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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
julkaisumyynti@uef.fi
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: geoffrey.malinga@uef.fi
Supervisors:
Professor Heikki Roininen, Ph.D.
University of Eastern Finland
Department of Biology
P.O.Box 111
80101 JOENSUU
FINLAND
email: heikki.roininen@uef.fi
Dr. Anu Valtonen
University of Eastern Finland
Department of Biology
P.O.Box 111
80101 JOENSUU
FINLAND
email: anu.valtonen@uef.fi
Professor Philip Nyeko, Ph.D.
Makerere University
Department of Forestry, Biodiversity and Tourism
P.O.Box 7062
KAMPALA
UGANDA
email: nyeko@caes.mak.ac.ug
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: derek@imul.com
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: gw.fernandes@gmail.com
Opponent:
Professor Toomas Tammaru, PhD
University of Tartu
Department of Zoology
Vanemuise 46, EE-51014
TARTU
ESTONIA
email: toomas.tammaru@ut.ee
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).
16
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
18
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)
19
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
23
(’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.
24
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
25
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
26
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
27
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).
28
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
29
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.
31
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
33
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).
34
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
35
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.
36
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).
37
 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.
38
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50
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