UNIQUE ISLAND HABITATS – A COMPARISON
OF COMMUNITY ASSEMBLY IN MARINE AND
TERRESTRIAL CONTEXTS
Eleanor Margaret Velasquez Bachelor of Science (Botany and Ecology) The University of Queensland
Submitted in fulfilment of the requirements for the degree of Doctor of
Philosophy
School of Earth, Environmental and Biological Sciences
Science and Engineering Faculty
Queensland University of Technology
2019
Keywords
community assembly, critically endangered regional ecosystem, epibiont, urban forestry, general dynamic model of oceanic island biogeography, propagule pressure, pumice rafting, species–area relationship, theory of island biogeography.
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
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Abstract
Biodiversity loss has far-reaching implications for the survival of both human and other species on Earth. Countless studies have linked biodiversity to essential processes or ‘ecosystem services’ such as the provision of fresh water and purification of air. As human-modified ecosystems are now estimated to dominate the Earth, with the loss of biodiversity being far greater than natural background processes.
Understanding the abiotic (nonliving) and biotic (living) factors that influence the formation of communities over time and space has therefore never been more urgent. Thus, the main aim of the research presented in this thesis is to document and understand the abiotic and biotic factors driving the formation of insular biotic communities within two contexts. This PhD research also re- examines a fundamental theory in ecology, the theory of island biogeography
(TIB), and its central premise the species–area relationship (SAR), as predictors of ecosystem community formation.
The first insular community examined in this research was that of biota forming on floating pumice rafts in the Pacific Ocean. Each pumice stone was treated as a mini-island, as per the TIB and SAR. The patterns of richness forming on these stones were assessed against the key abiotic factors of age, area and climatic zone of collection, and the biotic factors of competition and facilitation. The second insular community examined was that of remnant forest fragments of the critically endangered regional ecosystem Melaleuca irbyana (R. T. Baker). Each remnant forest was treated as a human-made ii Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
island-like community as per the TIB and SAR, situated within the context of a highly modified human-made environment comprising either farmland or peri-urban environments. Here, the establishment success of M. irbyana seedlings was assessed against abiotic factors of remnant forest area and isolation, soil conditions and habitat disturbance (e.g. fire) and biotic factors of overstory and understory richness.
The examination of these two, rarely studied and different communities for my PhD research, was done purposefully to provide an opportunity to compare the differences between the two contexts. Firstly, the examination of the two systems allowed contrasts to be made between the influence of abiotic and biotic predictors of community assembly in marine versus terrestrial contexts. Secondly, I examined the differences in abiotic and biotic predictors of community assembly in connection to one of the most fundamental theories in ecology the TIB and associated lines of thinking such as the SAR. This examination was particularly relevant to contributing new knowledge to my field of study, as the communities were formed via substantially different processes. Pumice rafted island-like communities are formed by the colonisation of marine animals and plants, under unassisted conditions, in the open ocean. Whereas, island-like forest fragments of M. irbyana represent the human-made remaining fragments of a native community that has been extensively cleared for farming and housing developments.
In Chapter 3, I report that elements of the TIB, namely the SAR, are beneficial for predicting the richness forming on pumice stones as habitat area had one of the strongest correlations to species richness on pumice Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
iii
clasts. However, pumice invertebrate communities were also found to change depending on the age of pumice clasts and climatic zone of collection. In Chapter 4, I found more evidence in support of the TIB and SAR within pumice rafted communities. As pumice community functional trait diversity was not only found to increase as epibiont richness increased, but also in relation to age and habitat area and then also altered depending on the most influential climatic zone encountered.
In Chapter 5, I examined the connections between the TIB and SAR and establishment of M. irbyana seedlings into the understory of remnant forest areas. Here, my tests of the TIB and SAR (i.e. remnant area and isolation) did not directly aid in understanding the drivers of regeneration within this community. This was because seedling establishment of M. irbyana was linked to habitat disturbance and had little relationship to remnant forest area or isolation. However, the SAR did provide information on herbaceous native understory diversity, which increased with increasing remnant forest area. These research findings show that even the smallest remnant forests of M. irbyana provide increased chances of establishment success of this critically endangered community and, therefore, are worth preserving even when competing land uses such as development of housing estates, parks or roads threaten their conservation.
The research conducted in this thesis contributes to understanding the dynamics of community assembly in different contexts and further the use of the TIB and its central principles the SAR in aiding this. Although the TIB and
SAR provide useful predictive elements in some communities (e.g., pumice
iv Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
rafting), they were not helpful for explaining the drivers behind regeneration in remnants of M. irbyana forests. These results are important because many studies simply examine insular communities in terms of their relationship to the SAR. However, even in the pumice rafted community where the TIB and
SAR provided useful predictive elements, collection of additional abiotic and biotic data increased the power of models. For example, pumice community assembly was also influenced strongly by age, climatic zone of collection (as a measure of relative isolation) and the presence of foundation species such as barnacles of the genus Lepas. Overall, I find that age, isolation and area of ecosystems matter for species richness, functional trait diversity and specific needs of target species that may be critically endangered but that the
‘quality’ of an ecosystem is also important for predicting species establishment.
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
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Publications during candidature
Peer-reviewed papers
Eleanor Velasquez, Scott Bryan, Merrick Ekins, Alex G. Cook, Lucy Hurrey and Jennifer Firn. 2018. Age and area predict patterns of species richness in pumice rafts contingent on climatic zone encountered Ecology and Evolution
8: 5034-5046. https://doi.org/10.1002/ece3.3980.
Conference abstracts
Velasquez, E. M., Bryan, S. and Firn J. (2018) Plenary speed talk and poster:
Pumice rafting: A hitchhiker's guide to marine biodiversity. Ecological Society of Australia, September 2018. Brisbane, Australia. Presented by Eleanor
Velasquez.
Velasquez, E. M., Bryan, S. and Firn J. (2016) Speed talk: Pumice rafting: A hitchhiker's guide to marine biodiversity. Society for Conservation Biology 4th
Oceania Congress, July 2016. Brisbane, Australia. Presented by Eleanor
Velasquez.
Velasquez, E. M. and Firn, J. (2016) Poster presentation: Melaleuca irbyana: does remnant forest area drive seedling establishment in a critically
vi Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
endangered tree? The 2nd International Conference on Urban Tree Diversity,
February 2016. Melbourne, Australia. Presented by Eleanor Velasquez.
Velasquez, E. M., Bryan, S. and Firn, J. (2015) Contributed Talk: Havre pumice rafts: A unique test of the theory of island biogeography. The Student
Conference on Conservation Science, February 2015. The University of
Queensland, St Lucia, Brisbane. Presented by Eleanor Velasquez.
Velasquez, E. M., Bryan, S. and Firn, J. (2015) Contributed Talk: Havre pumice rafts: A unique test of the theory of island biogeography. The
International Biogeography Society – 7th biennial Conference, January 2015.
Bayreuth, Germany. Presented by Eleanor Velasquez.
Publications included in this thesis
I have chosen to incorporate one publication into my PhD thesis as follows:
Eleanor Velasquez, Scott Bryan, Merrick Ekins, Alex G. Cook, Lucy Hurrey and Jennifer Firn. 2018. Age and area predict patterns of species richness in pumice rafts contingent on climatic zone encountered Ecology and Evolution
8: 5034-5046. https://doi.org/10.1002/ece3.3980.
Contributor Statement of contribution Author Eleanor Velasquez (Candidate) Designed experiment (60%) Wrote and edited the paper (60%) Statistical analysis (70%)
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
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Contributor Statement of contribution Conducted field and lab work (50%) Author Jennifer Firn Designed experiment (30%) Wrote and edited paper (30%) Assisted with statistical analysis (30%) Author Scott Bryan Designed experiment (10%) Wrote and edited paper (5%) Conducted field and laboratory work (35%) Author Merrick Ekins Laboratory identification of biota (5%) Wrote and edited the paper (5%) Author Alex G. Cook Laboratory identification of biota (5%) Author Lucy Hurrey Laboratory identification of biota (5%)
viii Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
Table of Contents
Abstract ...... ii
Publications during candidature ...... vi
Table of Contents ...... ix
List of Figures ...... xv
List of Tables ...... xx
List of Abbreviations ...... xxiv
Statement of Original Authorship ...... xxv
Acknowledgements ...... xxvi
Poem ...... xxix
Chapter 1: Introduction ...... 1
1.1 The theory of island biogeography – can an old paradigm address modern ecological problems? ...... 1
1.2 Context ...... 4
1.2.1 Pumice rafting – testing the TIB by studying mass transportation of
marine hitchhikers ...... 5
1.2.2 Threats to shallow marine ecosystems ...... 9
1.2.3 Melaleuca irbyana – testing the TIB by studying urban forestry ...... 14
1.2.4 Threats to remnant forests of Melaleuca irbyana ...... 15
1.3 Purposes ...... 17
1.4 Thesis Outline ...... 21
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
ix
Chapter 2: Literature review ...... 25
2.1 Historical background ...... 25
2.2 The TIB and its application in modern ecological studies ...... 28
2.3 The TIB in marine contexts ...... 29
2.4 The TIB and urban forestry ...... 33
2.5 Summary and Implications ...... 36
Chapter 3: Journal article: Testing the Theory of Island
Biogeography and subsequent evolutions ...... 39
3.1 Abstract ...... 40
3.2 introduction ...... 40
3.3 Material and methods ...... 46
3.3.1 Home Reef raft and trajectory ...... 46
3.3.2 Havre Volcano raft and trajectory ...... 47
3.3.3 Pumice characteristics ...... 47
3.3.4 Sampling design ...... 48
3.3.5 Data analyses ...... 49
3.4 Results ...... 52
3.4.1 Do area and age predict epibiont richness (alpha diversity) and
does one have a stronger influence? ...... 53
3.4.2 How does the influence of area and age change for pumice clasts
that were collected from different climatic zones? ...... 56
x Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
3.4.3 Does pumice rafted community assembly (beta diversity) change
for pumice that originated from a different eruption and that took a
different trajectory? ...... 59
3.5 Discussion ...... 62
3.5.1 Do area and age predict epibiont richness and does one have a
stronger influence? ...... 62
3.5.2 How does the influence of area and age change for pumice clasts
that were collected from different climatic zones? ...... 63
3.5.3 Does pumice rafted community assembly change for pumice that
originated from a different eruption and that took a different
trajectory? ...... 65
3.6 Acknowledgements ...... 70
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems ...... 71
4.1 Abstract ...... 71
4.2 introduction ...... 72
4.3 Materials and methods ...... 79
4.3.1 Havre Volcano raft size & trajectory ...... 79
4.3.2 Characteristics of pumice rafts ...... 79
4.3.3 Sampling design ...... 80
4.3.4 Functional traits ...... 81
4.3.5 Data analyses ...... 82
4.4 Results ...... 86
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
xi
4.4.1 Does the trait space occupied by pumice rafted biota change over
time (age) and space (Crawley et al. 1986; Hart & Marshall 2012)? ..... 86
4.4.2 Does change in climatic zone (a measure of relative isolation
between pumice rafts) cause a resultant change in functional
richness of the pumice rafted community? ...... 94
4.4.3 Does a foundation species effect, such as that observed with
Lepas barnacles, also occur in pumice rafted communities (see Gil
& Pfaller 2016)? ...... 99
4.4.3.1 Sessile and motile biota as predicted by Lepas barnacles ...... 99
4.4.3.2 Sessile biota and Lepas barnacles ...... 100
4.4.3.3 Motile biota and Lepas barnacles ...... 102
4.4.3.4 Overall, feeding and reproductive trait richness as predicted by
Lepas barnacles ...... 102
4.5 Discussion ...... 104
4.5.1 Increased functional trait richness was found on pumice clasts that
were older and pumice clasts that had larger habitat space ...... 105
4.5.2 Change in climatic zone caused a resultant change in functional
richness of the pumice rafted community ...... 107
4.5.3 Lepas barnacles promote richness via a foundation species effect
in pumice rafted communities ...... 108
4.6 ACKNOWLEDGEMENTS ...... 112
Chapter 5: Small patches of endangered Melaleuca irbyana R. T.
Baker forests are critical refugia for plant species ...... 113
5.1 Abstract ...... 113
xii Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
5.2 Introduction ...... 114
5.3 Materials and methods ...... 124
5.3.1 Field surveys ...... 124
5.3.2 Estimation of area and isolation ...... 127
5.3.3 Soil samples ...... 128
5.3.4 Soil nutrient (LECO) analysis (total carbon and nitrogen) ...... 128
5.3.5 Soil pH analysis ...... 128
5.3.6 Data analysis ...... 129
5.4 Results ...... 130
5.4.1 Do remnant forest area, isolation and overstory forest variables,
such as live versus dead stems (as a measure of disturbance),
basal area (as a measure of productivity) and species richness,
correlate with the abundance of seedlings of M. irbyana and other
woody species? ...... 131
5.4.2 Do non-native or native understory plant species and remnant
forest size correlate positively with seedling establishment? ...... 136
5.4.3 How do soil characteristics such as soil nutrients and pH relate to
remnant forest area and seedling establishment of M. irbyana
compared with other species? ...... 142
5.5 Discussion ...... 143
5.5.1 Disturbance of overstory trees and increasing overstory richness
was strongly linked to establishment success of M. irbyana
seedlings...... 144
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
xiii
5.5.2 Non-native herbaceous species richness and cover correlated with
increases in M. irbyana seedling establishment in small disturbed
remnant forest areas, whereas native herbaceous species
richness and cover correlated with larger remnant forest areas...... 149
5.5.3 Seedling number of M. irbyana decreased with increasing nitrogen
levels whereas other seedling species increased in richness...... 151
5.6 Acknowledgements ...... 156
Chapter 6: Discussion ...... 159
6.1 Chapter 2 ...... 162
6.1.1 Summary of key outcomes ...... 162
6.1.2 Future work and improvements ...... 163
6.2 Chapter 3 ...... 163
6.2.1 Summary of key outcomes ...... 163
6.2.2 Future work and improvements ...... 164
6.3 Chapter 4 ...... 167
6.3.1 Summary of key outcomes ...... 167
6.3.2 Future work and improvements ...... 168
6.4 Chapter 5 ...... 170
6.4.1 Summary of key outcomes ...... 170
6.4.2 Future work and improvements ...... 170
6.5 Conclusions ...... 172
Appendices ...... 177
Bibliography ...... 214 xiv Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
List of Figures
Figure 3.1 Conceptual diagram of pumice ontogeny. This conceptual
diagram depicts the journey of a pumice clast from (a) The
Havre under-water volcano which erupted in July 2012, formed
approximately four trillion pieces of floating pumice stone (b).
This pumice then formed what is known as a pumice raft (c)
which was so large it could be seen from space. The raft slowly
dispersed over the open ocean driven by winds and currents,
and while this occurred marine biota (d) colonised the empty
surface of the clasts. Finally (e), pumice is either washed onto
the coastlines of islands and continents or sinks due to
waterlogging or biofouling...... 44
Figure 3.2 Mixed-effects model regression estimates for the combined
data of Home and Havre (n = 5,279) events within climatic
zones: a) temperate (n = 70), b) subtropical (n = 5,043), and c)
tropical (n = 166); showing epibiont richness as a function of the
covariates of: age (days since eruption), area (an estimation of
available habitat calculated for each individual pumice clast
using the surface area of a sphere), and a combined effect of
age x area. The error bars displayed in the above figure are the
standard error as derived from the coefficient estimates in the
2 model. The R m values indicate the amount of variation
explained by the model without the random effects, while the
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
xv
2 R c values indicate the amount of variation explained by the
model with the random effects ...... 55
Figure 3.3. nMDS of a) age (where e = early, m = middle, and l = late
arrivals of pumice clasts to beaches on the east coast of
Australia and Pacific Islands), b) climatic zone (where sth =
subtropical, t = tropical, and ct = temperate stranding locations),
and c) area effect on pumice rafted community composition
distinguished by location for two events Home (right-hand
cluster) and Havre (left-hand cluster). Note for panel b), the
effect of climate is more pronounced for Home with a clear
distinction between tropical and subtropical. For panel c), note
that larger pumice stones are represented by larger circles and
warmer colors, while smaller and cooler colored circles indicate
smaller pumice clasts, and the effect of area is more distinct for
the Home event (right-hand cluster) ...... 58
Figure 3.4. Percent dominance of different epibiont groupings a) by
event (Home, n = 4,547*) (Bryan et al., 2012) versus (Havre, n
= 403) and b) stage of pumice clast arrival for the combined
data of Home and Havre): early (n = 265), middle (n = 3,944)
and late (n = 741). *Note: A reduced number of clasts was
analyzed to produce these graphs for the Home event as
species had to be aligned and combined between the two
datasets. As there was a significant time lapse between
collections and also different authors, some data were excluded
xvi Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
due to the inability of ensuring the correct species were aligned
in both datasets ...... 61
Figure 4.1. Mixed-effects model regression estimates for a) total trait
richness; b) reproductive trait richness; and c) feeding trait
richness. Note there is little difference between the influence of
the factors age and area for feeding and reproductive trait
richness. For overall trait richness, age begins to predict the
trait richness to a slightly greater extent than area...... 87
Figure 4.2. nMDS of Havre functional trait richness. a) Area effect on
pumice rafted community composition abundance. Larger
pumice stones are represented by larger circles and warmer
colours, and smaller pumice clasts are represented by smaller
and cooler-coloured circles. It is clear from panel a) that larger
clasts have increased functional trait richness. b) Pumice clasts
are defined by age. e = early, m = middle and l = late arrivals of
pumice clasts to beaches on the east coast of Australia and
Pacific Islands. c) Pumice is indicated by climatic zone. sth =
subtropical, t = tropical and ct = temperate-stranding locations.
For panel b), the effect of age was more pronounced for early
arrivals, whereas for panel c), the effect of climate is not as well
defined...... 92
Figure 4.3. Mixed-effects model regression estimates for functional trait
groupings examined by climatic zone: a), b) and c) temperate (n
= 70), d), e) and f) subtropical (n = 218) and h), i) and j) tropical
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
xvii
(n = 116). Tropical and temperate climatic zones have negative
slopes in relation to trait richness and age. This indicated a
change in species composition and dominance as pumice
moved into water with new species pools and abiotic influences. .... 95
Figure 5.1. Mixed-effects model regression estimates for: a) Live M.
irbyana seedlings number/block as predicted by overstory
richness in all remnant forests; b) Dead M. irbyana seedlings
number/block as predicted by overstory richness in all remnant
forests; c) Live total no. seedlings number/block as predicted by
overstory richness in all remnant forests; d) Live M. irbyana
seedling number/block as predicted in M. irbyana dominated
remnant forests; e) Dead M. irbyana seedling number/block as
predicted in M. irbyana dominated remnant forests and f) Live
total no. seedlings number/block as predicted in M. irbyana
dominated remnant forests...... 134
Figure 5.2. Mixed-effects model regression estimates for: a) richness of
non-native understory / block as predicted in a mixed species
overstory; b) cover of non-native understory / block as predicted
in a mixed species overstory; c) richness of non-native
understory / block as predicted by M. irbyana dominated
overstory; d) non-native cover / block as predicted in M. irbyana
dominated overstory...... 138
Figure 5.3. Mixed-effects model regression estimates for: a) richness of
native understory/block as predicted in a mixed species
xviii Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
overstory; b) cover of native understory/block as predicted in a
mixed species overstory; c) richness of native understory/block
as predicted by M. irbyana dominated overstory; d) native
cover/block as predicted in M. irbyana dominated overstory...... 139
Figure 5.4. Mixed-effects model regression estimates for native and
non-native richness and cover as explanatory variables of: a)
Live M. irbyana seedling number / block; b) dead M. irbyana
seedling number / block. And total richness and cover of the
herbaceous layer as explanatory variables of: c) Live total
seedling number / block (excluding M. irbyana); d) Live M.
irbyana seedling number / block; e) Live total seedling number /
block (excluding M. irbyana)...... 141
Figure 5.5. Mixed-effect model regression estimates showing seedling
number as predicted by the abiotic explanatory variables of
remnant forest area (ha), pH (soil), total nitrogen (soil) and total
carbon (soil): a) live M. irbyana seedling number/block; b) dead
M. irbyana seedling number/block; c) live total seedling
number/block (excluding M. irbyana)...... 143
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List of Tables
Table 3.1 Results of model comparison using Akaike information
criterion (AICc) values to identify factors explaining variations in
epibiont richness between the pumice clasts within climatic
zones using the surface area of a sphere as an estimate for
available habitat ...... 54
Table 4.1. Pumice rafted functional traits and their modalities ...... 82
Table 4.2. Results of model comparison using Akaikie information
criterion (AICc) values to identify factors explaining variations in
functional trait richness. Analyses was conducted for total trait
richness, feeding trait richness and reproductive trait richness
per pumice clast combined and examined in relation to the fixed
effects of age and habitat area. Note all models represented in
this table were created using a normal distribution...... 88
Table 4.3. Results of model comparison using Akaikie information
criterion (AICc) values to identify factors explaining variations
between functional trait modalities. Analyses was conducted for
individual trait modalities and data combined for climatic zones
in relation to the fixed effects of age and habitat area...... 89
Table 4.4. PERMANOVA test of differences between pumice rafted
community trait modality composition abundance formed on
pumice collected from different locations, ages, sizes and
xx Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
climatic zones: subtropical (n = 218), tropical (n = 116) and
temperate (n = 70)...... 91
Table 4.5. PERMDISP analysis of community trait richness and
abundance as predicted by the grouped stage of arrival of
pumice clasts, into the categories of early, middle and late
arrivals. This analysis provides a distance-based test for
homogeneity of multivariate dispersions between pumice
stones of differing ages (NB: the number of permutations was
set to 9999 for all models)...... 93
Table 4.6. Pair-wise comparison tests of pumice rafted community trait
richness by grouped stage of arrival of early, middle and late
arrivals...... 93
Table 4.7. Results of model comparison using Akaikie information
criterion (AICc) values to identify factors explaining variations in
functional trait richness. Analyses was conducted for total trait
richness per pumice clast within separate climatic zones:
temperate (n = 70), subtropical (n = 218) and tropical (n = 116).
Note all models conducted for the following table were
conducted using a normal distribution...... 95
Table 4.8. PERMDISP analysis of pumice rafted community trait
richness and climatic zone providing a distance-based test for
homogeneity of multivariate dispersions between climatic zones
of tropical (n = 116), subtropical (n = 218) and temperate (n =
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
xxi
70) (NB: the number of permutations was set to 9999 for all
models)...... 99
Table 4.9. Pair-wise comparison tests of pumice rafted community trait
richness by climatic zones of tropical (n = 116), subtropical (n =
218) and temperate (n = 70)...... 99
Table 4.10. Results of model comparison using Akaikie information
criterion (AICc) values to identify factors explaining variations in
functional trait modality. Analyses was conducted for the
number and area of motile and sessile biota per pumice clast
with the predictors of age, area and Lepas barnacle counts or
cover. Note all data represented in the following table were
derived using a normal distribution and, where necessary, the y
variable was logged to enable model fitting...... 100
Table 4.11. Results of model comparison using Akaikie information
criterion (AICc) values to identify factors explaining variations in
functional trait richness. Analyses was conducted for the total
trait richness per pumice clast with the predictors of age, area
and Lepas barnacle counts or cover. Note that all models
represented in the following table were created using a normal
distribution...... 103
Table 5.1. Details of remnant forest locality and area and the associated
number of blocks sampled during the course of the field work
undertaken for this study...... 125
xxii Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
Table 5.2. Establishment number of M. irbyana seedlings by remnant
forests examined for this study...... 130
Table 5.3. Model outputs for ANOVA method derived from mixed-
effects models for overstory forest metrics as explanatory
variables of M. irbyana seedling establishment and seedling
establishment overall...... 133
Table 5.4. Model outputs for ANOVA derived from mixed-effects models
for overstory forest metrics as explanatory variables of non-
native versus native establishment into the understory...... 136
Table 5.5. Model outputs for ANOVA method derived from mixed-
effects models for understory non-native and native richness
and cover as explanatory variables of M. irbyana seedling
establishment...... 140
Table 5.6. Model outputs for ANOVA method derived from mixed-
effects models for the abiotic factors of remnant forest area and
soil nutrients (nitrogen, carbon and silicon) and pH as predictors
of M. irbyana versus total seedling establishment...... 142
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
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List of Abbreviations
AICc Akaike Information Criterion
ANOVA Analysis of Variance
DBH Diameter at breast height
GDM The general dynamic theory of oceanic biogeography
MEM Mixed Effects Model
nMDS non-metric Multidimensional Scaling
SAR The species–area relationship
TIB The theory of island biogeography
xxiv Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
Statement of Original Authorship
The work contained in this thesis has not been previously submitted to meet requirements for an award at this or any other higher education institution. To the best of my knowledge and belief, the thesis contains no material previously published or written by another person except where due reference is made.
Signature: QUT Verified Signature
Date: January 2019
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Acknowledgements
Many thanks to Associate Professor Jennifer Firn for being second to none in her unfailing optimism and confidence in me as a researcher, even when my own confidence was absent. Associate Professor Firn is one of the most hard-working, driven and passionate people I have ever met. Despite her commitments she always makes time for her students. Providing advice, help with statistics and code that won’t behave at a moment’s notice and even fed our lab group many lunches during my time in her lab. Associate
Professor Firn encouraged me to pursue many things during the course of my PhD that I would not have considered without her suggestion. I am very grateful she did as I believe these activities (e.g. science communication competitions) were an invaluable part of my PhD journey.
Thank you also to Associate Professor Scott Bryan, whose passion, knowledge and enthusiasm for pumice rafted biodiversity is second to none.
Without his knowledge of the South-western Pacific’s underwater volcanoes and previous pumice rafted biotic diversity publications, this PhD would not have been possible. Thank you also to Dr. John Hayes, whose careful guidance, sound bites of wisdom and vast knowledge of geographical information systems have shaped my ability to visualise data in maps. I also wish to thank fellow members of the Firn Lab Group for their consistent support, critical thinking and passion for what they do, which I believe helped to propel us all forward. Thank you also to Dr. Laurel MacKinnon (a
xxvi Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
consulting scientific editor) for assisting with a final light editing on my overall thesis.
Many thanks to Anna Marcoola from Logan City Council for her advice, feedback and help in organising the field sites for my study of Melaleuca irbyana. Anna is passionate about protecting our remaining wild places, and her efficiency in helping me with information was second to none.
Thank you to the huge team of undergraduate and postgraduate science volunteers, whose help were essential to completing the field work for my study of Melaleuca irbyana. These include Thita Soonthornvipat,
James Beattie, Jacob Rolley, Kerrod Bate, Nicola Green, Caitlin Riordin,
Samantha Burns, Bianca Knaggs, Susanna Imarisio and Elysia Andrews.
Through many hot, hot days in Logan and Ipswich City Council areas, we measured trees, identified species and took soil cores, your dedication in helping me in my research efforts was outstanding.
A huge thank you also to John Thompson, formerly of the Queensland
Herbarium and who is now completing his own PhD at Griffith University, for his invaluable assistance in identifying and confirming the identities of the species collected for this PhD research. Another sincere thank you goes to
Ms Karine Harumi Moromizato, who patiently trained me in the relevant soil preparation and sampling methods required for nutrient and pH analysis for the study.
Thank you also to my grandmother Gwenyth McLeod, who died during the course of my studies. You encouraged me from an early age to believe in myself and to follow my passions. As a woman who also held a science
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
xxvii
degree and yet came from a very different era, you achieved so much and were an amazing role model.
Thank you also to my dog Samba. Although he cannot read this dedication, it should be known that he sat diligently at my feet through countless hours of reading, writing and statistical analysis. He took me outside on a daily basis to make sure I received enough fresh air and sunlight, and he gave me many puppy cuddles when I needed them.
Thank you to my adoring husband and best friend David Velasquez, as without your support none of this would have been possible. You have always been the loudest voice in the cheering squad throughout the highs and lows of my research journey, and I appreciate to the bottom of my heart the sacrifice we undertook together so I could return to university to study.
I dedicate this thesis to my new baby boy Elias (‘Eli’) Velasquez and to all future babies who will inherit the legacy we have created in this world in its protection of the environment, the treatment of its animals and the protection of human rights. I can only hope that this body of work contributes in some way to making the world a better place.
xxviii Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
Poem
There rolls the deep where grew the tree.
O earth, what changes hast thou seen!
There where the long street roars, hath been
The stillness of the central sea.
The hills are shadows, and they flow
From form to form, and nothing stands;
They melt like mist, the solid lands,
Like clouds they shape themselves and go.
But in my spirit will I dwell,
And dream my dream, and hold it true;
For tho’ my lips may breathe adieu,
I cannot think the thing farewell.
An excerpt from ‘In Memoriam’ by Alfred, Lord Tennyson
Unique island habitats – a comparison of community assembly in marine and terrestrial contexts
xxix
Chapter 1: Introduction
1.1 THE THEORY OF ISLAND BIOGEOGRAPHY – CAN AN OLD
PARADIGM ADDRESS MODERN ECOLOGICAL PROBLEMS?
Understanding the abiotic and biotic factors that explain the number of species (or biodiversity) found in space and time is the prime goal of ecological research (MacArthur & Wilson 1963; MacArthur & Wilson 1967;
Magurran 2004; Whittaker et al. 2008). This drive to understand and predict the patterns observed in nature has led to the many hypotheses and theories that attempt to explain community assembly or how abiotic (e.g. habitat size and isolation, age or climatic influence) and biotic (e.g. competition, biological thresholds or food requirements) factors mechanistically explain species coexistence (MacArthur & Wilson 1963; MacArthur & Wilson 1967; Whittaker et al. 2008). The main aim of my PhD research was to test tenets of a long- standing theory in ecological science, the theory of island biogeography
(TIB), in two rarely studied ecological contexts: i) pumice rafted marine communities that originated in the South-western Pacific and ii) remnants of
Melaleuca irbyana forest located in South-eastern Queensland (MacArthur &
Wilson 1963; MacArthur & Wilson 1967; Crawley et al. 1986). I have examined these two insular ecosystem types to evaluate the relevance of the initial premise of the theory, the species–area relationship (SAR), in conjunction with additional factors which are thought to drive species assembly, for example, habitat age and isolation (Whittaker et al. 2008).
