temperature influence the growth and development of the host tree and alter its nutritional quality and quantity in different periods (Araújo & Dos Santos, 2009).

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3.6 GALLING INSECT COMMUNITIES ARE AFFECTED BY HABITAT FRAGMENTATION

Although galling insects are highly resilient to clear-cut and selective logging (III), fragmentation of habitats significantly affected the number of species per tree (species density) and overall density of gallers (IV). In addition, galler community structure and composition was significantly altered. Similar relationships have been indicated for gallers in neotropical (Oyama et al., 2003) and boreal forests (Kaartinen & Roslin, 2011). Conversely, some studies have shown either no difference in the richness and abundance of gallers in fragmented and undisturbed habitats (Julião et al., 2004), or a greater richness and abundance in fragmented habitats (Araújo et al., 2011; Araújo & Espirito-Santo Filho, 2012). Given these discrepancies in the literature and our own studies, it is difficult to generalise with respect to how tropical gallers respond to habitat modification. The generally lower species richness and overall density of gallers in some fragments when compared to all the continuous forests (IV) are perhaps due to fragment-driven changes in local microclimatic conditions (Grimbacher et al., 2006; Savilaakso et al., 2009) or simply due to delays in the manifestation of fragmentation effects (Tilman, 1994; Ewers & Didham, 2006). On the other hand, the galler community structure and composition differed significantly among the eleven forests (IV). All the fragments except one (Lake Nkuruba) were clearly separated from continuous forests and from each other (Fig. 3, IV). The observed patterns in the structure and composition of gallers between continuous and fragmented forests is probably caused by differences in the sensitivity of individual galler species to habitat disturbance as depicted by results of indicator species analysis or is due to differences in the levels of disturbance. The lack of correlation between fragment characteristics (i.e. fragment area, host-tree density, distance of isolation from park boundary and from nearest neighbouring host tree) and galler

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community measures indicate that galler survival and extinction in fragmented forests is probably governed by fragment-specific factors, e.g., differences in matrix quality and within-fragment habitat quality (reviewed in Ewers & Didham, 2006) rather than predicted by fragment characteristics. These fragment-specific factors deserve greater attention in future studies. In addition, given the high specificity of gallers (Cuevas-Reyes et al., 2007), their limited dispersal abilities among patches (Cronin et al., 2001), and the low number of Neoboutonia trees (Table 1, IV), the individual Neoboutonia trees might act as ecological islands (Janzen, 1968; Julião et al., 2004) which limit the importance of fragment characteristics in explaining galler distribution at the fragment scale. Furthermore, the absence of Neoboutonia trees in the vegetation matrix might have restricted the movement of gallers among the forest fragments. In view of the present results, it is impossible to draw definitive conclusions on the specific area and habitat factors required for the persistence of galling insects in fragmented landscapes. Therefore, easily measured fragment characteristics, which could be potentially useful tools when designing and planning conservation areas (e.g., size, isolation distance), are not necessarily good indicators of species richness in all species groups.

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4 Conclusions In this study, the responses of galling insects to experimental bottom-up manipulations, forest harvesting and habitat fragmentation were studied. The results present new knowledge about the responses of poorly known tropical galling insects to altered environmental conditions. The main conclusions and future prospects are summarised as below:  Bottom-up induced changes in host-plant resource quality (plant vigour) and quantity (resource concentration) can trigger a bottom-up cascading effect and strongly impact on the abundance of gallers and their parasitoid population (I). These bottom-up induced changes can also alter the structures of galler communities and within-species gall-morphotype assemblages (II). Thus, bottom-up factors appear to be an important determinant of the population (I) and structures of tropical galling-insect communities, and within-species variation in gall-morphotype assemblages (II). The mechanisms behind these observed effects of increasing plant vigour and host density on galler community structure and gallmorphotype assemblages merit further study. Additionally, the effects of bottom-up induced plant responses on food-web structure deserves further attention in future studies, to understand better, how bottom-up induced responses impact ecosystem stability and function.  Resource concentration is more important than plant vigour (growth rate of a unit) at the resource-unit level, but when gallers are within the selected resource unit, they select the most vigorous leaves as predicted by the plant vigour hypothesis (I).  Mortality due to parasitoids is generally very low among galling insects in tropical habitats (I).  Seasonality is a fundamental determinant of communities of tropical insect gallers (III, IV).

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 Specialist galling insects on tropical pioneer host plants are resilient to logging, at least when source populations (primary forests or secondary forests with an established host-plant population) are sufficiently near. Overall, the results highlight the need to include recovering tropical forests into management and conservation priorities for galling insect biodiversity.  Habitat fragmentation can lead to a decline in the species richness per tree (i.e., species density) and to changes in the overall density and community structure of galling insects, emphasising the need to maintain large continuous forests as a long-term strategy for their conservation.  The similarity of community measures of gallers in some fragments and continuous forests indicate that the preservation of fragments might provide an important complement to the conservation of galling insect biodiversity. This highlights the need to include the remaining rainforest fragment habitats into management and conservation priorities. The present study did not identify specific habitat factors to predict which fragments have a high value for gallers, indicating that processes that produced high-value fragments might have been stochastic. This study therefore, urges caution in applying easily measurable fragment characteristics when planning and designing conservation areas in all species groups. In addition, a landscape-level management approach that encompasses both natural and modified habitats is recommended. Future studies need to investigate the influence of fragmentation on plantherbivore food-web structure.

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Responses to bottom-up manipulations, forest harvesting and fragmentation

Tropical ecosystems throughout the world are undergoing rapid changes due to human-induced activities. However, detailed understanding of how Arthropods which constitute the bulk of tropical biodiversity respond to these habitat changes are incompletely known. This thesis provides novel information about the responses of the poorly known tropical galling insects to experimental bottomup manipulations, forest harvesting and habitat fragmentation.

Publications of the University of Eastern Finland Dissertations in Forestry and Natural Sciences isbn: 978-952-61-1607-5 (printed) issnl: 1798-5668 issn: 1798-5668 isbn: 978-952-61-1608-2 (pdf) issnl: 1798-5668 issn: 1798-5676

dissertations | No 162 | Geoffrey Maxwell Malinga | Tropical galling insects in a changing environment

Geoffrey Maxwell Malinga Tropical galling insects in a changing environment:

Geoffrey Maxwell Malinga

Tropical galling insects in a changing environment: Responses to bottom-up manipulations, forest harvesting and fragmentation

Publications of the University of Eastern Finland Dissertations in Forestry and Natural Sciences No 162

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