Chapter 1: Introduction 1
Native biodiversity is being lost at an unprecedented pace (see
Ceballos et al. 2015); yet concurrent with this loss is the increasing homogenisation of biotas across countries and even continents via the widespread transport and establishment of species (Cardinale et al. 2012;
Hooper et al. 2012). As a result, understanding the fundamental processes that regulate the amounts of biodiversity has arguably never been as important in history as it is now. The TIB was first proposed in 1963 and, since then, numerous studies have tested its utility as a framework for predicting the dynamic processes acting on species populations (MacArthur
& Wilson 1967). Constructs of this theory have become instrumental in the field of conservation for managing fragmented landscapes, including SARs
(Diamond 1975; Diamond et al. 1976; Margules et al. 1982; Whittaker et al.
2005; Matthews et al. 2014). The TIB predicts that patterns of biodiversity in insular environs are a result of species turnover (immigration and extinction), which eventually reaches a dynamic equilibrium of species because resources and space become saturated within a given area of habitat
(MacArthur & Wilson 1967; Simberloff & Wilson 1969; Keppel et al. 2010).
The TIB also contains as its core premise, arguably, one of the most well-established relationships in ecology, the SAR (Triantis et al. 2008;
Dengler 2009; Whittaker & Triantis 2012). The SAR predicts that as the size of an isolated habitat increases so does the number of species that are able to reside within it and that species richness does not increase only because of increased resources but also because the number of different sub-habitats
(or habitat heterogeneity) increases (MacArthur & Wilson 1963; MacArthur &
Wilson 1967; Power 1972; Simberloff 1974; Simberloff 1976; Gilbert 1980;
2 Chapter 1: Introduction
Triantis et al. 2008; Dengler 2009; Goldstein et al. 2014; Martins et al. 2014).
As for the TIB, the SAR is hypothesised to saturate through time, as competition for space between biota intensifies for this finite resource.
However, the SAR has remained somewhat equivocal in relation to its underlying processes and application (Lynch & Johnson 1974; Gilbert 1980;
Lomolino 2000; Triantis et al. 2008). This is because of two key difficulties with the SAR. The first is that habitat size is difficult to quantify in native ecosystems. The second is that studies have tended to focus on specific taxa as a surrogate for all biodiversity; for example, bat diversity in forest patches, islands and farmlands (Mendenhall et al. 2014), small mammals on mountain tops (Brown 1971) or birds in islands (Diamond 1969; Gilbert 1980).
In addition, the assumption of the SAR that sub-habitat heterogeneity increases with area does not necessarily hold in human-modified landscapes, where anthropogenic management practices may promote homogenisation (Lynch & Johnson 1974; Gilbert 1980; Mendenhall et al.
2014). For example, a seminal study by Diamond (1969) largely ignored human modification of the landscape when quantifying bird species richness and associated habitat complexity. By simply focusing on area and ignoring anthropogenic pressure, Diamond (1969) found an inverse relationship between richness and area. Subsequent studies that incorporate habitat complexity and human modifications (e.g. Mendenhall et al. 2014) found that the strength of model predictions increased (Diamond 1969; Power 1972;
Triantis et al. 2008; Mendenhall et al. 2014).
Chapter 1: Introduction 3
1.2 CONTEXT
The TIB is a fundamental theory in ecology that posits that more species will assemble in larger islands (or habitats) as a result of species turnover (immigration and extinction) resulting in a dynamic equilibrium
(MacArthur & Wilson 1967). Due to this theory’s simplicity, its constructs are commonly tested to identify and to understand the drivers of community assembly (MacArthur & Wilson 1967; Lomolino 1986, 1994; Brown &
Lomolino 2000; Lomolino 2000; Lomolino et al. 2010). However, many tested habitats have not been ideal for testing the TIB because they may not be completely isolated or cannot be studied from a point in time when they were empty of biota, which has led to mixed results (Lomolino 2000).
The TIB has also been the subject of controversy because many of its central assumptions are rarely, if ever, met (Heaney 2000; Lomolino 2000).
Limitations of the TIB include the observation that isolated habitats rarely reach a dynamic equilibrium (Connell 1978; Heaney 2000; Lomolino 2000), intervening habitats are more often heterogeneous than homogenous
(MacArthur & Wilson 1967; Lomolino 2000), inter-specific interactions are ignored (Brown & Lomolino 2000; Lomolino 2000), and island age and isolation are not considered (Ross et al. 2002; Whittaker et al. 2008; Keppel et al. 2010). These issues have led to significant debate and subsequent enhancements of the theory in its original form. For example, the general dynamic model of oceanic island biogeography (GDM) was proposed in 2008 and incorporates the additional explanatory factors of island age and degrees of isolation (Whittaker et al. 2008).
4 Chapter 1: Introduction
Examination of the isolated ecological communities presented in this research are drawn from the lines of reasoning that underpin the TIB
(Hubbell 2005; Whittaker et al. 2008). Although each isolated ecosystem was not tested directly for the presence of the dynamic equilibrium (MacArthur &
Wilson 1963; MacArthur & Wilson 1967), I did measure the abiotic factors that are thought to result in ecosystem equilibrium as described by MacArthur and Wilson (1967) and by those who have attempted to improve this model
(e.g. Whittaker et al. 2008). The factors related to the TIB tested in this research include habitat area (and more specifically the SAR), isolation and
(for pumice rafted communities only) age and trajectory into different climatic zones as a measure of isolation and also exposure to different abiotic conditions (Whittaker et al. 2008; Velasquez et al. 2018).
The following section introduces the first study system I investigated for my PhD research, which is based on pumice rafted community assembly.
1.2.1 Pumice rafting – testing the TIB by studying mass transportation of marine hitchhikers Pumice rafts provide a unique opportunity to test the central principles of the TIB, such as the SAR, by treating each pumice stone as a mini-island
(MacArthur & Wilson 1967). Pumice rafts are formed at the same time and location and comprise potentially trillions of replicates (i.e. individual floating pumice clasts), which are gradually colonised by marine biota as they float on the surface of the ocean (Bryan et al. 2012). Testing the pumice rafted biota in this way may provide new insights on elements of the TIB, such as the
SAR and community assembly theory and, more specifically, the abiotic and biotic filters that govern species composition of communities of shallow marine ecosystem-dwelling organisms.
Chapter 1: Introduction 5
The dispersal of such large numbers of organisms via pumice rafting also has implications for increasing genetic diversity of founder populations while also potentially allowing the transport of new species into these areas
(Bryan et al. 2012; Velasquez et al. 2018). This phenomenon may also have implications for the identification of potential pathways for the unassisted arrival of species considered to be marine pests, such as invasive species of mussels, barnacles, tunicates and algae (Chapin et al. 2000; Bryan et al.
2004; Bryan et al. 2012). Arrival of invasive species has commonly been attributed to human-mediated mechanisms, such as shipping (Leppäkoski &
Olenin 2000; Yamaguchi et al. 2009) or the aquarium trade (Semmens et al.
2004). However, we now know that pumice rafts have been documented to transport, the invasive acorn barnacle Megabalanus coccopoma (Darwin,
1854) to new shallow marine ecosystems in Australia, which may lead to displacement of more sensitive native species particularly in disturbed environments (Yamaguchi et al. 2009; Velasquez et al. 2018). An example of the damage possible as a result of colonisation of invasive species, include that of the red algae, such as Acanthophora spicifera in Hawaiian coral reefs, where its resistance to herbivory combined with rapid growth rates has resulted in reef losses (Lafferty & Kuris 1996).
The Havre Submarine Volcano, which is located in the subtropical marine zone of the Kermadec Arc (the longest underwater chain of volcanoes on Earth), erupted in July 2012 and this eruption formed an enormous pumice raft, which forms the basis of the first two chapters of this thesis (For details of the location of Home Reef, Havre Volcano and the Kermadec Arc, please see Appendix A Figure S1.) (Francis 1993; Cole 2001; Priestley 2012;
6 Chapter 1: Introduction
2012). This raft eventually affected >550,000 km2 of open ocean (equivalent to the surface area of France) and contained at least 3–4 1012 pumice clasts (Jutzeler et al. 2014). By examining the pumice rafted biota that has recently arrived on the eastern Australian coastline from this volcano, I aim to quantify and compare species composition on the pumice clasts and rafts of different sizes and differing trajectories. In conjunction with the data I collected from the Havre pumice raft, data collected for a previous study (see
Bryan et al. 2012) for Home Reef, Tonga, was combined with the data collected for the Havre pumice raft and used in the first chapter of this thesis
(Velasquez et al. 2018).
Pumice rafts formed from submarine volcanic activity in the South- western Pacific have been arriving every five to ten years on the eastern
Australian coastline for at least the past 200 years (Bryan 1971; Bryan et al.
2004; Bryan et al. 2012). Pumice rafts allow the transport of shallow marine ecosystem-dwelling organisms across oceans to the coastlines of continents and islands (Bryan et al. 2004; Bryan et al. 2012). However, the importance and subsequent consequences of these rafts for the rapid dispersal of otherwise dispersal-limited (limited in terms of time and space) benthic marine organisms to eastern Australia have only recently been realised
(Bryan et al. 2012; Velasquez et al. 2018).
Despite the recurring potential impact of these pumice rafting events, long-distance dispersal of shallow marine ecosystem-dwelling organisms via pumice rafting has not been widely studied (Bryan 1971; Bryan et al. 2004;
Bryan et al. 2012; Velasquez et al. 2018). Previous research has shown that more than 100 species of marine organisms have arrived to eastern Australia
Chapter 1: Introduction 7
from previous pumice raft events; for example, the 2012 eruption of Havre
Volcano, the 2006 explosive eruption of Home Reef Volcano and the 2001 eruption of an unknown volcano (0403-091) in Tonga (Bryan et al. 2004;
Bryan et al. 2012; Velasquez et al. 2018). Home Reef and the unknown volcano (0403-091) are located approximately 1478 and 1559 kilometres north-east of the Havre Volcano, respectively, and lie within the tropical zone
(Wunderman 2012). Thus it can be expected that differences between the biota that have colonised the Havre pumice reflect differences in species between these tropical and subtropical zones (Schiel et al. 1986; Francis
1993; Cole 2001). In addition, the pumice from the Home Reef eruption is on average much smaller (1–2 cm diameter), whereas the pumice surveyed from Havre is larger (4–5 cm diameter). This size difference may indicate that, if consistent with the SAR, the Havre pumice provides additional habitat space and hence could transport more species (Bryan et al. 2012).
Experiments examining the relationship between surface rugosity, floating stability and buoyancy on smooth plastic, styrofoam and pumice found that the high surface rugosity and stability of individual pumice clasts resulted in increased cover and richness, compared to other substrata (Bravo et al. 2011). While a study by Bryan et al. (2004) found that many pumice rafted invertebrates settled within crevices or depressions on the pumice clast surface. Further to this, Velasquez et al. (2018) found that the size of pumice clasts was an influential predictive variable for pumice species richness.
For the purposes of my PhD research, I have determined that pumice raft trajectory into tropical, subtropical or temperate zones can be considered
8 Chapter 1: Introduction
a measure of pumice raft isolation. Differing raft trajectories are influenced by wind drag, surface currents and wave motions; and the timing of shallow marine ecosystem encounters (Bucher & Saenger 1994; Bryan et al. 2012;
Velasquez et al. 2018). Raft trajectory into different climatic zones is considered to be a test of the concepts illustrated in the TIB and its subsequent iterations (e.g. the GDM) because the climatic zone of collection can be considered a test of the relative effects of isolation between different groups of floating pumice (i.e. pumice rafts) (MacArthur & Wilson 1963;
Macarthur & Levins 1967; Whittaker et al. 2008). For example, pumice rafts
(and the communities formed on them) collected in the tropical climatic zone took a very different trajectory to those collected in the subtropical and temperate climatic zones (MacArthur & Wilson 1963; Macarthur & Levins
1967; Whittaker et al. 2008). Therefore, tropical pumice rafts can collectively, be considered to have taken a very similar trajectory to other tropical pumice rafts and particularly to those washed ashore at the same time and place.
Similarly, pumice rafts that took a similar trajectory over the open ocean and had encounters with similar shallow marine ecosystems and levels of propagule pressure can be said to have “experienced” similar levels of isolation from source propagules and shallow marine ecosystem encounters, particularly when they arrived together at the same climatic zone and location
(MacArthur & Wilson 1967; Whittaker et al. 2008).
1.2.2 Threats to shallow marine ecosystems Shallow marine coastal ecosystems have been identified as the most likely oceanic environments to be threatened by the cumulative impacts of anthropogenic activities (Halpern et al. 2008; Clarke Murray et al. 2015).
Chapter 1: Introduction 9
Anthropogenic threats to shallow marine coastal ecosystems are numerous and include, for example, wide-spread and high impact ecosystem effects resulting from fishing (e.g. high bi-catch and habitat modifying techniques) and the effects of climate change such as increased temperatures and ocean acidification (Halpern et al. 2008; Clarke Murray et al. 2015). In addition, coastal ecosystems are also impacted by high threat but localised impact activities such as industrial development, and pollution from terrestrial run-off and shipping (Halpern et al. 2008; Hoegh-Guldberg & Bruno 2010; Clarke
Murray et al. 2015). Due to the vulnerability of coastal shallow marine ecosystems, understanding the processes which drive the formation of these communities is urgently needed if we hope to restore them in the future
(Jackson et al. 2001; Hoegh-Guldberg 2006).
Marine invertebrates and algae are fundamental to the complex food webs that underpin many shallow coastal marine ecosystems (Chapin et al.
2000). They are also one of the dominant primary structural building organisms of the world’s coral reefs, which provide many ecosystem services
(New 1995; Chapin et al. 2000). These services include coastal and storm surge protection, nurseries to fish stocks, habitat to endangered species (e.g. marine turtles and dugongs) and, in the case of the Great Barrier Reef, an estimated $5 billion per annum in revenue (Chapin et al. 2000; Hoegh-
Guldberg et al. 2007; Great Barrier Reef Marine Park 2009; Hoegh-Guldberg
2012). Despite being the most abundant and diverse creatures in the ocean, invertebrate and algae biology and their contribution to ecosystem integrity and subsequent services are still not fully appreciated or understood (New
1995).
10 Chapter 1: Introduction
Invasive marine invertebrates and algae distributed by ship ballast waters and other means have caused damage and lasting changes to many shallow coastal marine ecosystems and the services they deliver (Lafferty &
Kuris 1996; Chapin et al. 2000; Ricciardi 2007). Once established, removal of these animals can be difficult because the chemicals that might be used on land to extinguish pests in terrestrial environs or on ships before voyage will be immediately transmitted via the water column to other biota in the surrounds (Carr et al. 2003). Therefore, identification, containment and control of potential outbreaks at the early stages, or before establishment, is preferable for reducing the potential damage to sensitive marine environments and/or the resulting high-costs and labour to remove these pests (Yamaguchi 1986; Lafferty & Kuris 1996; Quilez-Badia et al. 2008;
Piola et al. 2009b).
For example, outbreaks of the crown of thorns starfish on the Great
Barrier Reef have increased because of degradation caused by anthropogenic pressures, such as increased nutrients in run-off (Pratchett
2005). These outbreaks have been shown to be one of the major causes of damage on the Great Barrier Reef since surveys began in the 1960s
(Pratchett 2005; Hoegh-Guldberg 2006; Great Barrier Reef Marine Park
2009). Another example is the introduced ctenophore, Mnemiopsis leidyi, which after being established in the Black Sea and because of the lack of native predators, achieved sufficient densities to consume a large proportion of zooplankton. This altered the food chain, which led to the collapse of fisheries in this area (Lafferty & Kuris 1996).
Chapter 1: Introduction 11
Climate change has resulted in changes in water temperature for coastal marine ecosystems which has resulted in ecosystem degradation or complete loss of communities (Hoegh-Guldberg et al. 2007; Hoegh-Guldberg
& Bruno 2010; Filbee-Dexter & Wernberg 2018). These changes increase the likelihood that the receiving environments of pumice rafted communities are biologically suitable to new arrivals and will allow their range expansion
(Alexander et al. 2016). This has been predicted to occur in two potential ways i) temperature thresholds might become biologically suitable where previously they were not, and ii) empty habitat space might be available where once it was not (Alexander et al. 2016). While previous studies of pumice rafted species diversity indicates that invasive species attached to individual clasts were present at low abundances (Bryan et al. 2012;
Velasquez et al. 2018). Without first identifying the pumice rafted species composition, current measures to mitigate the effects of potential range expansions of species will not be tailored to address the arrival of new and potentially invasive species transported into new habitats via pumice rafting.
Examination of pumice rafted communities allowed me to test the TIB,
SAR and additional abiotic and biotic factors on a set of island-like habitats which formed from unassisted community assembly processes (Bryan et al.
2012; Velasquez et al. 2018). However, due to the current losses of biodiversity globally, many extant ecological communities exist as degraded human-made remnants of what were once much larger and diverse ecosystems (Schemske et al. 1994; Hobbs & Yates 2003; Ellis & Ramankutty
2008).
12 Chapter 1: Introduction
Human-made remnant communities often contain rare or threatened species and ecosystems not found elsewhere (Schemske et al. 1994;
Kirkpatrick & Gilfedder 1995; Wintle et al. 2018). These communities are artificially reduced in area and are increasingly isolated from other extant populations of the same species or ecosystem type due to anthropogenic landscape modification (Kirkpatrick & Gilfedder 1995; Hobbs & Yates 2003;
Ellis & Ramankutty 2008). Studies of human-made remnant communities using ideas contained within the TIB and SAR, has the potential to provide new or missing information on the effects of reduced habitat area and increased isolation on their long-term survival (Schemske et al. 1994;
Kirkpatrick & Gilfedder 1995; Hobbs & Yates 2003; Kuussaari et al. 2009;
Wintle et al. 2018). The ability to provide missing information on a human- made rare or endangered community or species led me to choose to study an additional community for my PhD research. The community I chose is the critically endangered ecological community comprised of the tree Melaleuca irbyana ((D.E.E.) 2005a, b, 2017). Examination of M. irbyana remnant forests allowed me to compare use of the TIB, SAR and additional abiotic and biotic factors between a community formed from unassisted community assembly processes (i.e. pumice rafts) and a relatively human-made community formed from degrading processes (i.e. M. irbyana). At the same time, I hope to provide new information on the factors which influence survival and regeneration of M. irbyana within extant remnant forests. The following section introduces the second study system I investigated for my PhD research, which is based on my examination of remnant forests of M. irbyana.
Chapter 1: Introduction 13
1.2.3 Melaleuca irbyana – testing the TIB by studying urban forestry Melaleuca irbyana is an Australian tree that forms dense thickets. As an ecological community, it is federally listed as critically endangered under the
Environment Protection and Biodiversity Conservation Act 1999 and as an endangered regional ecosystem under the Vegetation Management Act 1999
(Queensland) ((D.E.E.) 2004, 2005b, 2017). Because of its growth on low- lying flood plains with alluvial clay soils (known as tea-tree clays) commonly adjacent to streams, this tree was extensively cleared for agriculture in the past and now occurs in small remnant forests within South-east Queensland and North-eastern New South Wales (Harms 1996; Vickers & Cuong 2004).
Recent surveys indicate that only 1000 hectares of this community remains intact, which is only 8.1% of its former range ((D.E.E.) 2004; Vickers & Cuong
2004; Soonthornvipat 2018).
This PhD research aims to test community assembly and some of the general tenets of TIB and the SAR by using remnant forest area and isolation, overstory and understory biodiversity, productivity and soil pH and nutrient profiles of remnant forests of M. irbyana as explanatory variables to indicate the “health” of the remnant forest areas. A healthy remnant forest is one that is regenerating naturally (i.e. seedling establishment of M. irbyana is taking place) taking into account the known lifecycle of this species
(Schemske et al. 1994; Vickers & Cuong 2004; Soonthornvipat 2018). A potential outcome of this study is to improve understanding of the demographic status of this species and whether wild populations are stable, increasing or decreasing in abundance and at what point in its life cycle it is most vulnerable to reproductive failure (Schemske et al. 1994). These
14 Chapter 1: Introduction
relationships have been investigated to assist local, state and federal governments to more confidently manage the remaining remnant forests of this ecosystem and promote its survival into the future (Shaffer 1981;
Schemske et al. 1994; Kuussaari et al. 2009; Wintle et al. 2018).
1.2.4 Threats to remnant forests of Melaleuca irbyana Loss of native terrestrial ecosystems is increasingly caused by the urbanisation of the landscape (Duraiappah et al. 2005; Fischer et al. 2006).
As a result, our attention for the preservation of biodiversity and rare or endangered species now commonly rests on those remaining ecosystems or fragments of ecosystems that remain in a context of human-modified habitat such as urban or farmland contexts (Schemske et al. 1994; Kirkpatrick &
Gilfedder 1995; Ross et al. 2002; Lake & Leishman 2004; Van Rossum 2008;
Kuussaari et al. 2009; Wintle et al. 2018). However, questions arise for governments and reserve managers about the value of conserving these remnants, and if preservation is deemed worthwhile how to best achieve preservation both now and into the future (Schemske et al. 1994; Shafer
1995; Godefroid & Koedam 2003; Van Rossum 2008; Wintle et al. 2018).
Anthropogenic pressures that impact upon these ecosystem remnants include increased eutrophication via storm-water run-off and drains (Lake &
Leishman 2004), edge effects (e.g. increased solar irradiance and wind speeds at the boundary of the reserve as well as within the reserve because of pathways bisecting remnants) (Ross et al. 2002; Leishman & Thomson
2005), loss or alteration of natural disturbance regimes (e.g. fires or floods)
(Pickett & Thompson 1978; Schemske et al. 1994; Yates et al. 1994; Ross et al. 2002), increased human traffic (which can also transport non-native
Chapter 1: Introduction 15
species) (Lake & Leishman 2004; Leishman & Thomson 2005), and the potential loss of genetic diversity due to small population sizes resulting in in- breeding (Schemske et al. 1994; Ross et al. 2002; Godefroid & Koedam
2003; Hobbs & Yates 2003; Lake & Leishman 2004; Van Rossum 2008). In addition to these problems, research has shown that, in many cases, the smaller the fragment size the more species will be lost as it ages, which is often termed an extinction debt (Shafer 1995; Ross et al. 2002; Laurance
2008; Kuussaari et al. 2009).
Despite these problems, research has demonstrated the worth of preserving these small pockets of remnant ecosystems for their intrinsic worth (e.g. for protecting remaining pockets of rare species such as M. irbyana) and for the ecosystem services they can still provide, such as reduction of air pollution particulates, temperature regulation, carbon sequestration and noise reduction (Shaffer 1981; Shafer 1995; Fahrig 2003;
Escobedo et al. 2011; Lindenmayer 2018; Wintle et al. 2018). Therefore, to manage these remnant ecosystems into the future, managers and governments require information on both the biotic (species interactions, responses and effects) and the abiotic (environmental cues (e.g. flood or fire), remnant size and/or context) (Schemske et al. 1994; Ross et al. 2002;
Kuussaari et al. 2009; Wintle et al. 2018). Expanding such knowledge will help to allow the continued regeneration and resistance of these remnant ecosystems, particularly in the face of a changing climate (Simberloff & Abele
1982; Schemske et al. 1994; Shafer 1995; Ross et al. 2002; Fensham et al.
2015).
16 Chapter 1: Introduction
1.3 PURPOSES
The main aims of the research presented in this thesis is to examine two rarely studied and comparatively different ‘island-like’ ecosystem contexts (i.e. pumice rafting and remnants of M. irbyana forest) to improve understanding of the key biotic and abiotic factors that drive the resultant community assembly in time and space for these systems (Crawley et al.
1986; Funk et al. 2008). The two different study systems were chosen purposefully for this PhD research to compare the differences and similarities between a community which formed from unassisted community assembly processes and a human-made community formed from habitat fragmentation and degrading processes. For each community, comparisons were made between the drivers of community assembly, and the applicability of theory, such as the TIB and the SAR, in helping us to understand them.
The two study systems firstly differ in their context. Pumice rafts exist in the marine environment, whereas M. irbyana exists within terrestrial landscapes. Secondly, they were formed in very different ways. Pumice rafted island-like communities can be considered to be formed from unassisted dispersal and colonisation processes (Bryan et al. 2012;
Velasquez et al. 2018). This is because pumice rafted communities are formed by unassisted processes (i.e. volcanic eruption) and are colonised by marine animals and plants as they float through the ocean and encounter differences in temperature and propagule pressure from underlying species pools (Bryan et al. 2012; Velasquez et al. 2018).
In contrast to pumice rafting, remnant forests of M. irbyana are relatively human-made islands formed as a result of the extensive clearing of what
Chapter 1: Introduction 17
once was a much larger intact native ecosystem (Vickers & Cuong 2004;
Soonthornvipat 2018). In this context key processes, such as natural disturbance regimes are most likely missing or disrupted (Pickett &
Thompson 1978). As a result, studies such as this PhD research into M. irbyana communities attempts to piece together the original puzzle (i.e. original ecosystem processes) even when key pieces, such as natural disturbance regimes, are likely missing or disrupted (Pickett & Thompson
1978; Hobbs & Yates 2003).
Both ecosystem contexts have been rarely studied, as for both, there are very few published studies examining them. For example pumice rafting has been examined to the best of my knowledge in four papers (see Bryan
1971; Bryan et al. 2004; Bryan et al. 2012; Velasquez et al. 2018). With the most comprehensive studies documenting all biota on more than 5000 pumice clasts occurring in 2012 and 2018 (see Bryan et al. 2012; Velasquez et al. 2018). While for M. irbyana there have been even fewer studies and resultant publications on this critically endangered ecosystem with the most comprehensive being an honours thesis completed by Vickers and Cuong
(2004) and a PhD Thesis completed by Soonthornvipat (2018). The knowledge gaps that exist for each ecological community have provided an opportunity for research such as this PhD to aim to provide additional understanding of the most influential processes resulting in community assembly and resistance within each context.
Additional aims of this PhD research were to use these unique contexts to re-examine elements of one of the oldest theories in ecological science the
TIB and its central premise the SAR and to ascertain its continued value (or
18 Chapter 1: Introduction
otherwise) as a starting point, and possibly an end point, for the examination of these systems (MacArthur & Wilson 1963).
Overall, I found that the key factors that explain diversity for the ecosystems examined vary dependent on context, including the abiotic and biotic conditions in which an isolated habitat is situated, rather than adhering to a strict pattern (e.g. the SAR) as described in the TIB (MacArthur & Wilson
1963; Whittaker et al. 2008). For example, in pumice rafted communities, I find that while the central premise of the TIB such as the SAR has continued merit for describing patterns of diversity (e.g. species richness and functional trait diversity) forming on pumice clast surfaces, additional predictors such as the age of individual pumice clasts and climatic zone of collection are beneficial and often more influential for describing the resultant community assembly (see Velasquez et al. (2018) and Chapters 3 and 4). In contrast to my study of pumice rafted communities, my examination of fragmented remnant forests of M. irbyana showed that both remnant isolation and the
SAR (see Chapter 5) were ineffective for predicting the drivers of ecosystem health. In that study, the key drivers of seedling establishment (a relevant definition of ecosystem health for this particular forest type) were strongly linked to disturbance regimes (e.g. fire) that led to the death of mature overstory trees within the remnant forests and which occurred independently of remnant forest area (Pickett & Thompson 1978; Yates et al. 1994; Ross et al. 2002; Vickers & Cuong 2004).
Because of conflicting evidence, where the principles of the TIB have been both useful (e.g. for predicting pumice rafted community assembly in time and space) but at the same time cannot explain the key processes
Chapter 1: Introduction 19
affecting resultant community assembly in space (e.g. the establishment of
M. irbyana seedlings), the TIB has been criticised extensively (see Gilbert
1980; Laurance 2008). This criticism is mostly in relation to the strict manner in which many subsequent ecologists and biologists have applied its principles. For example, by assuming that the SAR will hold despite landscape modification and therefore large patches of habitat have higher conservation value (for example, see Diamond 1969). Or when the TIB and
SAR are used by conservation managers to exclusively promote the preservation of large habitat remnants with high connectivity, while undervaluing or ignoring the potential conservation value of small isolated habitat remnants (Wintle et al. 2018). However, the TIB has been shown to have continued merit (see Whittaker et al. 2008) when it is adapted to include further contextual information such as the age of isolated habitats (Ross et al.
2002; Keppel et al. 2010).
Although I found conflicting evidence in support of the TIB and SAR, I found that it remains reasonable to use these models, at the very least as a starting point, when examining the drivers of ecosystem form and function in time and space (Lomolino 2000). However, this should be done cautiously and must also consider the diversity of abiotic and biotic factors in which an ecosystem exists in time and space and, where possible, additional data should be collected. Examples of additional data that might be helpful include alternative abiotic influences such as seasonal or latitudinal temperature gradients or consideration of biotic drivers such as foundation species effects
(Lynch & Johnson 1974; Brown & Lomolino 2000; Lomolino 2000; Gil &
Pfaller 2016; Velasquez et al. 2018).
20 Chapter 1: Introduction
1.4 THESIS OUTLINE
This thesis is presented as a series of studies that are intended for publication as journal papers. At the time of writing of this thesis, the third chapter is published, while chapters 4 and 5 have been prepared for submission to journals relevant to the field of study. At the beginning of chapter 3, the citation is given and all listed authors and their contributions are acknowledged.
Chapter 2
In this chapter, I review the literature with the aim of providing the context behind the TIB by detailing both the historical and modern iterations and adaptations of the theory, which have aided its continued use in ecological research. Also included are the criticisms of the theory and how its application should be used flexibly acknowledging that it is not always a good predictor of species or functional trait richness in certain contexts.
Chapter 3
This chapter is a published paper where I provide evidence in support of the continued use of the central premise of the TIB, namely the SAR, in the rarely studied ecological context, of pumice rafting. Here, I examine the data from two pumice rafting events—the 2006 eruption of Home Reef and the 2012 eruption of the Havre Volcano and their associated pumice rafts—in relation to traditional SAR predictive variables such as area. I have also included in the analysis the later additions of both the age and climatic context as a measure of isolation.
Chapter 1: Introduction 21
Findings from this work have found strong connections between pumice rafted epibiont richness and the SAR. The models are strengthened by the use of further driving processes such as the age of the pumice clasts
(measured as the duration of time spent afloat in open ocean from the day of eruption to collection on the coastlines of islands and continents) and the climatic zone of pumice raft arrival, which gave an indication of the water temperatures and changing species pools that influenced pumice rafted species diversity most strongly.
Chapter 4
In this chapter, I explore the pumice rafted community for the Havre
Volcano only in relation to the functional traits of the community that forms on individual pumice clast surfaces. This was again done in relation to the SAR, namely habitat area, and included the additional predictive variables of age and climatic zone of collection.
Here I found that the SAR was a good predictor of community trait richness on individual pumice clasts and that the models were improved when the additional predictive variables of pumice age and climatic zone of collection were also considered. I also found evidence that barnacles of genus Lepas had a facilitative foundation species effect for increased community richness which formed on floating pumice ecosystems.
Chapter 5
In this chapter, I examine the TIB and SAR in relation to a different ecological context, the remnant forests of the critically endangered ecosystem M. irbyana (swamp tea-tree). Twelve isolated remnant forest
22 Chapter 1: Introduction
areas containing M. irbyana within south-eastern Queensland were examined and quantified in terms of their overall “health” as measured by the establishment of M. irbyana seedlings into the understory. Remnant forest health was then examined in relation to the potential predictive variables of area, isolation, overstory and understory diversity (both native and non- native), productivity, soil characteristics and evidence of disturbance.
In this study, I found no relationship between the TIB (i.e. area and isolation) and my definition of remnant forest health (i.e. seedling establishment). Establishment of seedlings related more closely to the disturbance history of mature overstory trees and soil characteristics (e.g. amount of nitrogen and pH) than to the remnant forest area or isolation within the environment.
Chapter 6
In this final chapter, I examine the contribution that this PhD research has made generally to ecological theory. I also highlight its contribution to the management strategies that may be altered in light of the increased understanding of the key drivers of community assembly in the two rarely studied contexts I investigated. In this chapter, I compare and contrast the different conclusions I reached via applying principles detailed in the TIB and
SAR to these two rarely studied ecosystems. I also summarise my key findings, describing the limitations, and suggesting future research in these areas.
Chapter 1: Introduction 23
Chapter 2: Literature review
2.1 HISTORICAL BACKGROUND
For the purposes of this chapter, I outline a brief history of the TIB, including descriptions of the most influential studies that have used it as a predictive model in the study of community assembly in space and time. This is followed by analysis of its limitations as a model, combined with reasoning as to why, despite these limitations, the theory of island biogeography (TIB) has continued value at the very least as a useful starting point in the study of the key drivers of community assembly in different contexts.
Despite the widespread use of the TIB as a simple model for understanding how species assemble in insular habitats, it has been marred by controversy because many studies have found that the equilibrium state is rarely, if ever, achieved in nature (Lynch & Johnson 1974; Gilbert 1980;
Lomolino 1994; Heaney 2000; Lomolino 2000). In what is considered by many to be the most comprehensive test of the theory to date, Simberloff and
Wilson (1969, 1970) removed all terrestrial arthropods, by methyl bromide tent fumigation from six small islands in Florida Bay, and monitored recolonisation at frequent intervals for one year (Simberloff & Wilson 1969,
1970). They found that recolonisation occurred as described by the TIB’s dynamic equilibrium; that is, recolonisation increased sharply at first (when resources were not saturated) and tapered off to reach a stable point that
Chapter 2: Literature review 25
was balanced by immigration and extinction (the dynamic equilibrium) once resources became saturated (Simberloff & Wilson 1969, 1970).
However, in later follow-up studies, Simberloff (1976) suggested that the initial research (see Simberloff & Wilson 1969, 1970) overestimated the amount of actual turnover and attributed some to a form of ‘pseudo-turnover’, a term coined by Lynch and Johnson (1974). Pseudo-turnover is defined as an example of overestimating the turnover of species because temporary immigrants to islands are counted as the presence of legitimate breeding pairs and extinctions are recorded for individuals merely transiting through a suitable habitat (Lynch & Johnson 1974; Simberloff 1976). Simberloff (1974) initially also considered Diamond’s (1969) study to support the theory, which is contested by Lynch and Johnson (1974) and Gilbert (1980). Later, even
Simberloff (1976) alludes to Diamond’s (1969) study as being possibly indicative of ‘pseudoturnover’ for the same reasons (Diamond 1969; Lynch &
Johnson 1974; Simberloff 1974; Simberloff 1976).
In Diamond’s (1969) study, species richness of birds was quantified and compared between two surveys (one in 1917 and the other in 1968) of nine islands off the coast of Southern California (Diamond 1969). Diamond’s study concluded that bird richness remained constant between the surveys as a result of immigrations and extinctions, and thus demonstrated that a dynamic equilibrium was occurring (Diamond 1969). However, Lynch and Johnson
(1974) (with later support from Gilbert (1980)) contest this conclusion on three key grounds. Firstly, the initial study by Howell (1917), which contained the primary data for comparison in Diamond’s (1969) work, was in fact a collation of records and anecdotal evidence dating from the 1860s until 1917
26 Chapter 2: Literature review
and was not a comprehensive field survey of resident bird species for the specified period in time (Diamond 1969; Lynch & Johnson 1974; Gilbert
1980). Secondly, Diamond did not consider the human modification of the landscape significant enough to cause the extinction of bird species in these islands in addition to normal equilibrial turnover (Lynch & Johnson 1974;
Simberloff 1976; Gilbert 1980). However, it has been shown that habitat heterogeneity or complexity and modification by anthropogenic means has an effect on species richness and must be taken into account (Power 1972;
Simberloff 1976; Gilbert 1980; Mendenhall et al. 2014).
Thirdly, the inability to record the true immigration of a highly mobile animal such as a bird (via breeding) and its subsequent extinction (via mortality or migration elsewhere) and yet recording the presence of a bird
(sighting it in the field) as a colonisation and subsequent absence as an extinction led Lynch & Johnson (1974) to term this artefact ‘pseudo-turnover’.
This misinterpretation of the scientific evidence (immigration and emigration interpreted as colonisation and extinction, respectively) is also acknowledged by Diamond (1969) and is particularly misleading because it increases the rate of equilibrial turnover by an unknown amount (Diamond 1969; Lynch &
Johnson 1974; Simberloff 1976; Gilbert 1980). Gilbert (1980) also noted that
Diamond (1969) found that species richness was inversely proportionate to island area, which is in contradiction to principles of the TIB namely the SAR
(Diamond 1969; Gilbert 1980).
Chapter 2: Literature review 27
2.2 THE TIB AND ITS APPLICATION IN MODERN ECOLOGICAL
STUDIES
Despite these limitations, lines of reasoning that underpin the TIB and its central principles, such as the SAR, are frequently used to study plant and animal community assembly within insular habitats (e.g., Godefroid &
Koedam 2003; Goldstein et al. 2014; Mendenhall et al. 2014). This has been done with some success, particularly when the TIB is tested in consideration of modern advancements to the theory (Brown & Lomolino 2000; Lomolino
2000; Whittaker et al. 2005; Laurance 2008; Whittaker et al. 2008).
For example, Whittaker et al. (2008) proposed the general dynamic model of oceanic island biogeography (GDM), which includes alterations to the TIB that incorporate processes operating on geological and evolutionary timescales. The GDM expands on the TIB’s original concepts of immigration and extinction by including processes of oceanic island lifecycle (Darwin
1859) and the impact these processes have on island biota both in time and space (Darwin 1859; Whittaker et al. 2008). The GDM proposes that species richness is not linear but instead increases quickly (upon island formation) before reaching a plateau because of interactions between age (time) and area, and that isolation removes certain species from the pool of immigrants
(Whittaker et al. 2008). These additional factors were tested in the study of
Keppel et al. (2010), who used the strength of predictive variables such as age, area, isolation (via the proximity to source propagules) and the additional abiotic factor of cyclone strength and frequency to assess drivers of lowland rain forest community assembly in islands of the tropical South
Pacific. Keppel et al. (2010) found that both island age and area were the
28 Chapter 2: Literature review
strongest predictors of species richness and that island age and isolation were the strongest predictors of endemism.
2.3 THE TIB IN MARINE CONTEXTS
Dispersal and colonisation processes are an important area of research for understanding both community assembly and the invasion of ecosystems by new species (Shea & Chesson 2002; Kinlan & Gaines 2003). As described by Shanks et al. (2003), dispersal of benthic marine larvae is thought to occur primarily as a result of propagule (e.g. spores, eggs and larvae) transportation away from source populations (Shanks et al. 2003). By contrast, colonisation can be defined as the immigration, persistence and population increase of an organism in an insular environment (MacArthur &
Wilson 1967). Dispersal and colonisation processes are essential for restoration and establishment of new or beneficial species in an area and can be understood and then managed to control invasive species (Shea &
Chesson 2002; Shanks et al. 2003).
Dispersal processes vary greatly between marine and terrestrial environs (Carr et al. 2003; Kinlan & Gaines 2003). For example, Kinlan and
Gaines (2003) found that dispersal distances of sedentary marine organisms exceeded that of terrestrial plants by one to two orders of magnitude and that the shortest average dispersal distance for marine organisms equalled the maximum average distance of dispersal for terrestrial plants (Kinlan & Gaines
2003). However, most marine organisms are still separated by thousands of kilometres of open ocean (Shanks et al. 2003). Studies have shown that many marine propagules survive only for a few days before they must find a
Chapter 2: Literature review 29
location to colonise and that they can travel up to one kilometre from parent organisms to do so (Shanks et al. 2003).
Despite the importance of dispersal for contributing to community dynamics, dispersal within the marine environment is still poorly understood
(Kinlan & Gaines 2003). As a result, recent interest has focussed on examination of floating objects in the marine environment, such as wood, algae, pumice and plastic debris, which have all been found to aid in the dispersal of marine biota across vast distances in the ocean (Bryan et al.
2012; Goldstein et al. 2014; Gil & Pfaller 2016; Velasquez et al. 2018). The study of pumice rafting provides a unique opportunity to study one of the processes of dispersal of shallow marine organisms and allows the potential addition of much needed new knowledge to this field (Bryan et al. 2004;
Bryan et al. 2012; Velasquez et al. 2018). Understanding the phenomenon of pumice rafting is important because of its ability to transport marine organisms rapidly over long distances and across deep oceans (for example,
>5000 km from Tonga and 3000 km from Havre) (Bryan et al. 2012; Jutzeler et al. 2014). Pumice rafts contain trillions of individual clasts, each of which can act as a rafting vehicle for marine organisms and provide opportunities for long-distance dispersal while overcoming physiological and biogeographic or climatic limitations (Bryan et al. 2004; Bryan et al. 2012; Priestley 2012;
Velasquez et al. 2018).
The eruption of the Havre Seamount, previously thought to be a dormant or extinct volcano, forms the foundation of this project and the subsequent investigation of long-distance dispersal mechanisms of marine invertebrates (Priestley 2012; 2012). The Havre Volcano, lies in the
30 Chapter 2: Literature review
subtropical zone of the Kermadec Isles mid-way between New Zealand and
Tonga (2012). Pumice from this event subsequently arrived on the eastern
Australian coastline beginning in March 2013 and continued to arrive for the next two years. The Havre eruption was further south than previous eruptions
(e.g. Home Reef in 2009), which led to the prediction that pumice rafted communities could contain a mix of both tropical and temperate species resulting in communities comprised of a higher species diversity than that of the Home Reef study, which comprised mostly tropical species (Bryan et al.
2004; Bryan et al. 2012).
Pumice rafting is a mechanism that has transported large numbers of marine invertebrates to the east coast of Australia (Bryan et al. 2012;
Velasquez et al. 2018). Pumice rafting has the potential not only to spread shallow marine ecosystem pests but to also enrich populations of existing marine invertebrates (Bryan et al. 2004; Bryan et al. 2012; Velasquez et al.
2018). Dispersal of such large numbers of organisms has implications for increasing genetic diversity of founder populations while also allowing the transport of new species (Bryan et al. 2004; Lockwood et al. 2005; Bryan et al. 2012; Velasquez et al. 2018). The successful dispersal and subsequent colonisation of marine invertebrates has often been attributed to those species that arrived via ship ballast waters or encrusted on the sides of ships
(Ruiz et al. 2000; Ricciardi 2007; Piola et al. 2009a). Although marine invertebrates that encrust ships can be managed to some degree using anti- fouling chemicals before voyage, such chemicals often cannot be used once the invasive organism becomes established in a sensitive marine ecosystem
(Piola et al. 2009b).
Chapter 2: Literature review 31
The examination of pumice rafted biota will aim to perform novel tests of the SAR and to demonstrate how biodiversity of the Home Reef and Havre pumice is affected by the size of individual pumice clasts (MacArthur &
Wilson 1967). In addition, additional variables, such as those suggested by the GDM, will also be tested by examining the relative age of the pumice clasts (measured as days elapsed since eruption and subsequent collection on coastlines) and the effects of isolation as measured by the climatic zone of collection both on species richness and community trait composition
(Whittaker et al. 2008; Velasquez et al. 2018). An assessment of the reproductive and feeding traits of the pumice rafted biota will be undertaken to assess dominance or otherwise in the pumice rafted community. While indications of facilitative processes occurring within the community, for example the initial colonisation of a founder species, which increases the chances of survival in subsequently colonising biota, will also be examined
(Gil & Pfaller 2016).
Previous studies examining the SAR in relation to floating objects have found evidence in support of the lines of reasoning underpinning the TIB.
Two studies that investigated the diversity of communities colonising floating plastic objects within the Pacific ocean found that increasing habitat harboured increases in diversity, as per the SAR (Goldstein et al. 2014; Gil &
Pfaller 2016). Goldstein et al. (2014) hypothesised that this was due to larger objects having increased habitat and stability at the surface of the ocean, which is associated with increased migration, as predicted by the TIB. By contrast, Gil and Pfaller (2016) hypothesised that barnacles from the species
Lepas facilitate colonisation on smooth plastic surfaces by providing
32 Chapter 2: Literature review
increased diversity of habitat on inhospitable plastic surfaces. Both studies found evidence in support of the SAR with the study of Gil and Pfaller (2016) also providing evidence of the influence of Lepas barnacles causing increases in diversity of the organisms colonising plastic debris, particularly of coastal dwelling motile species (Gil & Pfaller 2016).
Further evidence in support of using the SAR to understand marine community ecology is shown in experiments performed by Osman (1978) and Anderson (1999) who both tested the SAR in two in situ experiments.
Osman (1978) tested the SAR by examining invertebrate settlement on different sized boulders and pieces of slate at two different times of the year in shallow marine waters located at Nonamesset Island, Massachusetts.
Anderson (1999) examined invertebrate settlement on marine plywood of different sizes at two different times of the year in shallow marine waters located at Salamander Bay, New South Wales. Both studies found that the relationship between habitat area and colonisation differed at different times of the year. Osman (1978) found that this related to the rate at which species colonisation occurred, which was slower or faster according to the season and associated larval establishment. Anderson (1999) found that the SAR increased with time in spring and decreased with time in late summer.
2.4 THE TIB AND URBAN FORESTRY
Since its inception, the TIB has been tested in multiple contexts to determine both its utility as a model of the natural world and whether it can be extended to allow managers to determine the best strategies for conservation of remaining wilderness areas (Simberloff & Abele 1982;
Chapter 2: Literature review 33
Laurance 2008). The fundamental premise of the TIB suggests that larger remnant reserves should contain more species than smaller ones (MacArthur
& Wilson 1967). However, according to Simberloff and Abele (1982), the TIB is actually neutral with regard to whether a single large or several small reserves are adequate to protect a species or ecosystem because this question is an empirical one requiring further research specific to each unique context (Simberloff & Abele 1982). In addition, for many species, there is no longer a choice to consider conservation of larger or smaller tracts of intact habitat, and scientists and land managers must work to conserve species and ecosystem services within the habitat fragments that remain
(Schemske et al. 1994; Shafer 1995; Fahrig 2003; Ross, 2002 #800; Hobbs
& Yates 2003; Wintle et al. 2018). Many studies have tested empirically whether the SAR holds in relation to the conservation of species richness and also in relation to the protection of particular target species within remnant reserves (Kitchener et al. 1980; Simberloff & Abele 1982; Ross et al.
2002; Matthews et al. 2014; Mendenhall et al. 2014). These studies have resulted in multiple conclusions, which are mostly species and ecosystem specific (Kitchener et al. 1980; Simberloff & Abele 1982; Ross et al. 2002;
Matthews et al. 2014; Mendenhall et al. 2014).
Terrestrial ecosystem processes are often unable to be predicted by the
SAR alone, and multiple outcomes are found possible when examining the drivers of resultant species richness in island-like habitats or habitat remnants (Ross et al. 2002; Fahrig 2003; Laurance 2008; Mayfield et al.
2010). For example, studies have found that the required habitat complexity or ecosystem processes were not only available to biota in large reserves but
34 Chapter 2: Literature review
could often be found in smaller reserve sizes (Kitchener et al. 1980; Ross et al. 2002; Wintle et al. 2018). For example, Kitchener et al. (1980) found that, while lizard richness in the Western Australian wheatbelt was related to reserve size, small reserves with intact vegetation diversity were also valuable refuges for lizard species. In addition, when models incorporated habitat diversity this was a stronger predictor of lizard richness than those incorporating area alone (Kitchener et al. 1980). A study of avifauna diversity on a Californian island also found vegetation richness, which corresponded with latitude (i.e. wetter, larger islands have greater vegetation diversity), correlated more strongly with increased diversity of birds rather than simply island area or isolation (Power 1972). While Ross et al. (2002) found that in
Eucalyptus forest fragments an examination of species richness in relation to fragment size, age, anthropogenic disturbance and fire history, that age and disturbance history were the most important predictive variables of species diversity and that native richness increased after fire but decreased in smaller remnants greater than 10 years old. More recently, Wintle et al. (2018) found that small isolated remnant ecosystems had higher conservation value than larger remnants because the species they contained were not found elsewhere.
Alternatively, Brown (1971) when examining mammals inhabiting montane island habitats found a close correlation between the area of the habitat and the number of mammal species. While the findings of Keppel et al. (2010) support the GDM in showing that both island area and age were significant variables for explaining differences in species richness and composition across 10 tropical South Pacific islands (Keppel et al. 2010).
Chapter 2: Literature review 35
Keppel et al. (2010) concluded that endemic species correlated with islands of older age and greater isolation, and that older and larger islands had the greatest species richness and diversity (Keppel et al. 2010).
2.5 SUMMARY AND IMPLICATIONS
The TIB and SAR have been tested by a multitude of studies as a basis for understanding the natural world (Simberloff & Abele 1976; Simberloff &
Abele 1982; Lomolino 2000). Hence in this thesis, I have examined two different insular ecosystems i) marine communities that form on the surface of pumice clasts floating in the South-western Pacific and ii) remnants of a critically endangered forest ecosystem located in a matrix of peri-urban, urban and farmland contexts. For both of these systems, I have recorded and examined multiple abiotic and biotic factors to determine: i) for the pumice rafting study, their effects on resultant community composition, species richness and functional trait richness and ii) for the Melaleuca irbyana study, as a test of ecosystem resistance and health. It is never possible to know certainly whether the TIB or the SAR will hold for a particular ecosystem type, regardless of this it is often used initially to understand how ecosystem processes operate (Lomolino 2000; Whittaker et al. 2008). This is particularly true as the TIB and the SAR continues to be of interest to modern ecosystem managers for identifying which abiotic and biotic factors have the strongest effects on resultant ecosystem function and resistance to pertubation
(Lomolino 2000; Whittaker et al. 2008). The use of concepts contained within the TIB and the SAR as a starting point to think predictively about the abiotic and biotic drivers of different communities and ecosystem processes in space and time is still relevant today (Whittaker et al. 2005; Whittaker et al.
36 Chapter 2: Literature review
2017). Studies such as this one allow not only the assessment of what may be causing resultant ecosystem change in the insular environment being examined but at the same time, allow discussion about the relevance of the
TIB and the SAR in the current modern context (Lomolino 2000).
In my examination of pumice rafted biota in the marine context, I hypothesise that the SAR will hold with larger pumice clasts containing increased species richness and possibly functional traits (Cadotte et al.
2011). At the same time, I expect that through time (age), older pumice clasts will exhibit further increases or changes in community composition drawing from the ideas contained in the GDM (Whittaker et al. 2008). In addition, I expect that the community composition will change dependent on pumice clast trajectory to differing climatic zones (as a measure of relative isolation between pumice rafts) because underlying species pools will be altered and, at the same time biological thresholds for certain biota will be exceeded
(Wichmann et al. 2012).
For M. irbyana, I hypothesise that larger and less isolated remnant forests will contain increased seedling establishment, preserved remnant forest health and greater productivity (as measured by stand density) because larger remnant forests should be protected from the mitigating effects of anthropogenic disturbance including edge effects (e.g. increased solar radiation, wind speed, nutrient loads and non-native species establishment) (Ross et al. 2002; Lake & Leishman 2004). I expect the incidence of non-native species to increase as remnant forest size decreases because of a reduction in both human and introduced animal traffic in a larger remnant forest, alongside a reduction in the quantity of wind-dispersed
Chapter 2: Literature review 37
seeds (e.g. from non-native grasses and garden plants) making their way from edges into the centre of a large remnant forest (Lake & Leishman 2004).
In conjunction with this, I expect large remnant forests would have reduced nutrient loads and hence further reduction in non-native species.
I expect that both studies will provide new knowledge about each rarely studied ecosystem context, which will help further the understanding of the ecological drivers for each context. For pumice rafting we may gain new knowledge on this previously little-known phenomena and its ability to transport trillions of marine biota over thousands of kilometres of open ocean
(Bryan et al. 2012; Velasquez et al. 2018). It is hoped that this information will increase understanding about how non-native or invasive species reach new habitat providing an opportunity for colonisation, and the manner in which both sessile and motile biota colonise and thrive in new habitats within the marine environment (Bryan et al. 2012; Gil & Pfaller 2016).
For M. irbyana it is hoped that new knowledge will be gained on the conditions that allow M. irbyana seedlings to become established in the understory of remnant forests. At the same time I hope to highlight those ecological factors that cause ecosystem resistance and reduction of non- native species within M. irbyana forests. This may then allow managers of this ecosystem to develop different management strategies for the remaining forests, including alternative disturbance regimes.
38 Chapter 2: Literature review
Chapter 3: Journal article: Testing the
Theory of Island
Biogeography and
subsequent evolutions
SYNOPSIS
This chapter includes the content of a journal article which has been published in the journal Ecology and Evolution. For this article the reference for the publication is:
Eleanor Velasquez, Scott Bryan, Merrick Ekins, Alex G. Cook, Lucy Hurrey and Jennifer Firn. 2018. Age and area predict patterns of species richness in pumice rafts contingent on climatic zone encountered Ecology and Evolution 8: 5034-5046
AUTHOR CONTRIBUTIONS
EV, JF, and SEB designed the study. EV collected the data for the
Havre eruption, developed the models, performed the analysis, and wrote the first draft of the manuscript. JF assisted with both statistical analysis and manuscript development. SEB collected the data for the Home Reef eruption.
ME, AGC, and LH all assisted with marine biota identification. SEB, ME,
AGC, and LH all contributed to editing the manuscript.
Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions 39
3.1 ABSTRACT
The theory of island biogeography predicts that area and age explain species richness patterns (or alpha diversity) in insular habitats. Using a unique natural phenomenon, pumice rafting, we measured the influence of area, age, and oceanic climate on patterns of species richness. Pumice rafts are formed simultaneously when submarine volcanoes erupt, the pumice clasts breakup irregularly, forming irregularly shaped pumice stones which while floating through the ocean are colonized by marine biota. We analyze two eruption events and more than 5,000 pumice clasts collected from 29 sites and three climatic zones. Overall, the older and larger pumice clasts held more species. Pumice clasts arriving in tropical and subtropical climates showed this same trend, where in temperate locations species richness
(alpha diversity) increased with area but decreased with age. Beta diversity analysis of the communities forming on pumice clasts that arrived in different climatic zones showed that tropical and subtropical clasts transported similar communities, while species composition on temperate clasts differed significantly from both tropical and subtropical arrivals. Using these thousands of insular habitats, we find strong evidence that area and age but also climatic conditions predict the fundamental dynamics of species richness colonizing pumice clasts.
3.2 INTRODUCTION
The globe is experiencing its sixth mass extinction event, and considerable evidence suggests that native biodiversity is being lost as a result of human activities (see Ceballos et al. 2015). Concurrent with this loss 40 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
is the increasing homogenization of biotas across countries and even continents via the widespread transport and establishment of species
(Cardinale et al. 2012; Hooper et al. 2012). Due to increasing numbers of non-native and potentially invasive species arriving in new habitat, understanding the fundamental processes that regulate differences in diversity levels has arguably never been as important. A fundamental theory first proposed in 1963 to explain patterns in diversity, the theory of island biogeography (TIB), has been tested numerous times as a framework for predicting the dynamic processes acting on insular populations (MacArthur &
Wilson 1963; MacArthur & Wilson 1967). Key elements of this theory, for example, the species–area relationship (SAR), have become instrumental in the field of conservation for managing fragmented landscapes (Diamond
1975; Diamond et al. 1976; Margules et al. 1982; Whittaker et al. 2005).
Use of the SAR as a starting point and predictive tool for ecological research is frequently undertaken to see whether the expected relationship of increasing area results in an increased number of species being able to reside within that area (MacArthur & Wilson 1963; Simberloff & Abele 1976).
This expected relationship between species richness and habitat area as predicted by the SAR has been hypothesized to not only occur because of increased resources but also because the number of habitats (or habitat heterogeneity) increases, while at the same time a larger population has the flow on effect of reduced extinction rates (MacArthur & Wilson 1963;
Simberloff 1976; Brown & Kodric-Brown 1977; Triantis et al. 2008; Dengler
2009; Goldstein et al. 2014). However, the SAR has remained somewhat equivocal in relation to its underlying processes and application (Lynch & Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions 41
Johnson 1974; Gilbert 1980; Lomolino 2000; Triantis et al. 2008). This is due to two key difficulties with measuring the SAR: (1) habitat size can be challenging to estimate in natural ecosystems; and (2) studies have tended to focus on single-specific taxa (e.g., bats (see Mendenhall et al. 2014) or birds
(see Diamond 1969)) as a surrogate for all biodiversity (Gilbert 1980).
In concert with principles detailed in the TIB, other theories have developed simultaneously including the incorporation of multiple measures of biodiversity such as gamma, beta, and alpha diversity as detailed by
Whittaker (1960). Whittaker (1960) determined the total species diversity in the landscape (gamma diversity) is comprised of: (1) alpha diversity: being the mean species richness which exists within certain sites or habitats within the landscape, and (2) beta diversity: being the differences in species richness or diversity between the different sites or habitats. Together, the TIB and the concepts of alpha and beta diversity can be used to understand the similarities and differences in diversity when comparing insular habitats and the ecological drivers which influence the observed resultant biotic composition (Whittaker 1960; MacArthur & Wilson 1963). The TIB predicts that richness of biodiversity (or alpha diversity) in isolated environs or habitats at the local scale are explained by species turnover as a function of area and through processes of immigration, speciation, and extinction that will eventually reach a dynamic equilibrium of species, because resources and space become saturated (Whittaker 1960; MacArthur & Wilson 1967;
Simberloff & Wilson 1969; Keppel et al. 2010), while beta diversity allows us to compare the differences between species composition between similar
42 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
and different habitat types in a broader landscape or oceanic context
(Whittaker 1960; Anderson et al. 2006).
Since the inception of the TIB, aspects of this theory have been tested numerous times and the original ideas have evolved. For example, Whittaker et al. (2008) proposed the general dynamic model of oceanic island biogeography (GDM) to include processes operating on both geological and evolutionary timescales (Whittaker et al. 2008; Borregaard et al. 2016). The
GDM expands on TIBs original concepts of immigration and extinction by including processes of oceanic island lifecycle (Darwin 1859) and the impact these processes have on island biota both in time and space (Darwin 1859;
Whittaker et al. 2008). The GDM proposes that species richness increases quickly (upon island formation) before reaching saturation (as niche space becomes limited), because of interactions between age (time) and area, while isolation removes certain species from the pool of immigrants
(Whittaker et al. 2008).
Pumice rafts present a unique model system to understand how patterns of biodiversity change over time in insular habitats because habitat size and biodiversity can be measured; and pumice rafts from individual events are formed from the same submarine explosion (Bryan et al. 2012;
Jutzeler et al. 2014). These rafts are floating masses of individual pumice stones and can range in size dependent upon the force of the eruption from a few square kilometres to thousands of square kilometres floating on the surface of the ocean (Bryan 1971; Bryan et al. 2004; Bryan et al. 2012).
Pumice rafts provide the ideal opportunity to test the TIB, in particular the
Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions 43
SAR (with the inclusion of additional biotic and abiotic drivers) as each pumice stone acts as a “mini-island”; whose size (measured using the surface area of individual clasts), age (measured as the length of time (in days) from eruption until stranding on coastlines), and the trajectory path it has taken influence its exposure to different oceanic climatic zones (referred to from now on as climatic zone), which can all be measured as pumice clast ontogeny (see Figure 3.1) (MacArthur & Wilson 1963; MacArthur & Wilson
1967; Whittaker et al. 2008).
Figure 3.1 Conceptual diagram of pumice ontogeny. This conceptual diagram depicts the journey of a pumice clast from (a) The Havre under- water volcano which erupted in July 2012, formed approximately four 44 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
trillion pieces of floating pumice stone (b). This pumice then formed what is known as a pumice raft (c) which was so large it could be seen from space. The raft slowly dispersed over the open ocean driven by winds and currents, and while this occurred marine biota (d) colonised the empty surface of the clasts. Finally (e), pumice is either washed onto the coastlines of islands and continents or sinks due to waterlogging or biofouling.
To test fundamental concepts surrounding the SAR, we investigated three key questions: (1) Do area and age predict epibiont richness or alpha diversity which forms on pumice clasts and does one have a stronger influence? (2) How does the influence of area and age change the resultant biodiversity or alpha diversity forming on pumice clasts that were collected from different climatic zones? and (3) Does pumice rafted community assembly (beta diversity) change for pumice that originated from different eruptions or that took different trajectories? Based on the SAR, we predict that larger pumice stones will carry more species because of increased habitat heterogeneity, lower probabilities of extinction, and increased clast stability in the water column (MacArthur & Wilson 1963; Whittaker et al. 2008;
Bravo et al. 2011; Hart & Marshall 2012). Larger pumice clasts likely facilitate increased rates of immigration because of higher resource availability or just by chance because of a higher “target effect” (MacArthur & Wilson 1967;
Lomolino 1990). Target effect increases the chance of immigration due to size—larger islands or habitats are simply more likely to be “found” by potential colonizers than smaller habitats (Whittaker et al. 2014). Taking elements from the ideas contained in the GDM (i.e., age), we also predict that older pumice clasts are likely to carry more species (Whittaker et al.
2008). As habitat space is small on individual pumice clasts and hence can become saturated at low numbers of species and the amount of time pumice
Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions 45
spends in the ocean is relatively short, for example, when compared to geological or evolutionary time scales (Anderson 1999; Whittaker et al.
2008). We also predict that the trajectory path of the pumice rafts influences strongly the abiotic conditions (e.g., sea surface temperature, island or shallow reef encounters) experienced by the raft and the species pool the raft is exposed to, particularly when differing climatic zones (e.g., temperate, subtropical, and tropical) are traversed, and will thus influence species richness patterns found (Gray 2002; Thiel et al. 2003; Wichmann et al. 2012).
The influence of climatic zones is therefore expected to alter the influence of area and age dependent on climatic zone traversed. Further to this, the multivariate dispersion (or beta diversity) of pumice rafted communities is also expected to vary dependent on climatic zone encountered. As beta diversity is a measure of community similarity or dissimilarity among sampling units that are grouped based on the point of collection (climatic zone), we would expect that clasts of similar area and age from the same climatic zone would be comprised of similar communities (Anderson 2006).
3.3 MATERIAL AND METHODS
3.3.1 Home Reef raft and trajectory Home Reef (referred to from hereon as “Home”), Tonga, erupted from 7 to 16 August 2006 after 22 years of dormancy producing a floating mass of pumice containing approximately 2.5 × 1012 pumice clasts (for more detail of raft trajectory see Bryan et al. 2012). As concluded by Bryan et al. (2012), a conservative estimate of one-third of the pumice raft produced is expected to have reached the Eastern Australian coastline (Bryan et al. 2012).
46 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
3.3.2 Havre Volcano raft and trajectory The Havre Submarine Volcano, located adjacent to the Kermadec
Islands north-east of New Zealand, erupted on July 17, 2012 (For details of the location of Home Reef, Havre Volcano and the Kermadec Arc, please see Appendix A, Figure S1.) (Schiel et al. 1986; Priestley 2012; Wunderman
2012; Jutzeler et al. 2014). The resulting pumice raft containing approximately 3–4 × 1012 pumice clasts began arriving to the eastern
Australian coastline after approximately 8 months (for more details of the raft and its spread (see Priestley 2012; Wunderman 2012; Jutzeler et al. 2014)).
After Bryan et al. (2012), we assume that approximately 1/3 of the Havre pumice raft arrived to the eastern Australian coastline being 1.16 × 1012 pumice clasts.
All pumice clasts arriving to the eastern Australian coastline had been colonized, thus, taking a conservative 1:1 relationship of clast to organism ratio, more than one trillion individuals have been transported via these pumice rafts (Bryan et al. 2012).
3.3.3 Pumice characteristics Pumice is known to contain many small inclusions which trap air, leading to buoyancy and longevity at the surface of the ocean (Thiel & Haye
2006; Bravo et al. 2011). The inclusions cause pumice to have a heterogeneous surface, filled with many vesicles and crevices which increase surface area of individual clasts and further aids colonization by marine biota
(Bravo et al. 2011). (For more information on pumice clast formation and stability please see Appendix B. Supporting Information on pumice characteristics). Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions 47
3.3.4 Sampling design Samples of pumice stone were opportunistically collected from strandlines on beaches and coastlines in various locations (Bryan et al.
2012). Collection of pumice attempted to capture a diverse range of sizes and biodiversity as determined by the collector and what was available in the opportunistic stranding of the pumice clasts (Bryan et al. 2012). (For details of pumice raft collection sites and dates please see Appendix C, Table S1.)
Pumice clasts from the Home and Havre eruptions originated in the tropical and subtropical climatic zones, respectively (Schiel et al. 1986; Cole
2001; Bryan et al. 2012). Pumice clasts collected on coastlines were considered as belonging to one of three climatic zones: subtropical, tropical, and temperate based on the Australian Coastal Biogeographic and Climatic
Zone classification system (Bucher & Saenger 1994). As it was not possible to determine the exact trajectory of the pumice clasts and all of the different climatic zones they may have traversed, we have used their collection point to determine the most influential climatic zone on final species assemblages.
We acknowledge that while this approach does not account for all possible shallow marine ecosystem encounters or sea surface temperature effects, it still provides a good approximation of the oceanic climatic zone pumice spent a majority of its time afloat in.
For each clast, we estimated total habitat area using digital calliper measurements of maximum length and width and calculated the available surface area (or available habitat) using the surface area of a rectangular prism (formula: 2(wl + hl + hw) (where w = width, l = length, h = height)), or sphere (formula: 4πr2 (where r = radius)). We tested for strength of 48 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
correlation between sphere and prism measurements and found correlation values to be greater than 95%. We chose then to use sphere in all further analyses (for details of pumice clast sizes, please see Appendix J, Figure
S2).
The collected samples were stored in cold rooms and analysed as soon as possible but at a maximum of six months after collection. We identified all biota to their lowest level of classification, and where further formal classification could not occur, evident differences between individuals of the same family were undertaken to allow division into functional types, referred to as epibionts (Wahl 1989; Bryan et al. 2012; Martins et al. 2014). For example, worms of family Serpulidae were subdivided into functional types of white, pink, and gray-colored calciferous tubes. The term “epibiont richness” is used in place of species richness for this study as the pumice rafted organisms were not always able to be identified to species level (Bryan et al.
2012). The presence or absence of all biota was recorded for each pumice clast.
3.3.5 Data analyses We developed linear mixed-effects models (MEMs) using R (version
3.1.2; Foundation for Statistical Computing) and the lme4 library (Bates et al.
2015) to investigate the relationship between the response variable of epibiont richness and the fixed effects of: area and age; with a random effect structure of: event, place of collection, and date collected for the climatic zones tropical and subtropical. For samples collected in the temperate zone, the random-effects structure consisted of place of collection and date
Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions 49
collected because pumice was not collected from temperate waters for the
Home event. Due to the different scales for the fixed effects age and area, these were centered prior to modelling using the R (3.1.2) “center” function
(Cade 2015). Once a model was fit, residual plots were inspected for model fit and if the residual plots were reasonable, then it was concluded that the model provided a satisfactory fit to the data. Model comparisons were undertaken with the MuMIN package (Barton 2013). Models were evaluated with the corrected Akaike information criterion (AICc) using the model averaging function (Johnson & Omland 2004), and we considered models within four AICc units to be competing models (Burnham & Anderson 2002).
The AICc evaluation of component models is undertaken in this case due to the unbalanced design of the dataset resulting from this natural experiment
(Burnham & Anderson 2002). Parameter estimates using a random intercept structure from the simplest candidate model, following the principles of parsimony, were then plotted to compare effect sizes using the package coefplot2 (Bolker 2012). We chose a random intercept structure of date collected nested within location code and then within event as multiple collections occurred at the same location on different dates across both
2 2 events. We then generated R c and R m values for each model using the
“lmer” package for each candidate model in order to ascertain how much of the variation was explained by the models both including and excluding the random effect structure (Bates et al. 2015).
Prior to analysis, data from the eruptions of Home and Havre were combined. This was done as a majority of pumice from the Home eruption were from the subtropical climatic zone and no clasts from the temperate 50 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
climatic zone were collected. We ran the MEMs relating to climatic zone of collection by separating the data into each climatic zone, and this was done as using climatic zone as a fixed effect in our analysis resulted in oversaturation of the model.
We then performed tests of the differences and similarities between epibiont community composition, in relation to area, age, climatic zone, and location. Using the Primer 7 software package (version 7.0.10, with add-on:
PERMANOVA+ 1) utilizing the permutational multivariate analysis of variance
(PERMANOVA), pair-wise test and PERMDISP functions (see Appendix D
Table S2, Appendix E Table S3 and Appendix F Table S4) (Anderson 2001;
McArdle & Anderson 2001; Anderson 2006; Clarke & Gorley 2015). For the
PERMDISP analysis, only data from the Havre event were analyzed as there were too few collection points from different climatic zones for the Home event, with a majority from subtropical and only a few from tropical to perform this test (Anderson et al. 2006). Nonmetric multidimensional scaling (nMDS) was used to visualize these differences in assembly (Clarke & Gorley 2015).
Tests were conducted to compare one continuous quantitative covariable: area; and four factors: event (Home vs. Havre), age (early, middle, late), climatic zone (tropical, subtropical, and temperate), and location (nested within event, age, and climatic zone) of different clasts to determine whether epibiont communities differed based on these parameters (see Appendix D
Table S2). Age of the pumice clasts was grouped into early (pumice that arrived in the first 3 months based on first arrivals to the coastlines of continents and islands), middle (pumice that arrived after 3 months but before 11 months), and late arrivals (pumice which arrived after 11 months). Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions 51
The area of pumice clasts was extremely right skewed and hence was transformed to log (base 10) creating a normal distribution (see Appendix J
Figure S2). Quantiles of 0.25, 0.5, and 0.75 were calculated for the distribution of sphere sizes resulting in four size-class groups: a1, a2, a3, and a4 (from smallest to largest) forming a factor we called “area.q” to allow for ease of graphical representation. Averages for each combination of location
× area.q were calculated for the biotic data, and an average of location × area.q for the log (base 10) sphere values was also calculated. This process resulted in effectively treating each combination of location and the associated distribution of size classes of pumice that arrived at this location as a replicate for our study.
Comparisons between averaged log (base 10) sphere as a quantitative covariate, event, age, and climatic zone was conducted using epibiont biota presence/absence data which was averaged by area and location (area.q) and a Bray–Curtis resemblance matrix. This was performed using unrestricted permutation of raw data and number of permutations set to
9999. Initial comparisons yielded several inestimable terms, due to unbalanced properties of the design. These inestimable terms resulted from combinations in the model matrices that yielded cells that simply did not exist due to imbalance in the cell structure in the design, and hence, these terms were removed before further analysis was conducted.
3.4 RESULTS
We recorded more than 116 epibiont groups from 10 phyla after surveying 5,279 pumice clasts from the Havre and Home eruptions collected
52 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
at 29 locations and within three climatic zones (temperate, subtropical, tropical) (see Appendix G Table S5).
3.4.1 Do area and age predict epibiont richness (alpha diversity) and does one have a stronger influence? Model comparisons using combined data for Home and Havre showed that age is the most influential covariate for epibiont richness overall, with model weights between 0.37 and 0.91 in models calculated separately for each climatic zone; area was shown to be the second most influential predictor overall (model weights 0.09–0.32), with the interaction of area × age being the least influential (model weights 0.01–0.30) (see Table 3.1). It should also be noted that the AICc values for models produced for area or age are within four AICc points for subtropical and tropical climatic zones and as such are considered to be equivalent models. While for temperate these models did not fall within four AICc points, they were not considered equivalent. Using the R2 value to assess the component models, we found that a high degree of model variation was explained with our component models which tended to increase with the inclusion of random effects except for the temperate climatic zone (see Figure 3.2).
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Table 3.1 Results of model comparison using Akaike information criterion (AICc) values to identify factors explaining variations in epibiont richness between the pumice clasts within climatic zones using the surface area of a sphere as an estimate for available habitat
54 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
Figure 3.2 Mixed-effects model regression estimates for the combined data of Home and Havre (n = 5,279) events within climatic zones: a) temperate (n = 70), b) subtropical (n = 5,043), and c) tropical (n = 166); showing epibiont richness as a function of the covariates of: age (days since eruption), area (an estimation of available habitat calculated for each individual pumice clast using the surface area of a sphere), and a combined effect of age x area. The error bars displayed in the above figure are the standard error as derived from the coefficient estimates 2 in the model. The R m values indicate the amount of variation explained 2 by the model without the random effects, while the R c values indicate the amount of variation explained by the model with the random effects
Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions 55
3.4.2 How does the influence of area and age change for pumice clasts that were collected from different climatic zones? We found epibiont richness varied depending on: age, climatic zone, and area. For both tropical and subtropical climatic zones, epibiont richness increased with both time and size of the pumice clast (see Figure 3.2). In the temperate zone, the relationship between epibiont richness and time was negative suggesting epibiont richness may be lost over time as pumice drifted into cooler climates, but area had a positive correlation with epibiont richness.
Community composition of pumice rafted biota that was nested within age, event, and climatic zone was found to have a significant interaction
(Pseudo-F = 3.8539, p < 0.0001), while no distinct interaction between climatic zone and age or area was found (see Appendix D Table S2).
Community composition also differed depending on climatic zones (Pseudo-F
= 2.4565, p < 0.006) (see Appendix D Table S2). Visualization of the influence of climatic zone using nMDS to compare the two events shows some differentiation particularly in regard to the Home event where tropical clasts were clearly differentiated from subtropical, this is not as apparent for
Havre and this distinction may in part be due to the low number of collection points in the tropical climatic zone surveyed for the Home event (see Figure
3.3, panel b). The influence of climate on pumice raft community assembly is suspected to be related to the dispersion (beta diversity) of community composition. Tests of climatic zone dispersion were conducted for the Havre event (see Appendix E Table S3) with greatest dispersion found between tropical and temperate climatic zones (t = 3.4288, p < 0.006), followed by
56 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
subtropical and temperate (t = 2.5107, p < 0.02), while subtropical and tropical dispersion (t = 1.4796, p < 0.187) were similar. Assessment of the dominance of epibiont groupings by climatic zone for both Home and Havre
(see Appendix H Table S6) indicates a change in species composition and associated dominance of species as climatic zone was altered.
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Figure 3.3. nMDS of a) age (where e = early, m = middle, and l = late arrivals of pumice clasts to beaches on the east coast of Australia and Pacific Islands), b) climatic zone (where sth = subtropical, t = tropical, and ct = temperate stranding locations), and c) area effect on pumice rafted community composition distinguished by location for two events Home (right-hand cluster) and Havre (left-hand cluster). Note for panel b), the effect of climate is more pronounced for Home with a clear
58 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
distinction between tropical and subtropical. For panel c), note that larger pumice stones are represented by larger circles and warmer colors, while smaller and cooler colored circles indicate smaller pumice clasts, and the effect of area is more distinct for the Home event (right- hand cluster)
3.4.3 Does pumice rafted community assembly (beta diversity) change for pumice that originated from a different eruption and that took a different trajectory? We compared community change between pumice rafts from different origins with trajectories through differing climatic zones to determine whether differences in community composition or beta diversity occurred as a result.
Overwhelmingly, the origin of the pumice raft (Home vs. Havre) is the most important main effect in our results (Pseudo-F = 58.823, p < 0.0001) (see
Appendix D Table S2 and Appendix K Figure S3), followed closely by area
(log_sphere) (Pseudo-F = 28.82, p < 0.0001); the interaction of area and event (log.sphere × event) (Pseudo-F = 6.551, p < 0.0001); the location of collection which is nested within age, event, and climatic zone (Pseudo-F =
3.8539, p < 0.0001); age (Pseudo-F = 3.9378, p < 0.0005); and climatic zone
(Pseudo-F = 2.4565, p < 0.006) (see Appendix D Table S2). While overall a majority of pumice clast epibiont assemblages, regardless of climatic zone or event, were dominated by cyanobacteria, bryozoans, and calcareous algae, there are obvious differences in community structure and species between the two events of Home and Havre (see Appendix I Table S7 and Figure 3.4, panel a). For example, the Home raft contained Halobates spp. eggs (a marine insect), nudibranchs, and crabs, while the Havre event did not. The
Havre event meanwhile contained Megabalanus coccopoma (Darwin, 1854) an invasive acorn barnacle, gray serpulid worms, and two additional functional types of Lepas species that the Home event did not.
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Examination of community composition indicated that pumice clast area was the second most important explanatory factor in our data (Pseudo-F =
28.82, p < 0.0001) (see Appendix D Table S2). Visualization of this effect using an nMDS analyses shows most clearly the effect of pumice clast size for the Home event with larger clasts having different community composition; this same relationship between community composition and clast size is not as clear in the Havre event (see Figure 3.3, panel c).
Epibiont community composition was analyzed for the combined datasets of Home and Havre and was noted to change dependent upon the age of the pumice clasts (see Figure 3.4, panel b) with later arrivals being dominated by acorn barnacles. Middle arrivals were dominated by crabs and anemones, while early arrivals had a fairly even spread of community diversity indicating that through time diversity changed and increased. This change in diversity is reflected in the pair-wise tests conducted for the events separately, for the Havre event the largest difference in community composition was found between the early and late arrivals (t = 2.1523, p <
0.0001, see Appendix F Table S4). For the Home event, this trend differed with the largest difference in community composition being between late and middle arrivals (t = 2.7911, p < 0.0001). Overall (both events combined) area had the strongest interactive effect with event (Pseudo-F = 6.551, p <
0.0001) closely followed by the location of pumice clast arrival, which was nested in age, event, and climatic zone (Pseudo-F = 3.8539, p < 0.0001)
(see Appendix D Table S2). Visualization of the effect of age (see Figure 3.3) shows that while age has an effect, this is also affected by the climatic zone encountered. For example, when examining the Home event, tropical clasts 60 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
while being “young” in age had significantly different biota to other climatic zones.
Figure 3.4. Percent dominance of different epibiont groupings a) by event (Home, n = 4,547*) (Bryan et al., 2012) versus (Havre, n = 403) and b) stage of pumice clast arrival for the combined data of Home and Havre): early (n = 265), middle (n = 3,944) and late (n = 741). *Note: A reduced number of clasts was analyzed to produce these graphs for the Home event as species had to be aligned and combined between the two datasets. As there was a significant time lapse between collections and also different authors, some data were excluded due to the inability of ensuring the correct species were aligned in both datasets
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3.5 DISCUSSION
In this study, we tested the SAR and elements of the GDM (i.e., age) on thousands of floating pseudo-islands (i.e., floating pumice clasts) having the same substrate composition that were created on the same day and location for the respective volcanic eruptions (Whittaker et al. 2008; Bryan et al.
2012). Overall, we found evidence in support of the SAR and other abiotic drivers (i.e., age and climatic zone) that larger and older pumice clasts had higher epibiont richness (MacArthur & Wilson 1963; Whittaker et al. 2008), while the influence of raft trajectory through different climatic zones caused changes in species assembly likely because of differences in the exposure of rafts to biota and climatic conditions such as water temperature (Thiel &
Haye 2006). While age and area were found to correlate positively with species richness, the influence of abiotic conditions such as temperature that limit many marine species distributions and increase the dominance of others should be considered when assessing the processes that explain distributions and richness of biota in isolated (see, e.g., Wichmann et al.
2012).
3.5.1 Do area and age predict epibiont richness and does one have a stronger influence? Older pumice clasts and those with a larger surface area were found to have higher epibiont richness when data from both Home and Havre volcanic eruptions were considered (MacArthur & Wilson 1963; Whittaker et al. 2008).
Larger habitat areas were also found to support increased species diversity in the plastic rafted communities of the Northern Pacific Ocean, attributing
62 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
this to larger objects having greater stability in the water column in addition to simply increased habitat area (Goldstein et al. 2014).
3.5.2 How does the influence of area and age change for pumice clasts that were collected from different climatic zones? We found that both subtropical and tropical rafts had strong positive relationships between epibiont richness and age and area, while epibiont richness on temperate rafts showed a positive relationship with area with age becoming negative. When we compared the community assembly forming on pumice clasts of different age, size, and climatic zone, we found that area had the strongest influence on final community assembly followed by age and climatic zone. Unsurprisingly, the effect of combining these factors showed larger, older clasts from the same event and clasts which remained in the same climatic zone for longer periods, collected at the same time from the same location had epibiont communities that differed the most from other samples. Other studies have found that time spent under certain abiotic conditions (e.g., rafting with changes of water temperature relating to season and latitude) affects the number and types of organisms available from the species pool to colonize and subsequently survive on the surface of floating or immersed objects (Osman 1978; Anderson 1999; Wichmann et al. 2012).
Species assembly of pumice clasts was most influenced by the pumice origin (Home vs. Havre) of the pumice clasts, followed by area and climatic zone. Pumice rafted communities (regardless of trajectory or age) were dominated by marine fouling communities including cyanobacteria, bryozoans, and calcareous algae which occurred fairly evenly regardless of time passing. Other biota increased in the middle to late time periods
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including anemones and acorn barnacles, while crabs and a functional type of goose barnacle occurred in the middle time period, and while M. coccopoma occurred only in the late stages and the climatic zone temperate.
These differences may also be attributed to the origin of the pumice (Home vs. Havre) with the two different events having overwhelmingly different species present. Differences occurred between the three climatic zones such as the types of acorn barnacles observed increased for temperate clasts, while the presence of corals increased on tropical and subtropical clasts compared to temperate. Community composition or beta diversity differed between clasts from the Havre event with differing climatic zones collected, with the largest differences in community assembly being found between tropical and temperate, followed by subtropical and temperate. These differences were noted to be due to the dispersion of the diversity present on the clasts; for example, temperate clasts were significantly different from both tropical and subtropical communities in terms of their beta diversity, while we had no evidence for a difference between tropical and subtropical clasts
(Anderson 2006). This observation could be attributed to the different abilities of biota to survive in warmer or cooler water. Species richness of soft sediment dwelling invertebrates is known to decrease from the subtropics to the Arctic, but in the Southern Hemisphere where biodiversity hotspots frequently occur in cooler water as latitude increases, these same trends have been found not to hold at all spatial scales (Gray 2002). Further to this observation, a study that mapped global distribution of species inhabiting coral reefs found a cline from the tropics to the poles for corals, molluscs, reef fish, and lobsters, providing evidence that a biological threshold for reef-
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dwelling organisms comes into effect as water becomes cooler (Roberts et al. 2002). At the same time, we acknowledge that the reduced number of clasts collected for both tropical and temperate climatic zones may have caused some of the observed results.
3.5.3 Does pumice rafted community assembly change for pumice that originated from a different eruption and that took a different trajectory? Our results also suggest that raft trajectory into different climatic zones may cause a die-off and change in community assembly. Our finding that species are lost through time as pumice enters cooler waters indicates that water temperature change as a result of either season or latitude can cause a change in the numbers and types of epibionts able to colonize and survive on pumice rafted at different times of the year (a seasonality effect) and to different latitudes (a climatic zone effect) which are both influenced by the underlying local species pool (Anderson et al. 2006; Thiel & Haye 2006;
Mayfield & Levine 2010; Wichmann et al. 2012). This result is supported in similar studies whereby recruitment onto submerged habitats of different sizes in one location was affected by the time of year (season) and the size of the available habitat space (see Osman 1978; Anderson & Underwood
1994; Anderson 1999). Temperature can directly influence the reproduction of certain marine epibionts as recruitment by different species has been observed to occur at different times of the year (see Osman 1978; Anderson
& Underwood 1994; Anderson 1999), while habitat size affected the stability and niche space of the experimental habitats with larger habitats recruiting higher species diversity (Osman 1978). Even relatively small changes in latitude, for example, from north to south of a coastline have been shown to Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions 65
cause shifts in community composition (due to shifts from warmer to cooler waters) (see Wichmann et al. 2012) restrictions in the presence of rafting biota at different latitudes regardless of the presence of suitable rafting substrate (see Thiel et al. 2003; Thiel & Haye 2006). In addition to the effect of temperature, it is also possible that clasts collected from the temperate climatic zone had fewer shallow reef or island encounters on their voyage, and hence, species were lost due to reduced levels of recolonization from source populations (Brown & Kodric-Brown 1977). For example, Brown and
Kodric-Brown (1977) found that extinctions of invertebrates on thistle plants were related to distances to source populations (i.e., isolation), and hence, recolonization of species already present on plants from proximal sources saved some populations from potential extinctions resulting in what they term the “rescue effect.”
We also found Havre pumice that came ashore in temperate water, had subtropical species recruitment (e.g., corals), which while being present may have ceased growth and died as rafts dispersed into cooler water, while other species, for example, acorn barnacles increased in dominance and overgrew other epibionts under these conditions. In addition, several species found on the Havre pumice have only been recorded as present in warmer waters of tropical and subtropical climes but for the first time were documented washing up in the temperate water of Tasmania these included two species of pearl-oyster (Pinctada margaritifera and Pinctada sugillata) and the gastropod (Litiopa limnophysa) (as found by Grove 2014) and the corals
Porites lobata and an Acropora spp. as found in examination of Havre pumice from Tasmania examined in this study (Veron & Stafford-Smith 66 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
2000). Although these animals were dead upon collection and it would be difficult to know whether they died due to desiccation upon pumice stranding on the beach or due to the cooler temperature of the waters encountered, this information supports the trend that we have observed in the data of a change in assembly as pumice drifted further south and a die-off in species resulting in a negative relationship between age and epibiont richness. Also found in Havre temperate pumice was the invasive species of acorn barnacle
M. coccopoma, a native of the tropical eastern Pacific (Yamaguchi et al.
2009). This species is already recorded as present in Australia and possibly arrived initially via shipping, although in Tasmania records indicate presence on the hull of a ship and not an established population (Yamaguchi et al.
2009). The presence of M. coccopoma highlights the importance of studying and further understanding the phenomenon of pumice rafting. Many introductions of exotic species have been attributed to shipping as the main source of recruits, and however, other rafting substrates such as pumice and plastic are proving to be significant contributors to marine biota transportation due to their volume and persistence in the water column (Bryan et al. 2012;
Goldstein et al. 2014). M. coccopoma has already spread to Brazil, Europe,
Japan, and California, providing evidence of its ability to colonize, reproduce, and spread in new habitats after transportation is a significant concern for managers of shallow marine ecosystems in Australia (Yamaguchi et al.
2009).
We cannot be certain as to whether sessile pumice rafted biota such as corals, bryozoans, and barnacles from the Home and Havre rafts would then colonize habitats when they arrive on coastlines; however, studies have Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions 67
shown that colonization is possible (Jokiel 1989, 1992). Three possible mechanisms of coral rafted on pumice to colonize a new habitat are proposed (after Jokiel 1989): (1) the chance sinking of overladen pumice into shallow water allowing fouling organisms to overgrow (see Tunnicliffe 1981) for evidence of loose coral fragments being overgrown and secured by calciferous reef organisms); (2) dislodgement via scraping of pumice fragments on tidal reef flats via wave action (see Tunnicliffe 1981; Smith &
Hughes 1999); and (3) mature colonies reproducing at sea either asexually
(via budding, parthenogenesis, or polyp bailout) or sexually by eggs that are fertilized either before or after being released by the parent (see Sammarco
1982; Stoddart 1983; Hoeksema et al. 2011; Combosch & Vollmer 2013), which can be possible even if only one coral colony is present as many corals are self-fertile (Sammarco 1982; Stoddart 1983; Jokiel 1989;
Hoeksema et al. 2011; Combosch & Vollmer 2013). While the temperate waters of Tasmania are too cold presently for corals, it is possible that as sea temperatures rise the expansion of coral species into new climatic zones could occur. The spread and contraction of coral species into new habitats both now and historically has recently been documented in several studies
(see Fenner & Banks 2004; Precht & Aronson 2004; Greenstein & Pandolfi
2008; Hoeksema et al. 2011; Mantelatto et al. 2011; Yamano et al. 2011), which suggests that coral rafted on pumice may have an opportunity to escape unfavorable conditions (e.g., hotter water) via rafting as global temperatures rise (Greenstein & Pandolfi 2008; Hoeksema et al. 2011).
The results of this study were found despite an inability to identify all of the biota inhabiting the pumice clasts, and the departure of motile biota (such 68 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
as crabs, bristle worms, gastropods, and nudibranchs), which disembarked pumice clasts upon stranding and were often not captured during collection of pumice samples. The departure of motile biota will have reduced the effect of area on species richness, and as a result, we think our finding of a positive relationship between area and epibiont richness would have been even stronger should we have been able to capture this biota in our data as part of the study. In addition, we acknowledge that there is no way of knowing if clasts from the “older” collections in the temperate zone were less diverse in species assemblage due to potential sinking of more diverse assemblages; however, as older clasts from tropical and subtropical were quite diverse, we assume we captured range of diversity from each climatic zone and stage of arrival. Despite these limitations, we were able to demonstrate the importance of pumice rafting as a mass dispersal agent of marine biodiversity throughout the Pacific Ocean and beyond (Nikula et al. 2010; Bryan et al.
2012). For example, certain species of coral, are found within reefs throughout the Pacific Ocean and on the surface of pumice clasts. These species are documented to disperse via zooplankton and spawning with maximum dispersal limits ranging from a few meters to several hundred kilometres (Jokiel 1989; Shanks et al. 2003; Thiel & Haye 2006). Despite these dispersal limitations the same species of coral are found in reefs separated by thousands of kilometres throughout the Pacific Ocean (Jokiel
1989; Shanks et al. 2003; Thiel & Haye 2006). A similar observation was made (see Nikula et al. 2010) whereby a genetic study of nondispersive crustaceans which are known kelp rafters were sampled throughout the islands of the subantarctic. These crustaceans raft on kelp throughout the
Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions 69
circumpolar currents of the subantarctic and were found to come from the same haplotype providing evidence that kelp rafting contributes substantially to the composition of shallow marine communities in the subantarctic despite being separated by hundreds to thousands of kilometres (Nikula et al. 2010).
Overall pumice raft events have provided strong evidence in support of the key tenets within TIB, namely the SAR and the inclusion of additional abiotic and biotic drivers in models of species richness for example the GDM which predicts that age and area will be the major driving force in predicting biodiversity in insular habitats (MacArthur & Wilson 1963; MacArthur &
Wilson 1967; Whittaker et al. 2008). This study contains a line of evidence that these theories have continued relevance to the understanding of ecological communities and the abiotic and biotic processes which shape them (MacArthur & Wilson 1967; Whittaker et al. 2008; Keppel et al. 2010).
3.6 ACKNOWLEDGEMENTS
We thank Dr Simon Groves (Tasmanian Museum and Art Gallery);
Andrew Hosie (Museum of Western Australia); Dr John Healy (Queensland
Museum); Dr Robyn Cumming (Museum of Tropical Queensland); Dr Pat
Hutchings (Australian Museum, Sydney); Dr Elena Kupriyanova (Australian
Museum, Sydney) for their invaluable assistance in identifying the pumice rafted marine biota. We also thank Professor Marti J Anderson (Massey
University, New Zealand) who provided invaluable assistance and advice with statistical analysis.
70 Chapter 3: Journal article: Testing the Theory of Island Biogeography and subsequent evolutions
Chapter 4: Biotic drivers and a
foundation species effect
explain community assembly
on floating pumice
ecosystems
4.1 ABSTRACT
Despite an ongoing interest in the field of community ecology to understand how abiotic and biotic forces shape communities across spatial scales. Currently, within the marine context, there are few studies that examine the links between functional traits, change in abiotic environmental conditions such as temperature or available habitat, and biotic interactions such as competition or facilitation across spatial scales. Floating pumice rafts formed within the Pacific Ocean, provide a unique opportunity to study the different effects of abiotic and biotic factors on the formation of marine communities. I examined the ecological communities which formed on floating pumice rafts, produced following the 2012 eruption of the underwater
Havre Volcano, located north-east of New Zealand. Entire marine communities which formed on the surface of 405 pumice clasts collected from 28 locations within three climatic zones (tropical, subtropical and Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 71
temperate) were sampled. Here, I ask, how the functional traits of pumice rafted marine communities changed because of changes in abiotic and biotic conditions. Abiotic and biotic factors I investigated included: increases and decreases in habitat area, measured as the surface area of individual pumice clasts. Habitat age, which was calculated from the date of pumice formation to stranding on coastlines. Differing environmental conditions as pumice floated into different latitudes and climatic zones and finally, the characterisation of biotic interactions within the community such as competition and facilitation. I found that both older and larger pumice stones contained increased functional richness, whereas larger pumice clasts contained increased abundances within trait groupings. These effects varied depending on the climatic zone of collection, indicating different temperatures and change in underlying species pools as pumice trajectory altered. My results also suggest that biotic interactions such as a foundation species effect, are important drivers of pumice rafted community ecology. As strong evidence was found for the presence of a foundation species effect within the community because of the presence of barnacles of the genus Lepas.
4.2 INTRODUCTION
Functional traits can describe both an organism’s (biotic) response to, and effect, on the (abiotic) environment (Suding et al. 2008). Investigation of response traits helps in understanding the biotic response to abiotic conditions (Suding et al. 2008). Effect traits in this context are an example of how the biotic (organismal) influence on the abiotic environment and resultant ecosystem processes can be examined (Suding et al. 2008).
72 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Overall, functional traits comprise the comparable and measurable components of biota that enhance fitness or competitive performance and, thus, govern where biota can persist (McGill et al. 2006; Cadotte et al. 2011).
There are few specific examples in the literature of the empirical testing of marine organism response and effect traits. However, see Solan et al.
(2004) for an example of marine benthic invertebrate effect on the ecosystem function of bioturbation, Griffin et al. (2009) for an examination of macro- algae functional trait diversity effect on ecosystem productivity, and Frid and
Caswell (2016) for a deep time examination of benthic community traits and associated ecosystem functions. Examples of a marine biota’s response to the environment (i.e. response traits) might include biochemical processes, such as being able to photosynthesise or forming symbiotic relationships; methods of feeding, such as extracting food from the water column via filter feeding; and reproductive processes, which aid dispersal such as producing motile larvae or, when dispersal is not possible, the ability to reproduce asexually (in the absence of a suitable mate) (Cadotte et al. 2011). These examples are considered response traits because they are measurable features of biota that have evolved in response to environmental conditions allowing organisms to persist under these conditions (Suding et al. 2008;
Cadotte et al. 2011).
Effect traits may include feeding behaviours, such as removal of sediment from the water column via filter feeding, which allows subsequent colonisation by more sensitive biota into the immediate area (Hart & Marshall
2012). Another effect trait is the initial colonisation of habitat by primary
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 73
producers, which allows secondary consumers (e.g. grazers) to colonise because of the available food source (Funk et al. 2008; Suding et al. 2008;
Hart & Marshall 2012; Alexander et al. 2016). These characteristics are, in turn, defined as effect traits because the biota that possess them cause an effect (or change) within the environment that they inhabit and, as a result, alter the functioning of the ecosystem (Solan et al. 2004; Suding et al. 2008).
Abiotic (environmental) filters act as overarching filters to community assembly in specific locations and favour biota with traits that suit the conditions (Heino 2008). Abiotic filters can include, for example, available habitat, geographical boundaries (e.g. deep swathes of open ocean), and latitudinal temperature gradients. These abiotic components then work simultaneously as macro-scale filters that can affect the survival of an organism on a location-by-location basis (Keddy 1992; Stachowicz et al.
1999; Kraft et al. 2007; Wichmann et al. 2012). If environmental filters act more strongly as determinants of successful colonisers, organisms will show high trait similarity (referred to as under-dispersed) than expected by chance alone (Funk et al. 2008; Laughlin et al. 2012). Conversely, if biotic filters
(interactions between living organisms) act more strongly as determinants of successful colonisers, community traits will have higher richness being considered more dissimilar than expected by chance alone (referred to as over-dispersed) (Funk et al. 2008; Cadotte et al. 2011; Laughlin et al. 2012;
Cadotte et al. 2015).
Following dispersal, the colonising organisms may encounter competition with neighbouring organisms or be aided (facilitated) by the
74 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
presence of other biota (Chesson 2000; Mayfield & Levine 2010; Gil & Pfaller
2016). Competitive interactions fall into two broad categories: i) interference competition, whereby more dominant biota drive-off or dominate smaller weaker biota via behaviours or chemical defences that are not related to resource use, and ii) exploitation competition, whereby biota must compete for a limited resource (e.g. food or habitat space) (Crawley et al. 1986).
Following this line of reasoning, it can be hypothesised that new arrivals into a community either do this ‘from above’, in that biota are larger and rely on interference competition, or ‘from below’, in that the biota are smaller and are more efficient at resource uptake and conversion into growth, which results in exploitation competition (Crawley et al. 1986; Hart & Marshall 2012).
Recent research into benthic marine communities has found that some species can act as foundations that facilitate the recruitment of other less dominant species, which results in colonisation from below; examples are some species of Bryozoa (see Hart & Marshall 2013) and Lepas barnacles
(stalked barnacles of the genus Lepas) (see Gil & Pfaller 2016). Foundation species are biota that often, but not always, colonise a habitat first because of their traits (i.e. response traits) that confer an ability to survive the often harsh initial conditions (e.g. increased irradiance, water currents or salinity) of bare habitat. As they grow, these foundation species ameliorate the environmental conditions (an example of effect traits), which allows other more sensitive species to colonise successfully or simply allows more of the same species to colonise and survive (Bertness & Callaway 1994; Solan et al. 2004; Suding et al. 2008). For example, in the intertidal zone, high recruitment of the acorn barnacle Semibalanus balanoides correlated with Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 75
increased survival of other recruits of this species; this association was attributed to increased shading and reduction of heat stress in neighbouring barnacles (Bertness 1989). In another example, in just one growing season, reduced fiddler crab density in salt marshes led to decreased aboveground growth of the grass Spartina alterniflora (Bertness 1985).
A recent study of the plastic-rafted communities of the Pacific showed that Lepas barnacles facilitated colonisation by some species but were in direct competition with other sessile species, depending on the size of the habitat (Gil & Pfaller 2016). Lepas barnacles are thought to facilitate colonisation by providing increased structural complexity, provision of safe sites (via crevices and reduced water flow) and increased stability of these objects (Gil & Pfaller 2016). At the same time, as habitat availability decreases, Lepas barnacles begin to compete with other sessile biota for available habitat space (Gil & Pfaller 2016). This competitive effect was lessened on larger plastic objects but intensified on smaller objects where space was limited (Gil & Pfaller 2016).
A foundation species of bryozoan (i.e. Watersipora species) has also been found to facilitate its own colonisation and that of other bryozoans (e.g.
Bugula species) because of a reduction in sediment loads (an effect trait) through the creation of feeding flows by colonies of Watersipora (Stachowicz
& Byrnes 2006; Hart & Marshall 2012; Hart & Marshall 2013). Species with low space resource requirements, in particular, can take advantage of the conditions created by foundation species, and colonise small habitat gaps in benthic marine communities and complete their lifecycle within these smaller
76 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
habitat spaces (Hart & Marshall 2012). This illustrates the advantage of from below exploitation competition (i.e. the efficient use of limited habitat as a resource) (Hart & Marshall 2012). Experimental colonisation of these low space requirement species into artificially created larger habitat gaps resulted in increased mortality, which indicates that both from above and from below strategies can be successful within benthic communities (Hart & Marshall
2012)
Within shallow benthic marine invertebrate communities, one of the most important resources for determining final community structure is the proportional availability of vertical habitat (exposed regularly to solar radiation and commonly dominated by algae, or corals) and horizontal habitat
(meaning face down and most likely to remain immersed or shaded at all times) (Saunders & Connell 2001; Irving & Connell 2002b; Miller & Etter
2008; Hart & Marshall 2013). Other factors include forms of environmental stress such as water flow, trophic removal (e.g. via predation or grazing), sedimentation and light availability (Irving & Connell 2002b; Irving & Connell
2002a; Miller & Etter 2008). In benthic communities, suitable habitat for colonisation is often the greatest limitation, and it therefore assumed that from above interference competition dominates these communities
(Stachowicz et al. 1999; Hart & Marshall 2012). Although an organism’s ability to compete for space, usually via from above mechanisms (e.g. a larger species can overgrow a smaller species) in benthic communities is important to a species’ success, the ability of organisms to occupy small habitat gaps via from below mechanisms is also important (see Hart et al.
2012). Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 77
This study investigated how the trait space occupied by the community of species which colonised the Havre pumice rafts changed through time, within space and depending on foundation species effects and measures of pumice raft isolation. Pumice rafts formed from the eruption of submarine volcanoes provide a unique opportunity to study the assembly of shallow marine ecosystem communities and the traits they are comprised of (Bryan et al. 2012; Velasquez et al. 2018). By surveying the trait space occupied by the community of species which formed on pumice clasts that were stranded on the coastline of Australia and islands throughout the Pacific, I specifically addressed the following questions:
1) Does the trait space occupied by pumice rafted biota change over time (age) and space (Crawley et al. 1986; Hart & Marshall 2012)?
2) Does change in climatic zone (a measure of relative isolation between pumice rafts) cause a resultant change in functional richness of the pumice rafted community?
3) Does a foundation species effect, such as that observed with Lepas barnacles, also occur in pumice rafted communities (see Gil & Pfaller 2016)?
Based on past studies, I expect to find that the separate predictive effects of older and also larger clasts will allow a community to form that has increased trait richness. More specifically, I expect the community to exhibit an increased richness of feeding trait modalities ranging from primary producers to predators and richness of reproductive modalities, from spawners, asexual strategies and sexual reproduction. I also expect that the interaction of area age to be a weak predictor (Velasquez et al. 2018).
78 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Initial colonists may alter conditions (an effect trait) such that resource availability facilitates opportunities for other species to colonise through time or age (Levine 1999; Hart & Marshall 2013). Therefore, I predict that pumice clasts will exhibit a foundation species effect based on presence of Lepas barnacles (measured as both counts and cover) resulting in increases in the richness of functional traits found on pumice clasts (Gil & Pfaller 2016). I also expect this effect may change when examining differences between sessile and motile biota because Lepas barnacles comprise a sessile foundation species and may be a habitat resource competitor of other pumice rafted sessile biota (Gil & Pfaller 2016).
4.3 MATERIALS AND METHODS
4.3.1 Havre Volcano raft size & trajectory The Havre Submarine Volcano, located adjacent to the Kermadec
Islands north-east of New Zealand, erupted on 17 July 2012 (Schiel et al.
1986; Priestley 2012; Wunderman 2012; Jutzeler et al. 2014). The resulting pumice raft containing approximately 3–4 1012 pumice clasts began arriving on the eastern Australian coastline after about 8 months (for more details of the raft and its spread see Priestley 2012; Wunderman 2012; Jutzeler et al.
2014). After Bryan et al., (2012) I assume that approximately one-third of the
Havre pumice raft arrived on the eastern Australian coastline and comprised
1.16 1012 pumice clasts.
4.3.2 Characteristics of pumice rafts Pumice rafts formed from the eruption of submarine volcanoes provide a unique opportunity to study the assembly of shallow marine ecosystem
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 79
communities and their traits (Bryan et al. 2012). Pumice rafts are created from a single eruption at the same time and place and are initially devoid of species. Accumulation of species through time, from eruption to final stranding on coastlines, is considered to represent the ‘age’ of the individual clasts. As they voyage through the open ocean, pumice rafts are exposed to differing rates of propagule pressure via island and shallow reef encounters
(a measure of pumice raft isolation) and abiotic conditions (e.g. water temperature).
4.3.3 Sampling design Samples of pumice clasts were opportunistically collected from strandlines on beaches and coastlines in various locations (Velasquez et al.
2018). The collection of pumice attempted to capture a diverse range of sizes and biodiversity, as determined by the collector, and what was available in the opportunistic stranding of the pumice clasts (Velasquez et al. 2018).
Pumice clasts for the Havre pumice raft are considered to have originated in the subtropical climatic zone (Schiel et al. 1986; Cole 2001).
Pumice clasts collected on coastlines were considered as belonging to one of three climatic zones—subtropical, tropical and temperate—based on the
Australian coastal biogeographic and climatic zone classification system
(Bucher & Saenger 1994). As it was not possible to determine the exact trajectory of the pumice clasts and all of the different climatic zones they may have traversed I have used their collection point to determine the most influential climatic zone on final species assemblages. I acknowledge that, although this approach does not account for all possible shallow marine
80 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
ecosystem encounters or sea surface temperature effects, it still provides an approximation of the oceanic climatic zone that each pumice spent most of its time afloat in. Despite my best efforts, 50% of the samples for this study were collected from the subtropical climatic zone.
For each clast, I estimated total habitat area available on each clast using digital calliper measurements of maximum length and width in millimetres, and then calculated the available surface area (or available habitat) using the surface area of a rectangular prism using the following formula: 2(w l + h l + h w) where w = width, l = length, and h = height, or for a sphere 4r2 where r = radius. I analysed the strength of the correlations between sphere and prism measurements and found the coefficient of determination to be greater than 95%. I subsequently chose the sphere to use as the estimate of area in all analyses. For the purposes of this study, references to area or habitat area from herein mean the entire surface area of each individual measured pumice clast.
4.3.4 Functional traits A database of functional traits was compiled from published literature and from discussions with experts from the Queensland Museum, Tasmanian
Museum and Art Gallery, and Museum of Western Australia. The functional traits for the identified epibionts were divided into two main groups: feeding guilds and associated modalities, and reproductive guilds and associated modalities (Table 4.1, Appendix L Tables S8 and S9). Trait richness examined the diversity of traits per pumice clast, while abundance of traits forming on individual pumice clasts was determined from the number of
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 81
organisms that fell into each trait modality category. I also divided pumice rafted biota into two additional functional trait categories based on dominant life history mode of the adult life-form being i) motile or able to move freely and ii) sedentary or requiring a solid-substrate to colonise and grow.
Table 4.1. Pumice rafted functional traits and their modalities
Trait grouping Modality Functional interpretation Feeding guild carnivore, herbivore, The richness of feeding habits implies the omnivore, filter feeder, complexity of trophic webs forming within floating grazer, scavenger, predator, pumice communities. As well as the differences parasitic, borer, or changes in resource acquisition between photosynthetic, algal communities that arrived in different climatic symbiont zones due to different trajectories. Reproductive asexual, sexual, dioecious, The richness of reproductive modes guild protandrous hermaphrodite, demonstrates the difficulties biota experience in simultaneous hermaphrodite, producing viable offspring in each generation. For spawner, brooder, example, asexual and hermaphroditic fragmenter, motile larvae, reproductive modalities indicate that organisms teleplanic larvae are dispersal limited or sedentary in life-form and have reduced chances of sexual reproduction in each generation. The ability to reproduce asexually also indicates whether it is likely that pumice rafted biota could reach reproductive maturity and reproduce while floating on the open ocean before stranding on coastlines. Increased egg care in brooding organisms can be indicative of increased survival and hatching success. Reproductive modalities which allow dispersal such as spawning or motile larvae also indicate which biota, particularly sedentary biota, could disperse propagules whilst rafting on pumice or should the timing be right, upon stranding. Dominant motile or sedentary Dominant adult life-form indicates whether hard- adult life-form substrata habitat is essential for settlement and growth to maturity and reproductive life stages. It is also indicative of different community competitive effects such as the competition for ‘space’ within a habitat.
4.3.5 Data analyses We collated data for each epibiont on their reproductive and feeding traits and associated modalities and also recorded whether each epibiont was motile or sedentry in their adult life-form (Table 4.1). All traits were coded as nominal variables (i.e. being a ‘1’ or ‘0’) and summed for each pumice clast. This data was then analysed to determine whether the total
82 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
number of traits on each pumice clast was most influenced by biotic factors
(e.g. niche space, foundation species effect, or competition between epibionts) or abiotic factors (e.g. age or area). I developed linear mixed- effects models (MEMs) using R (version 3.1.2; Foundation for Statistical
Computing) and the lme4 package (Bates et al. 2015) to investigate the response variables comprising all trait modalities combined and separate categories of summed feeding trait modalities, summed reproductive trait modalities, motile species and non-motile species, and an analysis of each separate feeding or reproductive trait modality (Table 4.1, Appendix L Tables
S8 and S9 for a list of traits analysed). Both the individual and interactive effects were assessed using the fixed effects of: i) area, ii) age, iii) age area, iv) Lepas barnacle cover. Random effects consisted of place of collection and date collected.
The data were analysed to determine whether a foundation species effect was present in the pumice rafted community by testing whether habitat area, age or Lepas barnacle abundance (measured in terms of counts and cover) affected the functional richness of pumice rafted biota (Gil & Pfaller
2016). The Lepas barnacle counts and cover were excluded from the ‘sessile biota’ counts and cover used in the developed models to ensure that the presence of Lepas barnacles did not confound the analysis. Because of the different scales for the fixed effects of age and area, these were centred before running models that contained both of these effects and were modelled using the R (3.1.2) ‘centre’ function (Cade 2015).
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 83
I compared model fit using the MuMIN package (Barton 2013). Models were evaluated using corrected Akaike information criterion (AICc) (Lafferty &
Kuris 1996), and I considered models within four AICc units to be competing models (Burnham & Anderson 2002). Parameter estimates using a random intercept structure from the simplest ‘best fit’ candidate models, following the principles of parsimony, were then plotted to compare effect sizes using the package coefplot2 (Bates et al. 2015). I chose a random intercept structure of date collected nested within location code because multiple collections often occurred at the same location but on different dates. If a normal distribution did not provide the best fit, I used the presence or absence data and created generalised linear mixed-effects models with binomial distributions with the fixed, random and conversion principles described above (Bates et al. 2015).
Based on plots of the model residuals and quantiles (for the normally distributed models), it was decided that all models included in this study were reasonable descriptors of the data and that the quantile plots fit most of the models. I could not run models for all of the different feeding and reproductive trait modalities in the tropical climatic zone due to data deficiency for the following trait modalities photosynthetic, asexual and motile larvae.
I then analysed epibiont community trait composition, which formed for the Havre eruption in relation to area, age, climatic zone and location. To do this, I used the Primer 7 software package (version 7.0.10, with add on:
PERMANOVA+ 1) using the permutational multivariate analysis of variance
(PERMANOVA), pair-wise test and PERMDISP functions (Anderson 2001;
McArdle & Anderson 2001; Anderson et al. 2006; Clarke & Gorley 2015). 84 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Non-metric multi-dimensional scaling (nMDS) was used to visualise these differences in assembly (Clarke & Gorley 2015).
The data were analysed to compare the one continuous quantitative co- variable area and the three factors age (early, middle, late), climatic zone
(tropical, subtropical and temperate) and location (nested within event, age and climatic zone) of different clasts to determine whether epibiont communities differed according to these parameters. To complete this analysis, pumice clast ages were grouped into early (pumice that arrived in the first three months based on the timing of the first arrivals to the coastlines of continents and islands in the Pacific), middle (pumice that arrived after three months but before 11 months) and late arrivals (pumice that arrived after 11 months).
The area of pumice clasts measured as the surface area of a sphere was skewed and hence was log transformed (base 10) to create a normal distribution. Quantiles of 0.25, 0.5 and 0.75 were calculated for the distribution of sphere sizes and resulted in four size–class groups (a1, a2, a3 and a4, from smallest to largest) that were then used as a factor called
‘area.q’ to allow for ease of graphical representation. Averages for each combination of location area.q were calculated for the biotic data and an average of location area.q for the log (base 10) sphere values was also calculated to match for use in further analysis. This effectively treated each combination of location and the associated distribution of size classes as a replicate for the study.
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 85
4.4 RESULTS
Overall, I recorded a total of 11 different feeding functional group modalities and 10 different reproductive functional group modalities (Table
4.1, Appendix L Tables S8 and S9) on the 405 pumice clasts processed from the Havre eruption collected from 28 locations and three climatic zones
(temperate, subtropical and tropical).
4.4.1 Does the trait space occupied by pumice rafted biota change over time (age) and space (Crawley et al. 1986; Hart & Marshall 2012)? Overall trait richness of the pumice clast epibiont communities increased over time and depending on the size of the clasts collected. Trait richness correlated positively with age (model weight 0.6), which was defined as the time elapsed from the date of eruption to pumice clast collection on coastlines, and positively correlated with the size of the pumice clast (model weight 0.4). The interactive effect of age area was the least influential predictor. I found a similar result when I conducted separate analyses for the richness of feeding or reproductive traits, which both increased with age and area of pumice clasts (Figure 4.1 and Table 4.2).
86 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Figure 4.1. Mixed-effects model regression estimates for a) total trait richness; b) reproductive trait richness; and c) feeding trait richness. Note there is little difference between the influence of the factors age and area for feeding and reproductive trait richness. For overall trait richness, age begins to predict the trait richness to a slightly greater extent than area.
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 87
Table 4.2. Results of model comparison using Akaikie information criterion (AICc) values to identify factors explaining variations in functional trait richness. Analyses was conducted for total trait richness, feeding trait richness and reproductive trait richness per pumice clast combined and examined in relation to the fixed effects of age and habitat area. Note all models represented in this table were created using a normal distribution.
Trait modality Effect df logLik AICc Delta Weight Full or reduced model Total trait Age 6 1067 2147 0.0 0.6 richness F area 7 -1067 2147 0.8 0.4 feeding trait age 6 -881 1773 0.0 0.5 richness area 7 -880 1774 0.3 0.5 F age x area 5 -891 1792 18.3 0.0 reproductive age 6 -748 1508 0.0 0.7 trait richness F area 7 -748 1509 1.6 0.3
Age was the most influential predictive variable for separate feeding and reproductive trait richness (Table 4.3) with few exceptions. Where area became more influential than age (e.g. for the feeding modalities of scavengers and parasitic biota), it fell within four AICc points of age and, therefore, the models can be considered equivalent. This trend of age explaining the largest amount of variation in trait richness was consistent for all reproductive trait modalities (Table 4.3). The interactive effect of age area became more influential when examining individual feeding and reproductive trait modality richness but was never more than the individual effects of age and area (Table 4.3).
88 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Table 4.3. Results of model comparison using Akaikie information criterion (AICc) values to identify factors explaining variations between functional trait modalities. Analyses was conducted for individual trait modalities and data combined for climatic zones in relation to the fixed effects of age and habitat area.
Trait modality Effect df logLik AICc Delta Weight Binomial or Full or normal reduced distribution model Carnivore Age 6 -153 319 0.0 0.4 binomial F area 4 156 -319 0.4 0.3 age x 5 -155 320 0.5 0.3 area herbivore null model* binomial F
omnivore age 7 -854 1722 0.0 0.6 normal F area 6 -855 1723 1.3 0.3 age x 5 -858 1726 4.3 0.1 area algal symbiont null model* binomial F filter feeder null model* binomial F grazer null model* binomial F scavenger area 4 -152 311 0.0 0.4 binomial F age 5 -151 312 0.3 0.4 age x 6 -150 313 1.6 0.2 area photosynthetic age 7 -555 1125 0.0 1 normal F area 6 -560 1133 8 0.0 age x 5 -564 1139 13.6 0.0 area predator age 6 -166 345 0.0 0.6 binomial F area 4 -169 347 1.8 0.2 age x 5 -169 347 2.1 0.2 area parasitic area 4 -150 309 0.00 0.4 binomial F age 5 -149 309 0.2 0.4 age x 6 -149 310 1.5 0.2 sphere asexual age 7 -933 1881 0.0 1 normal F area 6 938 -1889 7.7 0.0 sexual age 7 -889 1792 0.0 1 normal F area 6 -894 1801 8.9 0.0 dioecious age 7 -720 1453 0.0 1 normal F protandrous age 6 -196 405 0.0 0.5 binomial F hermaphrodite area 4 -199 406 1.3 0.3
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Trait modality Effect df logLik AICc Delta Weight Binomial or Full or normal reduced distribution model age x 5 -198 406 1.4 0.2 area simultaneous age 5 -167 345 0.0 0.5 binomial F hermaphrodite area 6 -167 346 0.7 0.4 age x 4 -170 347 2.3 0.2 area spawner area 4 -177 363 0.0 0.5 binomial F age 5 -176 363 0.2 0.4 age x 6 -176 365 2.2 0.2 area fragmenter age 7 -642 1298 0.0 1 normal F area 6 -648 1308 9.5 0.0 motile larvae age 7 -796 1607 0.0 0.7 normal F area 6 -798 1609 1.8 0.3 *A null model is where the random effects (location and date of pumice clast collection) explained the data to the same degree as the fixed effects (age and area). Examination of trait abundance on each pumice clast showed that area
(or habitat size) was the most important predictive variable, followed by age, climatic zone and location (Table 4.4). These results are illustrated further using non-metric multidimensional scaling (nMDS) (Figure 4.2), which showed that the effect of area (the strongest predictor) exhibited clustering of pumice stones of similar size. Age also showed some grouping within the graph based on arrival time, although this was shown less clearly than area
(Figure 4.2).
90 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Table 4.4. PERMANOVA test of differences between pumice rafted community trait modality composition abundance formed on pumice collected from different locations, ages, sizes and climatic zones: subtropical (n = 218), tropical (n = 116) and temperate (n = 70).
Comparison of Pseudo-F p Unique permutations location, age, area and climatic zone
Area (log.sphere) 32.4 <0.001 9942
age 5.6 0.01 9955
climatic zone 2.6 0.02 9944
location (age x 2.3 0.01 9925 climaticzone)
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 91
Figure 4.2. nMDS of Havre functional trait richness. a) Area effect on pumice rafted community composition abundance. Larger pumice stones are represented by larger circles and warmer colours, and smaller pumice clasts are represented by smaller and cooler-coloured circles. It is clear from panel a) that larger clasts have increased functional trait richness. b) Pumice clasts are defined by age. e = early, m = middle and l = late arrivals of pumice clasts to beaches on the east coast of Australia and Pacific Islands. c) Pumice is indicated by climatic zone. sth = subtropical, t = tropical and ct = temperate-stranding locations. For panel b), the effect of age was more pronounced for early arrivals, whereas for panel c), the effect of climate is not as well defined. 92 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Analysis of the beta diversity (or dispersion) between pumice clasts with differing ages was also performed. Early and late-arriving pumice rafted communities differed significantly from each other (t = 2.19, p < 0.05), but all other comparisons were not significant (Table 4.5). Similarly, age of pumice clast arrival was examined using pair-wise tests, which showed two significant relationships. The largest difference in pumice rafted trait richness occurred between late and early arrivals (t = 3.26, p < 0.001) followed by late and middle arrivals (t = 2.09, p < 0.02) (Table 4.6).
Table 4.5. PERMDISP analysis of community trait richness and abundance as predicted by the grouped stage of arrival of pumice clasts, into the categories of early, middle and late arrivals. This analysis provides a distance-based test for homogeneity of multivariate dispersions between pumice stones of differing ages (NB: the number of permutations was set to 9999 for all models).
Stage of arrival t value p
Late, early 2.19 0.05
late, middle 1.81 0.10
middle, early 1.00 0.35
Table 4.6. Pair-wise comparison tests of pumice rafted community trait richness by grouped stage of arrival of early, middle and late arrivals.
Stage of arrival t value p Unique permutations
Late, early 3.26 <0.001 9956
late, middle 2.09 0.02 9952
middle, early 1.29 0.20 9892
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 93
4.4.2 Does change in climatic zone (a measure of relative isolation between pumice rafts) cause a resultant change in functional richness of the pumice rafted community? When pumice arrivals were separated into the distinct climatic zones
(temperate, subtropical and tropical), age was again the most influential covariate for total trait richness on each pumice clast (Table 4.7). This analysis also showed that the richness of traits differed depending on the climatic zone where the pumice raft was collected from. For example, pumice collected in the temperate zone showed a negative relationship between trait richness and age, and the combined effects of age area indicating a die-off or change in pumice rafted richness as pumice drifted into temperate water.
Similarly, tropical pumice rafts also showed a negative relationship between age and trait richness, and retention of the positive slope with area and the interacting effects of age area (Figure 4.3). Habitat area retained a positive slope throughout each climatic zone and was consistently the second-most influential predictive variable (Table 4.7 and Figure 4.3). These trends did not vary when analyses were conducted on the separate categories of ‘feeding trait richness’ or ‘reproductive trait richness’ (Figure 4.3). In all cases, the effect of age area was the least influential predictive variable (Table 4.7)
94 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Table 4.7. Results of model comparison using Akaikie information criterion (AICc) values to identify factors explaining variations in functional trait richness. Analyses was conducted for total trait richness per pumice clast within separate climatic zones: temperate (n = 70), subtropical (n = 218) and tropical (n = 116). Note all models conducted for the following table were conducted using a normal distribution.
Climatic zone Effect df logLik AICc Delta Weight Full or reduced models (F or R) Temperate Age 6 -159 332 0.0 0.6 F (n=70) area 7 -159 333 1.4 0.3 age x 5 -164 339 7.6 0.0 area subtropical age 7 -577 1169 0.0 0.6 F (n=218) area 6 -579 1170 0.9 0.4 tropical age 6 -289 590 0.0 0.5 F (n=116) area 7 -288 590 0.3 0.5 age x 5 -293 597 6.4 0.0 area
Figure 4.3. Mixed-effects model regression estimates for functional trait groupings examined by climatic zone: a), b) and c) temperate (n = 70), d), e) and f) subtropical (n = 218) and h), i) and j) tropical (n = 116).
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Tropical and temperate climatic zones have negative slopes in relation to trait richness and age. This indicated a change in species composition and dominance as pumice moved into water with new species pools and abiotic influences.
Separate analysis of individual feeding trait modalities collected from different climatic zones showed that age was the most influential covariate
(Appendix M Table S10). Herbivores in temperate pumice rafts increased through time (age) and with the combination of age area (all with positive slopes) as the presence of carnivores decreased. Model weights relating to herbivores showed that age and area were almost equal in weighting and that age area provided a high level of explanatory power when compared with the subtropical climatic zone. For the subtropical climatic zone, herbivores present on pumice clasts increased through time (model weight
0.63) with a positive slope and had slightly positive slopes for both area
(model weight 0.27) and age area (0.10) (Appendix M Table S10). These trends observed in herbivores showed a direct inverse relationship with the presence of carnivores. For example, carnivores decreased with age and age
area in temperate climatic zones and decreased again with age in subtropical climes but increased with area and age area in subtropical climatic zones (Appendix M Table S10). Analysis of herbivores on tropical clasts showed no differences in explanatory power for either random or fixed effects, and this trend was also observed when the climatic zone data were combined (Appendix M Table S10). An important caveat of these results is that the models for age and area were within four AICc points and therefore explain a similar degree of variation in the data.
96 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Other feeding trait modalities, which may have increased in abundance similarly to herbivores because of release from potential predation by carnivores, are filter feeders. Filter feeders also exhibited positive slopes for age and the interactive effects of age area in temperate pumice rafts
(Appendix M Table S10). Biota that decreased, possibly because of increased pressure from herbivores, are primary producers (photosynthetic) such as cyanobacteria and algae. In temperate pumice, primary producers exhibited negative slopes for both age and age area. While primary producers collected on subtropical pumice exhibited positive slopes for age, area and age area with the individual fixed effect of age accounting for almost all the variation (model weight 0.96). In addition to these trends, two other trait modalities, scavengers and parasites (which can be considered similar to ‘carnivores’ in their feeding mode), also responded to climatic zone change by decreasing in abundance in temperate when compared with subtropical climes.
Separation of the reproductive trait richness data into climatic zone of arrival showed that age remained the most influential covariate (Appendix M
Table S10). Temperate reproductive trait richness was negatively related to both age and age area. Reproductive trait modalities measured from clasts collected from the subtropics showed positive correlations with all covariates.
By contrast in tropical water age became negative with area and age x area remaining positive (Appendix M Table S10 and Figure 4.3). Specifically, age explained most of the variation for the following reproductive traits. In temperate water, asexual reproducers (model weight 0.9); in subtropical
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 97
water, sexual (model weight 1); and in tropical water, spawner (model weight
1) (Appendix M Table S10). Where area became more influential (e.g. for protandrous hermaphrodites in subtropical water (model weight 0.6); for simultaneous hermaphrodites in tropical and tropical water (model weights
0.5) it was never more than 4 AICc points away from age in the model averaging table. Therefore, the models can be considered equivalent
(Appendix M Table S10).
Several reproductive trait modalities also responded to climatic zone change by decreasing in abundance in temperate climes for age and age area when compared to subtropical (e.g. asexual and sexual reproducers, dioecious biota, spawners and fragmenters) (Appendix M Table S10). The following trait modalities showed no influence of the tropical climatic zone in model estimates when comparing fixed and random effects: carnivores, herbivores, algal symbionts, filter feeders, grazer, scavenger, predator, dioecious and fragmenters. Therefore, it difficult to draw inferences for data relating to the tropical climatic zone.
Examining the Havre pumice data using PERMANOVAs showed that climatic zone of collection was a significant predictor of trait modality abundance (Table 4.4). However, visualisation using nMDS (Figure 4.2) showed that climate had reduced visible structure on the graph and that most climatic zones were fairly evenly spread throughout the graph. Differences in dispersion between the climatic zones of pumice arrival showed that the largest community trait modality composition changes were observed between the subtropical and temperate climes and that all other tests were
98 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
not significant (Table 4.8). Pair-wise tests indicated that the largest differences in pumice community composition were between tropical and temperate, followed by subtropical and tropical (Table 4.9).
Table 4.8. PERMDISP analysis of pumice rafted community trait richness and climatic zone providing a distance-based test for homogeneity of multivariate dispersions between climatic zones of tropical (n = 116), subtropical (n = 218) and temperate (n = 70) (NB: the number of permutations was set to 9999 for all models).
Climatic Zone t value p
Subtropical, temperate 2.7 0.02
subtropical, tropical 1.8 0.12
tropical, temperate 0.9 0.43
Table 4.9. Pair-wise comparison tests of pumice rafted community trait richness by climatic zones of tropical (n = 116), subtropical (n = 218) and temperate (n = 70).
Climatic Zone t value p Unique permutations
Tropical, temperate 1.61 0.01 9943
subtropical, tropical 1.60 0.05 9935
subtropical, 1.56 0.08 9956 temperate
4.4.3 Does a foundation species effect, such as that observed with Lepas barnacles, also occur in pumice rafted communities (see Gil & Pfaller 2016)? 4.4.3.1 Sessile and motile biota as predicted by Lepas barnacles The presence of Lepas barnacles (measured as both counts and cover) were a significant predictor of sessile species abundance, particularly with regard to the cover sessile species occupied per pumice clast and, to a lesser extent, motile species abundance (Table 4.10).
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4.4.3.2 Sessile biota and Lepas barnacles The best-fit predictive models for the effect of Lepas barnacles on sessile biota abundance examined both the cover of Lepas barnacles on individual pumice clasts compared with habitat area and a separate model comparing the number (or counts) of Lepas barnacles with habitat area.
These models showed that Lepas barnacle counts or cover accounted for
100% of the variation in the model and had a positive slope (Table 4.10).
Comparison of pumice age with the number of Lepas and sessile biota counts showed that age explained more variation than Lepas barnacle count.
However, the difference was small and the models were all within four AICc points. All other models examining sessile biota counts or cover showed that
Lepas barnacles were the most influential predictive variable (Table 4.10).
Table 4.10. Results of model comparison using Akaikie information criterion (AICc) values to identify factors explaining variations in functional trait modality. Analyses was conducted for the number and area of motile and sessile biota per pumice clast with the predictors of age, area and Lepas barnacle counts or cover. Note all data represented in the following table were derived using a normal distribution and, where necessary, the y variable was logged to enable model fitting.
Trait modality Effect df logLik AICc Delta Weight Full or reduced model (F or R) Motile count No. of 5 -397 803 0.0 0.5 F (y variable Lepas logged) age 7 -395 804 1.1 0.3 age 6 -396 804 1.2 0.3 No. of Lepas motile count No. of 5 -397 803 0.0 0.6 F (y variable Lepas logged) area 6 -397 805 1.9 0.2 No. of 7 -396 806 2.3 0.2 Lepasx area motile count Lepas 7 -401 817 0.0 1 F area
100 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Trait modality Effect df logLik AICc Delta Weight Full or reduced model (F or R) (y variable area 6 -406 824 6.7 0.0 logged) Lepas 5 -407 825 7.7 0.0 area area sessile count age 7 -360 735 0.0 0.4 F (y variable No. of 6 -362 735 0.4 0.3 logged) Lepas
age 5 -363 736 1.0 0.3 No. of Lepas sessile count Area of 5 -408 825 0.0 0.6 F (y variable Lepas logged) age 6 -407 826 1.2 0.3
age 7 -407 828 2.9 0.1 area of Lepas sessile count No. of 6 -357 726 0.0 0.7 F (y variable Lepas logged) area 7 -357 729 2.1 0.3 No. of 5 -363 736 9.4 0.0 Lepas area sessile area Lepas 7 -268 549 0.0 1 F (y variable area logged) area 5 -274 559 9.1 0.0 Lepas 6 -274 560 10.5 0.0 area area sessile area No. of 7 -267 547 0.0 1 F (y variable Lepas logged) area 5 -274.2 559 11.1 0.0 No. of 6 -273.7 560 12.2 0.0 Lepas area sessile area No. of 5 -329.9 670 0.0 0.5 F (y variable Lepas logged) age 7 -328.3 671 1 0.3 No. of 6 -329.5 671 1.3 0.2 Lepas age sessile area Lepas 5 -334.8 680 0.0 0.5 F (y variable area logged) age 7 -333.3 681 1.2 0.3 age 6 -334.4 681 1.3 0.3 Lepas area
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4.4.3.3 Motile biota and Lepas barnacles For motile biota, the explanatory power of Lepas barnacle counts or cover was reduced when compared with other variables. Most models examining the relationship between motile biota and Lepas barnacles indicated that the random effects of location and date of collection explained the data as much as the covariates examined. Three models remained valid for motile biota and Lepas barnacles in relation to the number of motile biota found on clasts. In all cases, Lepas barnacle counts or cover was a more influential predictor than area or age (Table 4.10). In particular, a model examining the area of Lepas barnacles, habitat area and the response variable of motile biota counts showed that the most influential predictor was
Lepas barnacle counts, which accounted for 100% of the motile biota numbers (Table 4.10). For all of these models, Lepas barnacle counts or cover was positively related to motile biota.
4.4.3.4 Overall, feeding and reproductive trait richness as predicted by Lepas barnacles For models examining the relationship between predictive variables of area of Lepas barnacles and habitat area to the response variable of total trait richness per clast, Lepas barnacle area accounted for all of the variation in the model (model weight 1). This trend held for both feeding and reproductive trait richness (Table 4.11). In models comparing the effects of the number of Lepas barnacles present with the response variable of total trait richness per clast and predictive variables of age or habitat area, both age and habitat area were more influential than the number of Lepas present
(model weights 0.42 and 0.45, respectively).
102 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Table 4.11. Results of model comparison using Akaikie information criterion (AICc) values to identify factors explaining variations in functional trait richness. Analyses was conducted for the total trait richness per pumice clast with the predictors of age, area and Lepas barnacle counts or cover. Note that all models represented in the following table were created using a normal distribution.
Trait grouping Effect df logLik AICc Delta Weight Full or reduced model (F or R) Total trait richness Age 7 -1011 2036 0.0 0.4 F
No. of 6 -1012 2036 0.4 0.3
Lepas age x No. 5 -1014 2037 1.4 0.2 of Lepas total trait richness habitat area 5 -1004 2019 0.0 0.5 F
No. of 7 -1003 2020 0.6 0.3
Lepas habitat area 6 -1004 2020 1.3 0.2 x No. of Lepas total trait richness Lepas area 7 -994 2002 0.0 1 F (habitat area Lepas area)
feeding trait Lepas area 7 -822 1659 0.0 1 F richness (habitat area Lepas area) reproductive trait Lepas area 7 -676 1366 0.0 1 F richness
(habitat area Lepas area) reproductive trait No. of 6 -684.0 1380 0.0 0.4 F richness Lepas
area 5 -685.2 1380 0.2 0.4
No. of 7 -683.5 1381 1.0 0.2 Lepas x area
reproductive trait age 7 -692.7 1400 0.0 0.4 F richness
No. of 6 -693.8 1400 0.2 0.4 Lepas
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Trait grouping Effect df logLik AICc Delta Weight Full or reduced model (F or R) age x No. 5 -695.7 1402 2.1 0.2 of Lepas
Models examining the total number of feeding trait modalities showed that the random effects of place and date of collection explained as much variation as the fixed effects apart from the model examining Lepas barnacle area (compared with habitat area and Lepas barnacle area). For reproductive trait richness, the trend was different because the number of Lepas correlated positively with the richness of reproductive traits present compared with habitat area, but the age of pumice clast was a stronger predictive variable than was Lepas number.
4.5 DISCUSSION
The assembly of functional trait richness on pumice rafts provides new insights into community assembly theory and functional trait richness of shallow marine ecosystem-dwelling biota. Specifically, I found strong evidence for overall trait richness increasing in relation to the age of pumice clasts indicating that biotic influences were the most influential community driver. Lending further weight to the dominance of biotic processes within pumice rafted communities, is the finding that Lepas barnacles had a strong positive association with increased trait richness while, at the same time, providing evidence in support of a foundation species effect (Gil & Pfaller
2016). I also found evidence that pumice clasts may be recruiting increasing
104 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
functional trait richness over time regardless of their habitat area as I did not find a significant interaction between age and area. Examination of trait abundances showed that area correlated more strongly than age, which supports the idea that increased habitat provision allows higher abundances, however increases in area did not result in increased trait richness (Goldstein et al. 2014; Whittaker et al. 2014).
The influence of abiotic factors becomes more apparent when pumice trajectory is altered because trait richness decreased on pumice clasts that were collected in temperate regions and on clasts collected in tropical regions as the pumice clasts aged. This finding suggests that biota may have been lost as pumice clasts encountered cooler or warmer water temperatures and physiological limits were exceeded (Thiel & Haye 2006; Wichmann et al.
2012; Alexander et al. 2016). I found strong evidence that both the species richness (Velasquez et al. 2018) and the functional traits of the biota comprising these communities increase in relation to habitat area and age
(Cadotte et al. 2011). My results indicate that, for isolated pumice clast habitats, both age and area provide meaningful avenues to explore the relationship between drivers of community assembly and resultant species and functional richness, while at the same time considering other abiotic drivers such as climate (Velasquez et al. 2018).
4.5.1 Increased functional trait richness was found on pumice clasts that were older and pumice clasts that had larger habitat space Increased functional trait richness was found on both older pumice clasts and those that had a larger habitat area, whereas smaller and younger clasts had less richness (MacArthur & Wilson 1967; Whittaker et al. 2008).
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This indicates that, in clasts in which space was not as limited, biotic factors
(e.g. niche space, competition and facilitation) had the greatest influence on the resultant community composition (Levine 1999; Hart & Marshall 2013).
These results also suggest that, while interference competition (where a larger organism overgrows a smaller one) can occur in pumice rafted communities, this is not the only form of competition occurring as if interference competition dominated, then I would expect that richness might decrease or remain stable through time (Crawley et al. 1986). This was not the case for pumice rafts because the pumice biota clearly increased in richness through time, which suggests that exploitation competition, in which biota compete for a limited resource that often favours more effective users of the resource (e.g. space), are also competitive in this environment and may be aided by initial colonisers via facilitative competition (Levine 1999;
Hart et al. 2012).
Age was the most influential covariate for predicting overall variation for both feeding and reproductive trait richness on pumice clasts. This finding suggests that the community diversifies and changes through time and that these changes result in the presence of higher trophic orders (such as carnivores) on older clasts. However, this effect of age on higher trophic orders, such as carnivores was limited to pumice from the subtropical climatic zone because the temperate rafted pumice lost carnivores through time.
Although age was more important for predicting the richness of pumice clast community assembly, examination of the communities in terms of the abundance of individual traits populating pumice clast surfaces showed that
106 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
area became a more influential explanatory variable. That is, similarly sized pumice clasts harboured similar richness and abundance of community traits regardless of the climatic zone trajectory. This result indicates that increased numbers of individuals with similar traits colonised larger clasts (Suding et al.
2008).
4.5.2 Change in climatic zone caused a resultant change in functional richness of the pumice rafted community Examination of changes because of climatic zone of pumice raft collection indicates that the influence of abiotic conditions, such as change in water temperature as a result of latitude, can restrict the presence of biota.
For example, presence of carnivores was lessened in temperate pumice, most likely because these species were recruited in subtropical waters, and unable to tolerate cooler temperatures. This change then allowed increases in other biota, such as, herbivores and filter feeders in pumice collected in temperate waters when compared to tropical and subtropical rafted pumice
(for evidence of this effect in other marine systems please see Osman 1978;
Anderson 1999; Wichmann et al. 2012). I also found evidence of species richness found on pumice clasts (Velasquez et al. 2018) where the separate effects of age and habitat area caused increased richness that varied dependent on the pumice trajectory (or relative isolation).
Although age remained the most important predictive variable for pumice rafted functional richness regardless of climatic zone of collection, the influence of age differed between trait groupings. Traits from the pumice community varied through time as pumice drifted south into temperate waters; this movement appears to have led to a change in the community
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 107
composition as trophic orders were lost. For example, I observed a reduction in the numbers and types of carnivores in temperate pumice rafts, which had the flow-on effect of increased herbivore and filter feeder abundance. The increase in herbivores ultimately resulted in increased pressure on primary producers (Alexander et al. 2016).
Importantly, herbivores were restricted to two epibiont groups—the gastropods Litiopa limnophysa (Melvill and Standen 1896) of which there were 190 individuals collected on 71 pumice clasts, and Rissoides species, of which one individual was collected on one pumice clast. Carnivores included bristle worms (57 individuals collected on 64 clasts), ostracod egg casings (one individual, which was indicative of adult ostracods) and gastropods from the family Naticidae/Janthinidae with a total of three individuals from three clasts. Closer examination of these numbers showed that herbivores were restricted to a small number of individual species (two in total) and that one was represented by a single individual. Carnivores were more diverse in terms of their initial richness and showed a distinct decrease as pumice entered cooler water as only 14 temperate pumice clasts contained carnivores, and these were all bristle worms.
4.5.3 Lepas barnacles promote richness via a foundation species effect in pumice rafted communities Lepas barnacle presence was found to be an influential (biotic) explanatory variable of trait richness on pumice clasts for most of the trait groupings analysed. This finding supports the findings of other studies that have shown that this genus acts as a possible foundation species in sessile marine floating communities (Gil & Pfaller 2016). Lepas barnacle area
108 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
correlated positively and more strongly with trait richness than did Lepas frequency, which suggests further that Lepas barnacles facilitate opportunities for other biota to colonise on pumice clasts. If Lepas barnacles were supressing colonisers, a negative relationship between Lepas area and trait richness would have been expected; however, I found a significant positive relationship. This surprising trend of an association between Lepas barnacle cover with an increase in sessile biota richness despite the reduction in available habitat because of Lepas presence suggests that
Lepas barnacles have a founder effect in floating pumice rafted communities
(Gil & Pfaller 2016).
Lepas barnacles may act as a foundation species on pumice clasts for the following four ecological reasons: i) increased clast stability as Lepas provide a biological keel as they grow on pumice clasts, reducing the amount of turning or position changes in the water column while clasts float in the open ocean and which can be stressful to sensitive biota, particularly biota, that is sensitive to solar radiation (see Irving & Connell 2002b; Irving &
Connell 2002a; Hart & Marshall 2013); ii) the provision of increased safe sites on pumice clast surfaces via the network of barnacle stalks, iii) a reduction in water flow across the surface of pumice clasts which has the potential to dislodge small colonising biota and iv) reduction in sediment accumulation close to the surface of pumice clasts via feeding flows which may impact sensitive biota (Irving & Connell 2002b; Hart et al. 2012; Gil & Pfaller 2016).
These effects have been reported in other studies. For example, Hart and Marshall (2012) found biota with small space requirements died in
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 109
experimentally formed habitat gaps that were too large and thrived in those that were small. These findings suggested a facilitative effect conferred by surrounding biota on smaller species, which may also occur as a result of the presence of Lepas barnacles on pumice rafts. Another study by Miller and
Etter (2008) showed that shading increased the abundance of surrounding filter-feeding sessile invertebrates, which could also be attributed to shading provided by stalks of Lepas barnacles. Lepas barnacles are some of the earliest reported colonisers of pumice rafts, and these species may be key in aiding the establishment of high species richness and subsequent trait richness within pumice rafted communities (Priestley 2012; Gil & Pfaller
2016).
Where abiotic conditions remained the most stable (i.e. in the subtropical climatic zone for Havre pumice rafts), pumice trait richness was found to be explained by biotic influences as through time (age) both feeding and reproductive trait richness was found to increase (Crawley et al. 1986;
Mayfield & Levine 2010; Hart & Marshall 2012). The subtropical climatic zone can be considered the most stable for Havre pumice because these rafts both originated and arrived in the subtropics (Velasquez et al. 2018). Pumice size was not as influential in predicting trait richness as age, which suggests that competition between biota and the provision of additional safe sites and/or clast stability via species richness (which both increased through time) provided the greatest chance of increased epibiont colonisation on individual pumice clasts (Crawley et al. 1986; Gil & Pfaller 2016).
110 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Habitat area was also important for explaining the number of traits per clast. Competition for habitat intensifies with greater species richness, and species with different traits are less likely to compete for the same resources or amounts of resources (Stachowicz et al. 1999; Goldstein et al. 2014).
Smaller habitats with reduced richness have also been reported in studies of plastic-rafted marine communities (see Goldstein et al. 2014) and marine communities in general (see Stachowicz et al. 1999). Trait abundance was most strongly related to available habitat space, and the frequencies increased within trait groupings on larger pumice clasts.
Overall, I found that both age and habitat area were significant influencers of trait richness forming on pumice rafts (Velasquez et al. 2018).
While consideration of other abiotic variables (e.g. climate) and biotic variables (e.g. foundation species effect) increase the understanding of alternative drivers of shallow marine biotic community formation (Gil & Pfaller
2016; Velasquez et al. 2018). These results were found despite a significant lack of biological knowledge of the functional traits of species inhabiting shallow marine ecosystems and their associated ecosystem functions (Frid
2011; Frid & Caswell 2016). I consider this research to provide an important increase in understanding of the abiotic and biotic processes that govern shallow marine ecosystem processes and resultant functional richness (Frid
2011; Frid & Caswell 2016; Velasquez et al. 2018). I acknowledge that the pumice rafted system is doomed (i.e. pumice stranding on coastlines is a mass mortality event). However, understanding how species richness translates into functional richness may expand the understanding of the
Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems 111
assembly and function of shallow marine ecosystems in general (Alexander et al. 2016; Frid & Caswell 2016)
4.6 ACKNOWLEDGEMENTS
I thank Dr Merrick Ekins (Queensland Museum); Lucy Hurrey (The
University of Queensland); Dr Alex Cook (The University of Queensland); Dr
Simon Groves (Tasmanian Museum and Art Gallery); Andrew Hosie
(Museum of Western Australia); Dr John Healy (Queensland Museum); Dr
Robyn Cumming (Museum of Tropical Queensland); Dr Pat Hutchings
(Australian Museum, Sydney); and Dr Elena Kupriyanova (Australian
Museum, Sydney) for their invaluable assistance in identifying the pumice rafted marine biota. I also thank Professor Marti J Anderson (Massey
University, New Zealand) who provided invaluable assistance and advice with statistical analysis.
112 Chapter 4: Biotic drivers and a foundation species effect explain community assembly on floating pumice ecosystems
Chapter 5: Small patches of endangered
Melaleuca irbyana R. T.
Baker forests are critical
refugia for plant species
5.1 ABSTRACT
Melaleuca irbyana R. T. Baker, is a critically endangered tree that forms an ecological community, of which only 8% of its original habitat area remains. In recent times, remnant forest managers have noticed reduced or absent seedling establishment within remaining forests of this community, leading to concerns about its risk of extinction. These observations have led to an assessment of the abiotic and biotic drivers of seedling establishment and associated overstory and herbaceous layers of diversity within extant M. irbyana forests. In this study, I examined the relative influence of factors hypothesised to explain differences in seedling establishment within remnant forests including remnant forest area, isolation, internal disturbance, overstory and herbaceous layer diversity, and soil fertility characteristics.
Overall, I found no evidence that seedling establishment was related to elements of the theory of island biogeography (TIB), such as remnant forest area or isolation with comparatively small remnant forest areas having increased seedling establishment. Instead, seedling establishment was Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 113
highly influenced by canopy disturbance and death of mature trees which is thought to lead to increased availability of resources such as light.
5.2 INTRODUCTION
Forest clearing is a main driver of the loss of species, functional trait diversity and resultant ecosystem stability and function (Ross et al. 2002;
Hobbs & Yates 2003; Mayfield et al. 2010). Typically the loss of forests as a result of human landscape modification has been non-random with flatter, easier to clear, and more fertile regions, close to a fresh water source, being targeted for agricultural and human settlement purposes (Laurance 2008;
Wintle et al. 2018). As a result of these landscape modifications, fragments of less disturbed forest often remain in a matrix of farms or urban environments
(Shafer 1995; Laurance 2008; Wintle et al. 2018). The principles outlined in the TIB and SAR of increasing habitat area and connectivity leading to increased preservation of biodiversity, has led to global movement in conservation policy and supporting science for the prioritisation and protection of large remnant forest areas with high connectivity (Shafer 1995;
Lindenmayer 2018; Wintle et al. 2018). This has led to highly fragmented small and isolated remnant forest areas commonly being overlooked or ignored in conservation prioritisation (Lindenmayer 2018; Wintle et al. 2018).
These small remnant forests, which are often degraded, have recently been found to provide important refugia for the conservation of rare or threatened species, biodiversity, functional traits and ecosystem function, leading to a re- evaluation of their value for conservation (Lindenmayer 2018; Wintle et al.
2018).
114 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
The theory of island biogeography (TIB) and its central principles such as the species–area relationship (SAR) predict that larger and less isolated remnant forest areas should contain more biodiversity that is representative of the original ecosystem and, at the same time, is more resilient to perturbations that have the potential to cause increased extinction risk
(MacArthur & Wilson 1963; MacArthur & Wilson 1967; Wintle et al. 2018).
Correspondingly, the SAR predicts that small remnant forest areas, which are often the last place some species remain, contain reduced biodiversity, relative to similar larger intact areas, with increased susceptibility to perturbations—whether natural (e.g. fires or floods) or anthropogenic (e.g. increased invasion by non-native species)—that might result in extinction
(Pickett & Thompson 1978; Shaffer 1981; Schemske et al. 1994; Prober &
Thiele 1995; Shafer 1995; Ross et al. 2002; Fahrig 2003; Wintle et al. 2018).
Following the central principles of the TIB and SAR, research has shown that extinction risk increases as remnant habitat areas become smaller and more isolated (Diamond 1972; Tilman et al. 1994; Brooks et al.
1999; Laurance et al. 2002; Kuussaari et al. 2009). Commonly there is also a lag in time between the habitat perturbation and species extinction, with this lag being referred to as an extinction debt (Tilman et al. 1994; Kuussaari et al. 2009). An extinction debt occurs due to several interacting factors
(Kuussaari et al. 2009). Long-lived species which have correspondingly low turn-over rates, such as trees, can remain in the modified landscape for many years before it is realised that juvenile recruitment is reduced or not occurring (Kuussaari et al. 2009). These species-specific life history elements then interact with the concept of an ‘extinction threshold’ (Kuussaari et al. Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 115
2009). An extinction threshold is the minimum size of intact remnant habitat area that allows a species to persist and must be of a large enough size, connectivity and quality to allow recruitment and survival of the next generation (Kuussaari et al. 2009). At the same time, larger and less isolated habitat area is thought to have increased chance of immigration from individuals or dispersed propagules (e.g. pollen or seed), which further increases the chance of species survival, when compared to smaller and more isolated habitats (MacArthur & Wilson 1963; Macarthur & Levins 1967;
Pickett & Thompson 1978; Wintle et al. 2018).
Many studies have used the SAR to predict how richness and associated ecosystem integrity and resistance respond to landscape modification (Lovejoy et al. 1984; Kirkpatrick & Gilfedder 1995; Prober &
Thiele 1995; Laurance et al. 2002; Ross et al. 2002; Mendenhall et al. 2014;
Wintle et al. 2018). Such as the loss of continuous forest cover that leads to small isolated remnant forest areas contained within a matrix of farm or urban landscapes (Lovejoy et al. 1984; Kirkpatrick & Gilfedder 1995; Prober &
Thiele 1995; Ross et al. 2002; Mendenhall et al. 2014). The SAR is an effective framework for investigating biodiversity and regeneration in remnant forest areas because these habitats function much like islands. They are often surrounded by inhospitable habitat (for most species) such as farmland or highly modified urban environments (much like the ocean is to an island).
Because of this fragmentation, these habitats are isolated from source propagules and potential colonisers (MacArthur & Wilson 1963; Pickett &
Thompson 1978; Hobbs & Yates 2003). At the same time, these remnants can be more susceptible to non-native plant and animal invasion and illegal 116 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
clearing (Wintle et al. 2018). Despite these problems, small isolated remnant forest areas can also be comprised of disproportionately high numbers of species including rare and endangered species (Kirkpatrick & Gilfedder 1995;
Lindenmayer 2018; Wintle et al. 2018).
The TIB and SAR are often used in the management of rare and endangered plant species whose populations are scattered across the landscape in remnant forests (MacArthur & Wilson 1967; Kirkpatrick &
Gilfedder 1995; Wintle et al. 2018). The principles of the TIB and SAR predict that larger remnant forests that are less isolated should contain more viable plant populations, including increased numbers of seedlings (MacArthur &
Wilson 1963; MacArthur & Wilson 1967; Kirkpatrick & Gilfedder 1995).
Increased seedling establishment is predicted in larger remnant forests because it is expected that specific abiotic and biotic conditions that aid seedling germination and survival will have higher chances of being internally preserved within larger remnant forests (Schemske et al. 1994; Shafer 1995;
Hobbs & Yates 2003). For example, tree species often require specific soil moisture and nutrient profiles and have specific light requirements for seedling germination and establishment (Horn 1985; Harrington 1991;
Beckage et al. 2000; Beckage & Clark 2003). While population decline due to inbreeding and genetic drift is also expected to be reduced in larger remnant forests (Schemske et al. 1994; Shafer 1995; Hobbs & Yates 2003). Rare or endangered species are more likely to be habitat specialists and, correspondingly, are less likely to survive in surrounding modified habitat such as farmland or urban landscapes and, therefore, have increased
Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 117
chances of long-term survival if larger remnant forest areas are retained
(Schemske et al. 1994; Hobbs & Yates 2003).
Evidence of the importance of remnant forest area for predicting species richness in remnant forests and the protection of rare and endangered plant species is equivocal (Kirkpatrick & Gilfedder 1995; Prober
& Thiele 1995; Kemper et al. 1999; Ross et al. 2002; Hobbs & Yates 2003;
Matthews et al. 2014). In some circumstances, retention of biodiversity is a different conservation outcome to the protection of rare and endangered species (Schemske et al. 1994; Kirkpatrick & Gilfedder 1995; Hobbs & Yates
2003; Matthews et al. 2014). This is because of the differing requirements of species considered habitat specialists, which are commonly also rare species and habitat generalists which are more likely to be commonly occurring species (Schemske et al. 1994; Kirkpatrick & Gilfedder 1995; Hobbs & Yates
2003; Matthews et al. 2014). Factors which are important predictors of seedling establishment within remnant forests include time since fragmentation (i.e. age of habitat patch) (Ross et al. 2002), maintenance of natural disturbance regimes (e.g. fire) (Pickett & Thompson 1978; Yates et al.
1994; Kirkpatrick & Gilfedder 1995; Keeley & Fotheringham 2000; Ross et al.
2002; Yates & Broadhurst 2002), available light for seedling establishment
(Horn 1985; Harrington 1991; Beckage et al. 2000; Beckage & Clark 2003), reduced herbaceous layer competitors for seedling establishment (whether non-native or native) (Harrington 1991; Beckage et al. 2000; Yates &
Broadhurst 2002; Beckage & Clark 2003), soil moisture content (Horn 1985;
Harrington 1991; Beckage et al. 2000), soil characteristics such as nutrients and pH (Horn 1985; Davis et al. 1999; Beckage & Clark 2003; Lake & 118 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
Leishman 2004; Leishman & Thomson 2005) and the presence of dispersal or pollination agents such as bees, ants and birds (Bond 1994; Wilcock &
Neiland 2002; Hobbs & Yates 2003; Aguilar et al. 2006).
Conservation efforts have been preoccupied largely with remnant forest area as a surrogate measure of ecosystem health and the conservation value of remnant forest areas (Schemske et al. 1994; Haila 2002; Yates &
Broadhurst 2002; Hobbs & Yates 2003; Wintle et al. 2018). This simplistic focus on habitat size has the potential to misguide conservation efforts towards larger remnant forests (Kirkpatrick & Gilfedder 1995; Ross et al.
2002; Lindenmayer 2018; Wintle et al. 2018). While larger remnant forests are extremely important to preserve, this focus risks undervaluing smaller remnant forests, when forest area may not be the most important driver of continued ecosystem resistance nor the preservation and regeneration of rare and endangered plant species (Kirkpatrick & Gilfedder 1995; Ross et al.
2002; Hobbs & Yates 2003; Wintle et al. 2018). Understanding the relative importance of different factors for explaining differing levels of seedling establishment of rare and endangered species will help managers to make the best use of limited budgets for conserving rare and endangered species into the future (Pickett & Thompson 1978; Schemske et al. 1994; Kirkpatrick
& Gilfedder 1995; Prober & Thiele 1995; Hobbs & Yates 2003; Wintle et al.
2018).
Melaleuca irbyana (R. T. Baker) is an Australian tree that forms dense monoculture thickets and, as an ecological community, is federally listed as critically endangered under the Environment Protection and Biodiversity
Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 119
Conservation Act 1999 and as an Endangered Regional Ecosystem under the Vegetation Management Act 1999 (Queensland). Because of its growth on low-lying flood plains with alluvial clay soils commonly adjacent to streams, M. irbyana was cleared extensively for agriculture and now occurs in small remnant forests within South-east Queensland and North-eastern
New South Wales (Harms 1996; Vickers & Cuong 2004). Recent surveys indicate that only 1000 ha of this community remains intact, which represents a little over 8% of its former range ((D.E.E.) 2004; Vickers & Cuong 2004).
Melaleuca irbyana is a naturally rare species with populations being locally abundant but geographically limited in distribution, which may be explained by restrictive habitat requirements and/or reduced competitive ability at certain life stages (Schemske et al. 1994; Soonthornvipat 2018). In recent times, managers of remnant M. irbyana forest have identified low seedling establishment of new trees in large remnant forests (e.g. Purga Nature
Reserve) (pers. comm. Young 2015), an observation corroborated by one of the very few published studies of this critically endangered ecosystem
(Vickers & Cuong 2004). Low seedling establishment can impact the long- term survival of this species because reduced regeneration within old-growth
M. irbyana forests may indicate that important environmental or abiotic cues
(e.g. fires, floods, light penetration or soil moisture content) or biotic facilitation (e.g. key pollinators or the microclimatic conditions created by intact overstory trees), which lead to seedling germination and establishment, are being disrupted within the remaining stands (Pickett & Thompson 1978;
Schemske et al. 1994; Vickers & Cuong 2004).
120 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
Loss of understory richness and seedling establishment beneath the stands of M. irbyana is important more generally for long-term forest health and resistance. These elements of diversity have been shown to result in improved nutrient cycling (Firn et al. 2007), increased topsoil stability (Lamb
1998) and increased habitat provision to other native fauna (Lindenmayer et al. 2000; Simonetti et al. 2013). The potential loss of this critically endangered regional ecosystem via reduced or absent seedling establishment within remaining forests means there is an urgent need to understand the factors that influence the longevity, productivity and overall health (as measured by the establishment of new seedlings into the understory) of these remnant forest areas in a peri-urban and farm-land context (Schemske et al. 1994; Hobbs & Yates 2003).
Information about the factors that explain seedling establishment within this ecosystem is consistent with the ‘top-down’ approach described by
Schemske et al. (1994). The top-down approach proposes that the recovery and conservation of rare plant species require a detailed understanding of the biological status of the focal species including an understanding of: i) whether a plant species population is increasing, decreasing or stable?; ii) which life history stage is the likeliest to cause reproductive failure? and iii) the factors explaining variation in reproductive success or failure for the species in question. This information will help managers to determine strategies to aid the long-term survival of these remnant populations both now and into the future (Schemske et al. 1994).
Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 121
In this study, I investigated relationships between different abiotic and biotic factors in relation to seedling establishment of M. irbyana. The abiotic factors include recent disturbance to mature overstory trees, soil nutrients and pH, remnant forest area and isolation. While biotic factors include overstory and understory diversity such as the presence of non-native species in relation to seedling establishment of both M. irbyana and other species in the understory of Melaleuca irbyana forest. The ability to reproduce successfully is vital to the long-term survival of a species and may indicate whether management practises are aiding regenerative processes
(Shaffer 1981; Schemske et al. 1994). Seedlings are the essential stage in the reproductive lifecycle of most plant species and, in the case of tree species, represent the make-up of the next generation of forest community. I have studied seedlings as a measure of overall health and success of current management practises in remnant forests of M. irbyana particularly because of its unique natural growth as a monoculture (Schemske et al. 1994; Davis et al. 1999). My study addresses three key questions:
1) Do remnant forest area, isolation and overstory forest variables, such as live versus dead stems (as a measure of disturbance), basal area (as a measure of productivity) and species richness, correlate with the abundance of seedlings of M. irbyana and other woody species?
2) Do non-native or native understory plant species and remnant forest area correlate positively with seedling establishment?
122 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
3) How do soil characteristics such as soil nutrients and pH relate to remnant forest area and seedling establishment of M. irbyana compared with other species?
Consistent with key elements of the TIB such as the SAR, I expect that larger remnant forest areas will hold a higher plant species richness and more seedlings, particularly of the focal species such as the critically endangered tree M. irbyana when compared with smaller remnant forest areas (MacArthur & Wilson 1963; MacArthur & Wilson 1967). An explanation is that particular resources, such as low soil nutrients or a specific nutrient or pH balance because of reduced run-off from surrounding land, are preserved to a greater extent within remaining “larger” remnant forests (Schemske et al.
1994; Lake & Leishman 2004). This preservation of resources would more easily allow the establishment of M. irbyana seedlings into the species matrix
(Schemske et al. 1994; Lake & Leishman 2004). Seedlings may be further protected in larger forests because the intact canopies of mature trees reduce edge effects, such as increased irradiation and wind speeds, which can reduce soil moisture and directly affect seedling survival (Horn 1985;
Harrington 1991; Heinemann et al. 2000). At the same time, I expect to see a reduction in non-native species internally within larger remnant forests, due to the protective effect of a larger area of intact mature forest and associated herbaceous layer (Harrington 1991; Ross et al. 2002). Reduced non-native species is expected to correspond to increased tree seedling survival, as non-natives may outcompete and overgrow potential seedling recruits
(Harrington 1991; Ross et al. 2002).
Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 123
I also expect that remnant forest isolation, as measured by the distance to the nearest extant remnant forest area of M. irbyana, will correlate positively with seedling establishment and survival (MacArthur & Wilson
1963; MacArthur & Wilson 1967; Schemske et al. 1994; Hobbs & Yates
2003). This is because the chance of genetic mixing resulting from pollination is increased with decreased distance between individuals, which decreases the effects of small isolated populations such as inbreeding and genetic drift
(Schemske et al. 1994; Wilcock & Neiland 2002; Hobbs & Yates 2003). The chance of immigration via wind-dispersed seeds (i.e. seed rain) also increases with decreasing distance (MacArthur & Wilson 1963; MacArthur &
Wilson 1967; Schemske et al. 1994; Hobbs & Yates 2003; Vickers & Cuong
2004; Soonthornvipat 2018). Non-native species were expected to have an increased prevalence in those remnant forests that are smaller and have had recent disturbance (as measured by dead stems) (Ross et al. 2002; Lake &
Leishman 2004). Remnant forests that are larger and have reduced disturbance would be expected to have a lower prevalence of non-native compared with native species herbaceous species (Ross et al. 2002).
5.3 MATERIALS AND METHODS
5.3.1 Field surveys Field surveys were undertaken at 12 sites of remnant M. irbyana forest located in the Ipswich and Logan city council areas of South-eastern
Queensland. Data were collected from May 2014 to December 2015 (Table
5.1). A total of 74 blocks, each measuring 10 m 10 m, were measured using a retractable 50 m tape and situated randomly under overstory of M.
124 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
irbyana throughout the 12 remnant forests. The number of blocks measured within each remnant forest was based on the total size of the remnant forests and presence of the focal species, M. irbyana. Determination of block number was finalised once field work began because of the lack of local knowledge of the prevalence of M. irbyana or forest dominated by other species. To compare differences between remnant forests comprised exclusively of M. irbyana, I also measured blocks under the commonly occurring species Melaleuca bracteata F. Muell., which is often found growing adjacent to M. irbyana.
Table 5.1. Details of remnant forest locality and area and the associated number of blocks sampled during the course of the field work undertaken for this study.
Remnant Remna Melaleuc Number of forest nt a 100 m2 name forest irbyana blocks/remna area extent nt forest (ha) (%)*
Henderso 45 35 20 n Reserve
Purga 36 90 20 Nature Reserve
Bottlebrus 9 3 5 h Park
Moffatt 15 42 5 Park
Victoria 14 3 5 Park Reserve
Waterford 6 40 5 West District Sports Park
Jimboomb 22 2 4 a Park
Duncan 6 1 2 Park
Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 125
Remnant Remna Melaleuc Number of forest nt a 100 m2 name forest irbyana blocks/remna area extent nt forest (ha) (%)*
Edelsten 42 1 2 Reserve
Kurrajong 10 1 2 Park
Manning 1 1 2 Park
Monmouth 5 1 2 Park *Note this is the total remnant forest area divided by the estimated extent of extant M. irbyana remnant population estimated using Google Earth and following ground-based field work. Within each block, the following overstory measurements were taken: tree species (or identifying characteristics recorded and a sample taken for later identification), diameter at breast height (DBH) for each tree, an estimate of height using Pythagoras’ theorem and a Suunto PM5/1520 Hgt
Meter Clinometer (note a Nikon Forestry Pro Laser Rangefinder could not be used because of the density of M. irbyana stand), and a count of all seedlings noting species and height. Seedlings were defined as those trees less than two metres in height and with a DBH less than five centimetres. Both of these criteria had to be met to be defined as a seedling because some trees were very tall but had a correspondingly low DBH.
Within each 100 m2 block, the understory herbaceous layer was quantified using five randomly placed 1 m2 plots (370 plots overall). Within each of these plots, all herbaceous species were identified, and the percentage cover of each species was estimated using the Daubenmire technique (see Daubenmire 1959).
126 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
5.3.2 Estimation of area and isolation The area of each remnant forest was estimated using tools available in the
Google Earth package and following discussions with local council representatives and adjustments occurring once field surveys had commenced. Remnant forests were in various states ranging from dense monocultures of M. irbyana to those where M. irbyana trees were scattered individually within open grassy paddocks, mixed-forest verges bordering playing fields or groups of individual trees mixed within other forest types
(e.g. Eucalyptus forest). It is not known whether these more diffuse populations (e.g. individual mature trees in grassy pasture or small clusters in mixed forest types) were present naturally or whether the individual trees remained because of historical escape from paddock clearing or other intense disturbances. Where possible, estimation of the remnant forest area was closely related to the presence of live mature M. irbyana trees. Areas of remnant forests that did not contain populations of M. irbyana were excluded where necessary.
Distances between remnant forests (as a measure of isolation) were estimated using tools available in the Google Earth package and were defined as the shortest distance in a straight line between remnant populations (Wills et al. 2017). Remnants separated by a road and grassy verge (e.g. Henderson and Victoria parks) were considered isolated and thus separate populations. Populations of M. irbyana on private property were also considered when estimating final isolation distances. For example,
Manning Park had a large intact M. irbyana forest situated directly across the
Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 127
road on private property that could not be surveyed for the purposes of this study.
5.3.3 Soil samples Within each block, four random soil cores to 10 cm were taken and grouped together in a labelled plastic bag for later nutrient and pH analysis.
All soil samples were stored in refrigerators at 4 C before analysis and were later air dried for two days at 40 C and then ground using a mortar and pestle to enable samples to pass through a 2 mm sieve. Samples were then mixed and split using a Quantachrome Rotary Micro Riffler into eight homogenous subsamples for nutrient and pH analysis.
5.3.4 Soil nutrient (LECO) analysis (total carbon and nitrogen) Soil combustion analyses were used to estimate the total carbon and nitrogen in a representative soil sample for each remnant forest. Using the
RockLab soil grinder and steel mill head, approximately 20 g of soil was ground to a fine powder and then sent to the Queensland University of
Technology Central Analytical Facility for soil nutrient analysis using a LECO
TruMac Elemental CNS Analyser (Case et al. 2012; McDowell et al. 2012).
5.3.5 Soil pH analysis Soil pH was measured following the methods of Rayment and Lyons
(2011). Twenty grams of each soil sample was weighed and placed in 120 mL tubes, and 100 mL of deionised water (DIW) was added (Rayment &
Lyons 2011). The tubes were then sealed and placed in an end-over-end shaker for one hour, following this, tubes were left standing for half an hour to allow soil settlement (Rayment & Lyons 2011). All soil pH measurements
128 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
were made using the TPS Aqua-CPA Conductivity-TDS-pH-Temp meter on the same day within four hours of sample preparation. During measurement, the end of the meter was submerged in the suspension and not in the soil settlement zone, the meter was rinsed with DIW between each measurement, and a replicate measurement was taken every 10 samples to check the reliability (Rayment & Lyons 2011).
5.3.6 Data analysis Calculation of overstory tree densities per hectare followed the method of Fensham et al. (2015), and these calculations are based on stem densities and basal area per hectare. The overall mortality for M. irbyana and individuals of other species was calculated as the sum of all dead stems divided by the sum of all stems across the remnant forest area in question.
The seedling density per block for both M. irbyana and total species
(excluding M. irbyana) was simply a count of the respective species per block and as such is referred to simply as number of seedlings throughout this chapter.
I used additive linear mixed-effects models (MEMs) in R (version 3.1.2;
Foundation for Statistical Computing) with the lme4 library (Bates et al. 2014) to investigate individual effects according to various fixed effects depending on the question. Overstory biotic predictive variables (fixed effects) tested included: remnant forest area, remnant forest isolation, dead tree density/ha, live tree density/ha, basal area/block, overstory species richness/block, live
M. irbyana density/ha, and dead M. irbyana density/ha. Understory predictive variables (fixed effects) included: non-native herbaceous richness/block, non-
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native herbaceous cover/block, native herbaceous richness/block, native herbaceous cover/block, total herbaceous layer richness/block, and total herbaceous layer cover/block. Abiotic soil predictive variables (fixed effects) used included: soil pH, soil nitrogen content, and soil carbon content. All models included the random effects of: block nested within remnant forest. F statistics and p-values were calculated using analysis of variance (ANOVA) for each fixed effect to determine its influence on the response variable compared with other fixed effects.
5.4 RESULTS
I surveyed more than 4000 trees (of all species) and 254 M. irbyana seedlings (Table 5.2) at the 12 remnant forests surveyed.
Table 5.2. Establishment number of M. irbyana seedlings by remnant forests examined for this study.
Remnant forest M. irbyana Total number of Seedlings seedlings recorded Live or dead
Duncan Park live 2
Duncan Park sum 2
Edelsten Reserve live 5
Edelsten Reserve dead 1
Edelsten Reserve sum 6
Henderson live 4 Reserve
Henderson dead 2 Reserve
Henderson sum 6 Reserve
Jimboomba Park live 5
Jimboomba Park sum 5
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Remnant forest M. irbyana Total number of Seedlings seedlings recorded Live or dead
Kurrajong Park live 10
Kurrajong Park dead 2
Kurrajong Park sum 12
Manning Park live 4
Manning Park dead 1
Manning Park sum 5
Moffatt Park live 22
Moffatt Park dead 1
Moffatt Park sum 23
Monmouth Park live 1
Monmouth Park dead 1
Monmouth Park sum 2
Purga Nature live 80 Reserve
Purga Nature dead 29 Reserve
Purga Nature sum 109 Reserve
Victoria Park dead 1
Victoria Park sum 1
Waterford West live 81 District sports Park
Waterford West dead 2 District sports Park
Waterford West sum 83 District sports Park
Grand total 254
5.4.1 Do remnant forest area, isolation and overstory forest variables, such as live versus dead stems (as a measure of disturbance), basal area (as a measure of productivity) and species richness,
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correlate with the abundance of seedlings of M. irbyana and other woody species? The presence of live and dead M. irbyana seedlings (indicators of successful germination) were both strongly correlated with the presence of live M. irbyana overstory trees (live seedlings: F1,58 = 1575, p < 0.0001; dead seedlings: F1,58 1516, p < 0.0001) (Table 5.3 and Figure 5.1). Presence of live M. irbyana seedlings was then most influenced by the density of M. irbyana overstory. Variation in the number of live M. irbyana seedlings also correlated positively, although weakly, with overstory species richness (Table
5.3).
Variation in the number of dead seedlings of M. irbyana was then explained by the density of M. irbyana stems in the overstory, with a neutral slope. This was followed by species richness of the overstory having a slightly negative slope, which suggests a reduction in seedling mortality as richness increased (Table 5.3 and Figure 5.1). The abundance of M. irbyana seedlings, whether dead or alive, did not vary significantly with the size of the remnant forest area or isolation (Table 5.3)
The number of seedlings of species other than M. irbyana within M. irbyana dominated remnant forests were significantly positively correlated with overstory disturbance (dead trees: F1,58 = 2046, p < 0.0001) (Table 5.3 and Figure 5.1). Overstory species richness (block) was also significant with a weakly positive slope (F1,58 = 986, p < 0.0001), (Table 5.3 and Figure 5.1).
It is important to note that remnant forest area was not found to be a significant explanatory variable (Table 5.3).
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Table 5.3. Model outputs for ANOVA method derived from mixed-effects models for overstory forest metrics as explanatory variables of M. irbyana seedling establishment and seedling establishment overall.
Response variable Predictive variable df F-value p-value
Live M. irbyana seedling Dead trees (ha) 58 1808 <0.0001 number/block (log scale) live trees (ha) 58 950 <0.0001 overstory species 58 490 <0.0001 richness (block) remnant forest area 9 21 <0.001 (ha) distance (km) 9 5 0.05 basal area (block) 58 3 0.09
dead M. irbyana seedling dead trees (ha) 58 1147 <0.0001 number/block (log scale) overstory species 58 340 <0.0001 richness (block) live trees (ha) 58 243 <0.0001 basal area (block) 58 13 <0.0006 distance (km) 9 3 0.11 remnant forest area 9 0.17 0.70 (ha)
live M. irbyana seedling M. irbyana live trees 58 1575 <0.0001 number/block (log scale) (ha)
M. irbyana dead trees 58 1269 <0.0001
(ha) overstory species 58 1033 <0.0001 richness (block) basal area (block) 58 60 <0.0001 remnant forest area 9 24 <0.0009 (ha)
distance (km) 9 6 0.04
dead M. irbyana seedling M. irbyana live trees 58 1516 <0.0001 number/block (log scale) (ha) basal area (block) 58 45 <0.0001 overstory species 58 4 0.04 richness (block) M. irbyana dead trees 58 0.81 0.37 (ha distance (km) 9 3 0.11 remnant forest area 9 0.14 0.72 (ha) seedling number (excluding dead trees (ha) 58 1080 <0.0001 M. irbyana)/block (log scale) overstory species 58 899 <0.0001 richness (block) live trees (ha) 58 850 <0.0001 basal area (block) 58 164 <0.0001 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 133
Response variable Predictive variable df F-value p-value
distance (km) 9 266 <0.0001 remnant forest area 9 49 1 x 10-04 (ha) seedling number (excluding M. irbyana dead trees 58 2046 <0.0001 M. irbyana)/block (log scale) (ha) overstory species 58 986 <0.0001 richness (block) distance (km) 9 284 <0.0001 basal area (block) 58 279 <0.0001 M. irbyana live trees 58 139 <0.0001 (ha) remnant forest area 9 48 1 x 10-04 (ha)
Figure 5.1. Mixed-effects model regression estimates for: a) Live M. irbyana seedlings number/block as predicted by overstory richness in all remnant forests; b) Dead M. irbyana seedlings number/block as predicted by overstory richness in all remnant forests; c) Live total no. seedlings number/block as predicted by overstory richness in all remnant forests; d) Live M. irbyana seedling number/block as predicted in M. irbyana dominated remnant forests; e) Dead M. irbyana seedling number/block as predicted in M. irbyana dominated remnant forests
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and f) Live total no. seedlings number/block as predicted in M. irbyana dominated remnant forests.
The presence of M. irbyana seedlings (live versus dead) and the
presence of live seedlings of other species when examining mixed
overstory (including M. irbyana dominated) correlated strongly with
recent disturbance to the forest overstory, as indicated by the density of
dead trees per hectare (live M. irbyana seedlings: F1,58 = 1808, p <
0.0001; dead M. irbyana seedlings: F1,58 1147, p < 0.0001; live
seedlings of all other species: F1,58 1080, p < 0.0001) (Table 5.3).
For live M. irbyana seedlings, other influential and significant
explanatory variables were live tree density (ha) (including all species)
(F1,58 950, p < 0.0001) and overstory species richness (per block) (F1,58
490, p < 0.0001), with only overstory species richness having a slightly
positive slope (Table 5.3 and Figure 5.1). For dead M. irbyana
seedlings, this trend was slightly different; the next most influential
explanatory variables were overstory species richness (block) (F1,58 340,
p < 0.0001), live tree density (ha) (F1,58 243, p < 0.0001) and basal area
(block) (F1,58 13, p < 0.0006) (Table 5.3). Overstory richness, showed
a weak negative correlation with the number of dead M. irbyana
seedlings (Figure 5.1).
Remnant forest area (ha) and remnant isolation were not
significant explanatory variables of dead M. irbyana seedlings. By
contrast, for live M. irbyana seedlings, remnant forest area (ha) and
remnant isolation were weak but significant explanatory variables
(Table 5.3 and Figure 5.1).
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5.4.2 Do non-native or native understory plant species and remnant forest size correlate positively with seedling establishment? Non-native richness and cover in the understory, regardless of whether
M. irbyana dominated or mixed species overstory (including M. irbyana) were examined, correlated positively with disturbance, as indicated by dead trees
(Table 5.4 and Figure 5.2). Interestingly, for non-native richness in M. irbyana dominated forest, remnant forest area was the second most influential explanatory variable, followed by overstory species richness, which had neutral and positive slopes, respectively (Table 5.4 and Figure 5.2).
Following this, in mixed overstory forest (including M. irbyana), overstory richness was the second most significant predictor of non-native richness and cover, both of which had positive slopes (Table 5.4 and Figure 5.2).
Table 5.4. Model outputs for ANOVA derived from mixed-effects models for overstory forest metrics as explanatory variables of non-native versus native establishment into the understory.
Response variable Predictive variable df F-value p-value
Non-native understory Dead trees (ha) 58 352 <0.0001 richness/block (log scale) overstory species 58 226 <0.0001 richness (block) remnant forest area 10 136 <0.0001 (ha) live trees (ha) 58 0.53 0.47 basal area (block) 58 0.02 0.89
non-native understory dead trees (ha) 58 187 <0.0001 cover/block (log scale) overstory species 58 177 <0.0001 richness (block) basal area (block) 58 9 0.004 remnant forest area 10 2 0.16 (ha) live trees (ha) 58 0.00 0.97
non-native understory M. irbyana dead trees 58 568 <0.0001 richness/block (log scale) (ha)
remnant forest area 10 138 <0.0001
(ha)
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Response variable Predictive variable df F-value p-value
overstory species 58 90 <0.0001 richness (block) M. irbyana live trees 58 6 0.02 (ha) basal area (block) 58 0.53 0.47
non-native understory M. irbyana dead trees 58 185 <0.0001 cover/block (log scale) (ha overstory species 58 101 <0.0001 richness (block) basal area (block)) 58 11 0.002 M. irbyana live trees 58 6 0.02 (ha) remnant forest area 10 2 0.16 (ha)
native understory richness/ remnant forest area 10 1384 <0.0001 block (log scale) (ha) overstory species 58 1137 <0.0001 richness (block) live trees (ha) 58 588 <0.0001 dead trees (ha) 58 305 <0.0001 basal area (block) 58 47 <0.0001
native understory cover/ remnant forest area 10 748 <0.0001 block (log scale) (ha) live trees (ha) 58 501 <0.0001 overstory species 58 22 <0.0001 richness (block) basal area (block)) 58 14 0.0004 dead trees (ha) 58 3 0.10
native understory richness/ overstory species 58 1423 <0.0001 block (log scale) richness (block) remnant forest area 10 1364 <0.0001 (ha) M. irbyana dead trees 58 556 <0.0001 (ha) basal area (block)) 58 10 0.002
M. irbyana live trees 58 0.01 0.93 (ha)
native understory cover/ remnant forest area 10 675 <0.0001 block (log scale) (ha) basal area (block)) 58 37 <0.0001
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Response variable Predictive variable df F-value p-value
overstory species 58 37 <0.0001 richness (block) M. irbyana live trees 58 37 <0.0001 (ha) M. irbyana dead trees 58 0.62 0.43 (ha)
Figure 5.2. Mixed-effects model regression estimates for: a) richness of non-native understory / block as predicted in a mixed species overstory; b) cover of non-native understory / block as predicted in a mixed species overstory; c) richness of non-native understory / block as predicted by M. irbyana dominated overstory; d) non-native cover / block as predicted in M. irbyana dominated overstory.
Native herbaceous layer richness and cover in the understory was most strongly correlated with the remnant forest area, except for native richness in
M. irbyana dominated remnant forests (Table 5.4). Here native richness was correlated most strongly with species richness of the overstory but with a negative slope, while remnant forest area was the second most influential predictor with a positive slope (Table 5.4 and Figure 5.3). Native richness and cover had strong positive slopes in relation to remnant forest area in all
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forest types except for native cover within M. irbyana dominated forest which had a neutral slope (Figure 5.3).
Figure 5.3. Mixed-effects model regression estimates for: a) richness of native understory/block as predicted in a mixed species overstory; b) cover of native understory/block as predicted in a mixed species overstory; c) richness of native understory/block as predicted by M. irbyana dominated overstory; d) native cover/block as predicted in M. irbyana dominated overstory.
For both M. irbyana seedlings and other seedling species non-native richness showed a significant positive correlation (Table 5.5 and Figure 5.4).
Non-native cover was also weakly positively correlated with the number of live M. irbyana seedlings as was native richness, but live M. irbyana seedlings was negatively correlated with native herbaceous cover (Table 5.5 and Figure 5.4).
Seedlings of other species also exhibited a negative correlation to native richness, but not with native cover which was weakly positive (Table
5.5 and Figure 5.4). Dead M. irbyana seedlings were positively correlated Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 139
with both native and non-native richness (Table 5.5 and Figure 5.4). Whereas native and non-native cover had neutral slopes in relation to frequency of dead M. irbyana seedlings (Table 5.5 and Figure 5.4). Overall, regardless of native or non-native species, total richness of the herbaceous layer was correlated with increased presence of seedlings while understory cover was strongly negatively correlated with live M. irbyana seedlings (Table 5.5 and
Figure 5.4).
Table 5.5. Model outputs for ANOVA method derived from mixed-effects models for understory non-native and native richness and cover as explanatory variables of M. irbyana seedling establishment.
Response variable Predictive variable df F-value p-value
Live M. irbyana seedling Non-native richness / 58 325 <0.0001 number/block (log scale) block native cover / block 58 293 <0.0001 non-native cover / 58 182 <0.0001 block native richness / 58 47 <0.0001 block
dead M. irbyana seedling native richness / 58 497 <0.0001 number/block (log scale) block non-native richness / 58 167 <0.0001 block native cover / block 58 56 <0.0001 non-native cover / 58 5 0.02 block
live M. irbyana seedling total understory cover 60 221 <0.0001 number/block (log scale) / block total understory 60 196 <0.0001 richness / block
dead M. irbyana seedling total understory 60 10 0.003 number/block (log scale) richness / block
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Response variable Predictive variable df F-value p-value
total understory cover 60 2 0.13 / block
seedling number (excluding non-native richness / 58 444 <0.0001 M. irbyana)/block (log scale) block native cover / block 58 350 <0.0001 non-native cover / 58 69 <0.0001 block native richness / 8 7 0.01 block
seedling number (excluding total understory cover 60 764 <0.0001 M. irbyana)/block (log scale) / block total understory 60 167 <0.0001 richness / block
Figure 5.4. Mixed-effects model regression estimates for native and non-native richness and cover as explanatory variables of: a) Live M. irbyana seedling number / block; b) dead M. irbyana seedling number / block. And total richness and cover of the herbaceous layer as explanatory variables of: c) Live total seedling number / block Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 141
(excluding M. irbyana); d) Live M. irbyana seedling number / block; e) Live total seedling number / block (excluding M. irbyana).
5.4.3 How do soil characteristics such as soil nutrients and pH relate to remnant forest area and seedling establishment of M. irbyana compared with other species? Numbers of M. irbyana seedlings, both live and dead, were significantly positively correlated with soil pH and soil carbon content. By contrast, soil nitrogen content had a significantly negative correlation with numbers of live and dead M. irbyana seedlings (Figure 5.5). Interestingly, soil nitrogen content was significantly positively correlated with the abundance of seedlings of species other than M. irbyana (Table 5.6 and Figure 5.5).
Table 5.6. Model outputs for ANOVA method derived from mixed-effects models for the abiotic factors of remnant forest area and soil nutrients (nitrogen, carbon and silicon) and pH as predictors of M. irbyana versus total seedling establishment.
Response variable Predictive variable df F-value p-value
dead M. irbyana seedling C soil 59 228 <0.0001 number/block (log scale) pH soil 59 104 <0.0001
N soil 59 11 0.0014 remnant forest area 10 0.13 0.7244 (ha) live M. irbyana seedling C soil 59 430 <0.0001 number/block (log scale) pH soil 59 354 <0.0001
N soil 59 31 <0.0001 remnant forest area 10 14 0.004 (ha) seedling number (excluding N soil 59 1823 <0.0001 M. irbyana)/block (log scale) pH soil 59 687 <0.0001
C soil 59 249 <0.0001 remnant forest area 10 45 0.0001 (ha)
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Figure 5.5. Mixed-effect model regression estimates showing seedling number as predicted by the abiotic explanatory variables of remnant forest area (ha), pH (soil), total nitrogen (soil) and total carbon (soil): a) live M. irbyana seedling number/block; b) dead M. irbyana seedling number/block; c) live total seedling number/block (excluding M. irbyana).
5.5 DISCUSSION
Contrary to expectations, I found that my predictions based on the TIB and SAR of a reduction in remnant forest isolation and increasing remnant forest area were not significant explanatory variables of M. irbyana seedling number and survival. However, increased remnant forest area correlated with
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increased richness and cover of the other native plant species in the herbaceous layer, as described in these theories. Instead, I found that M. irbyana seedling abundance correlated positively with increased overstory disturbance and increasing overstory species richness. These results suggest that light availability is a significant predictor of M. irbyana seedling germination and establishment (Beckage et al. 2000; Heinemann et al. 2000;
Hautier et al. 2018). In addition, increases in soil nitrogen levels and herbaceous layer cover may act to suppress M. irbyana seedling germination and establishment.
5.5.1 Disturbance of overstory trees and increasing overstory richness was strongly linked to establishment success of M. irbyana seedlings. Disturbance to overstory trees, rather than remnant forest size, was the most influential variable acting on seedling number and survival within the understory. Specific examination of M. irbyana seedling establishment in relation to forests comprised of mature live or dead M. irbyana showed that these trends altered slightly. That is, live M. irbyana seedlings were influenced more by the abundance of live M. irbyana overstory followed by dead M. irbyana overstory. This finding suggests that, while live mature M. irbyana trees are important for providing the initial seeds for seedling establishment, without subsequent disturbance resulting in mature tree mortality, seedlings may not persist (Heinemann et al. 2000; Beckage &
Clark 2003). A similar result was found by Heinemann et al. (2000) who investigated overstory gaps in Nothofagus forest in Patagonia. Here they found that overstory gaps contained enough seed from surrounding adult trees to allow seedling establishment but that seedling germination and 144 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
survival were strongly related to the within-gap microclimate, with moist edges having the most seedlings (Heinemann et al. 2000).
Further evidence of the importance of light as a predictor of M. irbyana seedling abundance is my finding that numbers of dead M. irbyana seedlings were most strongly related to live M. irbyana overstory density; while dead M. irbyana overstory was not statistically significant. This finding suggests that healthy intact M. irbyana overstory may exclude and eventually cause the death of M. irbyana seedlings given sufficient passage of time without disturbances that cause overstory openings and light infiltration.
Mature tree death, increasing species richness of the M. irbyana forest overstory (as occasionally a species of Eucalypt or Acacia was present within
M. irbyana stands) and those seedlings recorded underneath canopies of
Melaleuca bracteata (which were found growing alongside or within dense stands of M. irbyana) may allow increased light to reach the forest floor within the M. irbyana dominated forests (Soonthornvipat 2018). Soonthornvipat
(2018) found that the dense overstory formed by M. irbyana monocultures had significantly reduced photosynthetically active radiation compared with forests comprising Melaleuca bracteata. In this study of M. irbyana forests,
Soonthornvipat (2018) planted both M. irbyana and M. bracteata beneath canopies of both mature trees of M. irbyana and M. bracteata. She found lower seedling survival beneath canopies of M. irbyana compared with M. bracteata. In seed germination trials, Soonthornvipat (2018) also found the same trends of reduced germination and survival of both species planted beneath mature M. irbyana trees compared with M. bracteata.
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Gaps in the overstory are known to increase seedling survival in other forest communities because of increased resource availability (Beckage &
Clark 2003). Disturbance in the overstory increases light, provides a flush of extra soil nutrients and reduces competition from understory plant species at least initially before any increase in colonisation (Beckage et al. 2000;
Beckage & Clark 2003).
In this research, visible signs of previous burning were noted during the vegetation surveys as the presence of mature dead trees with blackened trunks and stumps. Many of these were of unknown species because of difficulty with identification due to advanced decomposition, but they were most likely M. irbyana. These blocks also contained higher numbers of live seedlings of M. irbyana. This observation suggests that fire may provide an environmental cue that causes release of seeds from the overstory of M. irbyana, as is the case for other species of Melaleuca (see Kaufman &
Smouse 2001). This release would cause seedlings to germinate subsequently while at the same time providing an overstory opening and bare ground that allows light to penetrate to soil level (Keeley &
Fotheringham 2000).
By contrast, Vickers and Cuong (2004) found that after a mature M. irbyana tree was set alight, seed rain (the incidence of seed falling from the overstory layer of mature M. irbyana trees, which is known to be promoted by fire in other Melaleuca species) did not increase and nor did the establishment of seedlings in the months after this treatment. They acknowledged that this result could be attributable to the short length of time
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for their study, that only a small number of trees underwent treatment and that the fire duration, intensity and temperature were not measured (Vickers
& Cuong 2004). It should also be noted that the trees set alight for the study of Vickers and Cuong (2004) (of which only two were studied at Moffatt Park
(pers. comm. Markula 2015) and no data were available for the trees lit at
Purga Nature Reserve) were extremely difficult to set alight. This suggests that M. irbyana may be resistant to fire and that these controlled fires may not have been of the intensity needed for seed rain or seedling germination.
Hence, although fire may not directly promote the generation of seeds (in the form of seed rain) or directly influence seedling germination (as found by
Vickers & Cuong 2004 in laboratory fire treated germination trials) it may subsequently promote seedling regeneration by creating bare ground and overstory openings within the M. irbyana understory (Keeley & Fotheringham
2000; Ross et al. 2002).
Contrary to my prediction, based on the TIB and SAR, that larger remnant forest areas would contain greater numbers of seedlings, I found little or no relationship between either live or dead M. irbyana seedling presence and remnant forest area. Two of the largest remnant forests in my study, Henderson Nature Reserve comprising 45 ha and Purga Nature
Reserve comprising 36 ha, had completely different levels of M. irbyana seedlings, 6 and 109 seedlings, respectively. One of the smaller remnant forests, Waterford West District Sports Park (WWDSP), comprised of 6 ha in total and had 83 M. irbyana seedlings present. Observations of WWDSP in the field noted that many mature dead trees at this park had blackened bark, which suggested that a fire had occurred there in the past few years. The fire Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 147
was followed by flooding in early 2015, and Logan City Council staff noted they observed the emergence of additional seedlings following the flooding event (pers. comm. Markula 2015). This observation may be related to the fact that M. irbyana seedlings require both increased light and disturbance, as is the case for tree seedlings studied other ecological contexts (Horn
1985; Yates et al. 1994; Beckage et al. 2000). Another remnant forest in my study with relatively high levels of M. irbyana seedling abundance was
Moffatt Park. This remnant forest comprised 15 ha and had 23 seedlings present in my blocks. This remnant forest is the only remnant forest known to
Logan City Council as having had some incidence of fire in the past 10 years, in which about five wild fires are known to have occurred (pers. comm.
Markula 2015). In support of this argument, when I examined the incidence of seedling abundance other than M. irbyana (e.g. Acacia, Eucalyptus and
Lophostemon species), I found that these seedlings were more prevalent in relation to dead trees and were influenced by overstory species richness more than remnant forest area. This possible explanation is consistent with the study by Ross et al. (2002), who examined Eucalyptus forest fragment species richness in relation to age, anthropogenic disturbance and fire history. They found that remnant forest area was not the most important predictive variable but that age and disturbance type were more influential
(Ross et al. 2002). In that study, species richness was more reduced in small, young and medium, old fragments, whereas those fragments that had recently burned had increased native richness (Ross et al. 2002). The finding of Ross et al. (2002) that forest age had a deleterious effect on species richness, may be indicative of the presence an extinction debt for certain
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species within remnant forests they examined (Kuussaari et al. 2009). In another study of rare and threatened plant species in remnant forest areas in subhumid Tasmania, Kirkpatrick and Gilfedder (1995) found no relationships between remnant forest area, age or location in the landscape and the presence of rare and threatened plant species. Rare and threatened species examined in that study were located in a variety of habitat sizes and conditions, and some were in very poor condition (Kirkpatrick & Gilfedder
1995).
5.5.2 Non-native herbaceous species richness and cover correlated with increases in M. irbyana seedling establishment in small disturbed remnant forest areas, whereas native herbaceous species richness and cover correlated with larger remnant forest areas. Non-native understory richness and cover was closely related to the death of mature overstory trees and increasing species richness of the overstory. This provides further evidence that increased light availability caused by tree mortality and reduction in M. irbyana overstory
(Soonthornvipat 2018) increased the emergence of other species from the soil seed bank (Ross et al. 2002; Beckage & Clark 2003). The densities of both M. irbyana seedlings and seedlings of other species increased as both non-native and native understory richness increased. This finding suggests that light gaps and other disturbance promoted species emergence and richness on multiple levels (from herbaceous to woody species). Non-native cover increased in conjunction with M. irbyana seedling presence, whereas native cover seemed to have caused suppression of M. irbyana seedlings by outcompeting seedlings for limited resources such as light.
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Overall, regardless of whether the herbaceous layer comprised native or non-native species, increasing species richness of the herbaceous community was linked to increasing seedling number of species other than
M. irbyana. Herbaceous cover was overall negatively correlated with M. irbyana seedling survival, which indicated that as cover increased M. irbyana seedlings may have been outcompeted for limiting resources such as light or nutrients. Similar results have been found by several studies (Harrington
1991; Davis et al. 1999; Beckage et al. 2000; Yates et al. 2000; Yates &
Broadhurst 2002; Beckage & Clark 2003). In those studies, seedling establishment decreased in the presence of herbaceous layer competitors in relation to one or all of the limiting resources of light, water and nutrients.
Disturbance is commonly linked to the invasibility of ecosystems by both non-native and native species, and it is not surprising that loss of mature trees allows increased seedling and herbaceous layer growth in the forests I examined (Hobbs & Atkins 1988; Burke & Grime 1996; Duggin & Gentle
1998). This finding is consistent with evidence reported by Levine (2000), who found that diversity of invaders and native species occurred simultaneously and that the most diverse assemblages studied were the most likely to be invaded. This is deemed to occur not because of diversity itself but because of variation in resources in the environment (e.g. disturbance resulting in increases in available habitat space, light and nutrients), which promote the growth of both existing species and new species in the same location (Levine & D'Antonio 1999; Levine 2000). Other studies of forests have also found that disturbance (Duggin & Gentle 1998) or disturbance plus nutrients (Hobbs & Atkins 1988; Lake & Leishman 2004; 150 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
Leishman & Thomson 2005) promote successful invasion by non-native plant species.
Interestingly, remnant forest area was found to confer less protection than expected when it came to suppressing non-native richness. Non-native richness and cover were most strongly linked to recent disturbance in all forest types, but this relationship became even stronger in M. irbyana forests where non-native richness increased with increasing remnant forest area.
This finding contradicts the commonly held tenet of the SAR that larger remnant forests would confer a protective effect regarding invasibility by non- native species. At the same time, native understory richness and cover were also found to increase as remnant forest size increased, which lends weight to the continued relevance of the SAR when examining richness of all species regardless of their origin (Ross et al. 2002). Ross et al. (2002) found a similar result when examining the effect of fragmentation on eucalypt forest. Here native species richness increased even in small fragments where anthropogenic disturbance was low, but species were lost as fragments aged and with time since fire (Ross et al. 2002).
5.5.3 Seedling number of M. irbyana decreased with increasing nitrogen levels whereas other seedling species increased in richness. Increasing nitrogen content within soils examined, correlated with a decreased number of both live and dead M. irbyana seedlings. Soil pH and carbon increased with increased numbers of live M. irbyana seedlings. This indicates that, although the soils tested were acidic, as they approached neutrality (or became increasingly alkaline), M. irbyana preferred less acidic soils. This may reflect the link between rain events and M. irbyana
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germination (Soonthornvipat 2018). Interestingly, the number of seedlings other than M. irbyana (e.g. Acacia, Lophostemon or Eucalyptus species) increased markedly as the nitrogen content of soil increased. These findings suggest that other native seedlings can outcompete M. irbyana seedlings when nutrients and light levels increase simultaneously.
Studies of seedling survival in experimental plots where combinations of nutrients and water were added have shown that the herbaceous layer is a strong competitor for these limited resources (Harrington 1991; Davis et al.
1999). Both Davis et al. (1999) and Harrington (1991) found that seedlings could not outcompete herbaceous plants for nutrients or water within experimental plots but could take advantage of these resources when competitors were removed. Similar results were found in a study of native and non-native plants undertaken in the Hawkesbury Sandstone soils of
Sydney, Australia (Leishman & Thomson 2005). In that study, experimental addition of nutrients in the field or in a glasshouse increased the biomass and presence of non-native invasive species as well as native invasive species, such as Acacia spp. (Leishman & Thomson 2005). In another study of invasive Acacia spp. in the African Fynbos, Acacia increased the available soil nitrogen content, because of their ability to fix nitrogen, and subsequently altered the native plant composition as a result of their presence (see
Witkowski 1991).
Other studies have also shown that plant available soil nitrogen levels increase as a result of disturbance (e.g. fire) (Christensen 1973). This increase is due to increases in temperature of the soil layer (resulting in
152 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
increasing microbial activity that produces plant available nitrogen) combined with the removal of plants using nitrogen or in the case of fire disturbance
(Christensen 1973). Increases in plant available organic nitrogen and ammonium in the soil result from the addition of ash; hence, disturbance that promotes regeneration may also contribute to increases in the amount of available soil nitrogen (Vitousek & Melillo 1979; Tardiff & Stanford 1998;
D'Antonio & Meyerson 2002).
Overall, my results indicate that mature stands of M. irbyana can survive and thrive on soils of low nutrient content (e.g. nitrogen) and that their overstory cover can act to suppress the incidence of M. irbyana seedlings as well as seedlings of other species and the herbaceous layer beneath
(Beckage & Clark 2003; Soonthornvipat 2018). My results also indicate that disturbance that caused death of mature trees may be needed for seedling establishment and survival in the M. irbyana understory. However, these disturbances may also promote the occurrence of unfavourable non-native species and native species such as Acacia spp., which may change the soil nutrients and potentially the plant composition of a remnant forest (Witkowski
1991; Beckage & Clark 2003).
As Melaleuca irbyana exhibits low seedling establishment rates and population recovery, remnant forest managers may need to actively manage remaining remnant forest areas to reduce the extinction risk for this critically endangered species (Kuussaari et al. 2009). Active management could involve revegetating ecologically appropriate areas adjacent to existing stands to improve remnant forest area extent and connectivity (Kuussaari et
Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 153
al. 2009). In addition, methods could be adopted to promote selective disturbance of mature overstory trees to promote seedling establishment within remnant forests (Kuussaari et al. 2009). Selective canopy disturbance should be tailored to simultaneously promote seedling and native understory establishment, while at the same time suppressing non-native invasive species. Without actively causing M. irbyana regeneration, the extinction risk of this critically endangered ecosystem will only continue to increase
(Kuussaari et al. 2009). It is likely that remnant M. irbyana forests have an unrealised extinction debt due to its known long-lived life history in combination with its low levels of seedling establishment and the extent of its habitat fragmentation (Kuussaari et al. 2009). Evidence already exists for an extinction debt occurring within the herbaceous understory of M. irbyana forests with reduced native herbaceous layer diversity occurring within smaller remnant forest areas (Kuussaari et al. 2009).
The effects of climatic change may also result in loss of mature trees from these remnant forests in the long term (D'Antonio & Meyerson 2002;
Fensham et al. 2015; Hobbs et al. 2018). For example, increased drought or fire incidence can remove all mature trees from a remnant forest and, while this may result in new M. irbyana seedling emergence from the soil seed bank, it will mostly likely also promote the regeneration of other seedling species and non-native herbs (Fensham et al. 2015). In a study of
Eucalyptus dominated savannah ecosystems in the Desert Uplands biogeographic region of Queensland (see Fensham et al. 2015), increased drought and temperature extremes were found to affect the dominant tree species (i.e. Eucalyptus species), which had low population recovery rates 154 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
(similar to M. irbyana) the most severely. Although this species was able to respond rapidly to fire via resprouting, this came with the price of shallower root systems, which conferred reduced drought resistance compared with other species sampled for the study (Fensham et al. 2015).
If a selective management plan that uses disturbance to promote regeneration in remnant M. irbyana forest is adopted, these remnant forests would need careful monitoring both to increase understanding of the manner in which disturbance promotes regeneration of M. irbyana, but also to determine the risk of non-native and native invasive species becoming more prevalent as a result of disturbance in these remnant forests (D'Antonio &
Meyerson 2002; Leishman & Thomson 2005). Managers should therefore consider multiple ways in which mature overstory could be selectively disturbed and removed to simultaneously reduce the incidence of unwanted non-native species growth on remnant patches of M. irbyana forest
(D'Antonio & Meyerson 2002). For example, although M. irbyana has not been shown to be dependent on or to regenerate directly following fire, it also does not seem to exhibit reduced incidence of seedling germination after fire treatment compared with background seedling germination (Vickers & Cuong
2004). Therefore, following longer and more extensive fire studies on this species and the non-native species found in its understory, it may be possible to use controlled burns of a certain intensity, temperature and frequency to reduce above-ground M. irbyana overstory while at the same time removing from the soil seedbank undesirable non-native species
(D'Antonio & Meyerson 2002). As demonstrated in other studies, sometimes the use of fire or disturbance while promoting native species is quite Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species 155
successful in removing non-native species (see Hastings & DiTomaso 1996).
In other examples, fire or disturbance may significantly increase undesirable plants (see D'Antonio et al. 1993; Fensham et al. 1994).
In summary, disturbances to the overstory layer will most likely increase the seedling richness of all species and native and non-native herbs (for example see Levine & D'Antonio 1999; Levine 2000). However, leaving the remnant forests of M. irbyana as they stand with little regeneration and a potentially increasing non-native understory could lead to the complete loss of this threatened ecosystem, particularly under the influence of a changing climate (D'Antonio & Meyerson 2002; Kuussaari et al. 2009; Fensham et al.
2015; Hobbs et al. 2018).
5.6 ACKNOWLEDGEMENTS
I thank John Thompson, now retired, from the Queensland Herbarium for his invaluable assistance in identifying and confirming the identities of the species collected for the purposes of this study. I also thank Ms Anna
Markula for her invaluable assistance in determining the remnant forests in
Logan City Council area where I could survey remnant M. irbyana for the purposes of this study and her tenacity in providing information based on the knowledge of staff at Logan City Council. I thank Mr. John A. Young of
Ipswich City Council for meeting with us and allowing us to conduct field work at the largest forest remnant of M. irbyana located at Purga Nature Reserve. I sincerely thank Ms Karine Harumi Moromizato, who trained us in the relevant soil preparation and sampling methods required for nutrient and pH analysis for the study. I also thank the team of undergraduate science students from
156 Chapter 5: Small patches of endangered Melaleuca irbyana R. T. Baker forests are critical refugia for plant species
Queensland University of Technology who helped collect the primary data used to complete this paper including Jacob Rolley, James Beattie, Kerrod
Bate, Nicola Green, Caitlin Riordin, Samantha Burns, Bianca Knaggs,
Susanna Imarisio and Elysia Andrews.
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Chapter 6: Discussion
The main aim of the research presented in this thesis was to provide a better understanding of the abiotic and biotic factors that explain species assembly in two different and rarely studied ecosystems in two very different contexts: marine versus terrestrial. This study also aimed to contrast the application of fundamental ecological theories such as the TIB and SAR between the unassisted formation of communities on floating pumice rafts
(Chapters 3 and 4) versus the relatively human-made and ecologically degraded remnant forest communities comprised of M. irbyana (Chapter 5).
This work also aimed to add to the understanding of how the promotion of biodiversity might be achieved under differing climatic conditions (e.g. temperature) (Chapters 3 and 4) and how retention of biodiversity and regeneration of specific species might be linked (Chapter 5).
The marine context was examined by studying pumice raft community ecology in the Pacific Ocean, and the terrestrial context was examined by studying the health of remnant forests of a critically endangered ecosystem
M. irbyana (swamp tea-tree). Both ecological communities I investigated have rarely been researched. There are four previous publications on pumice rafted communities (see Bryan 1971; Bryan et al. 2004; Bryan et al. 2012;
Velasquez et al. 2018). While one Honours thesis and one PhD thesis have investigated forest regeneration, for remnant M. irbyana forests (see Vickers
& Cuong 2004; Soonthornvipat 2018). This ability to compare and contrast
Chapter 6: Discussion 159
two rarely studied ecosystems, has allowed me to provide new information on community assembly and resistance within each community context.
The two contexts I studied were different in terms of their formative processes and levels of connectivity. Pumice rafted marine communities were formed following formative community assembly processes on the surfaces of newly formed uninhabited pumice clasts. Pumice rafted communities, can also be considered to have higher connectivity, or reduced habitat isolation, when compared to M. irbyana remnant forest areas. This is particularly relevant when considering the mobility of the pumice rafts floating on the surface of the ocean and encountering differing source propagules.
This connectivity resulted in differing communities forming on the surface of pumice clasts depending on the climatic zone of collection (Velasquez et al.
2018). Variation in pumice rafted community composition was also dependent on key concepts illustrated in the TIB and SAR (MacArthur &
Wilson 1967). For example, pumice rafted species and functional richness both increased with pumice age, habitat area and changed depending on my definition of habitat isolation, which was derived from differing pumice raft trajectory (MacArthur & Wilson 1967; Velasquez et al. 2018).
In contrast to this, remnant forest areas of M. irbyana were formed from degrading processes resulting from human landscape modification
(Kuussaari et al. 2009). These degrading processes have led to remaining remnant forests of this ecosystem losing connectivity through habitat fragmentation and may explain why my predictions based on the TIB and
SAR were not upheld (Kuussaari et al. 2009; Wintle et al. 2018). For example, in this context my predictions, which were based on the TIB and
160 Chapter 6: Discussion
SAR, of increasing remnant forest area and reduced isolation (or connectivity) resulting in increased M. irbyana seedling establishment, increased native richness and suppression of non-native species were equivocal. Increases in remnant forest area was associated with increased diversity of the native herbaceous layer, but increased area did not translate to the suppression of non-native herbaceous species. While increased numbers of M. irbyana seedling establishment was found in smaller remnant forest areas with evidence of disturbance. It is likely that these remnant forests also have an unrealised extinction debt, which means that as these forest fragments relax through time towards a new equilibrium state, as described in the TIB, more native species including M. irbyana have the potential to become extinct, at least locally, as non-native species become increasingly dominant (Diamond 1972; Tilman et al. 1994; Kuussaari et al.
2009).
The observations made for each ecosystem were compared to one of the oldest theories in ecology the theory of island biogeography (TIB) and its central premise the species–area relationship (SAR) to determine their continued relevance (or otherwise) as predictors of ecological processes in time and space (MacArthur & Wilson 1967; Brown & Lomolino 2000;
Lomolino 2000). Overall, I learned that while generalised trends which adhere to fundamental ecological theories such as the TIB and SAR, exist in nature; the most important and correspondingly useful patterns found relate to more detailed examination of habitat and its quality rather than more simply the number of species (Kitchener et al. 1980; Kirkpatrick & Gilfedder
1995; Fahrig 2003). This chapter summarises my learning around the key
Chapter 6: Discussion 161
outcomes from each chapter and identifies my recommendations for future work and improvements that emerged from my PhD research.
6.1 CHAPTER 2
6.1.1 Summary of key outcomes The TIB has long been used as a theoretical model for how species richness forms in isolated habitats; however, in recent years, its continued use and relevance have been called into question because of the lack of strong evidence to support its principles of immigration and extinction, as suggested by the theory, in real ecosystem contexts (MacArthur & Wilson
1963; Gilbert 1980; Laurance 2008). Despite these difficulties, improvements and adjustments to the TIB have continued to be formulated by researchers wanting to understand the key drivers of community assembly in time and space. Therefore, additional contextual drivers have been added to the TIB and have aided its continued relevance in modern ecological research
(Whittaker et al. 2008). For example, Whittaker et al. (2008) was able to increase the predictive power of the TIB by using the TIB’s underlying assumptions and lines of evidence in the creation of a new mathematical model the GDM (Whittaker et al. 2008). Here Whittaker et al. (2008) added processes operating on geological timescales, such as island life cycle, and further considered the ‘age’ and isolation of islands examined. The GDM has been tested and has been shown in subsequent studies (for example see
Keppel et al. 2010) to markedly improve the predictive outcomes of these models. I tested elements of the GDM such as ‘age’ or pumice clast ontogeny (Chapters 3 and 4) to increases in both species and functional
162 Chapter 6: Discussion
richness (Velasquez et al. 2018). Here I found that age was the most influential explanatory variable for both of these measures of richness.
6.1.2 Future work and improvements As the saying goes, all models are wrong—although some are useful
(Whittaker et al. 2008). Keeping this in mind, I believe that the TIB has continued utility in modern ecological research by providing at minimum a starting point in thinking about how and why certain biota exist where they do in space and time. However, more importantly, my research found that in certain contexts, tests of this model provide one of the most parsimonious explanations of the key drivers of community assembly; for example, the species richness and functional richness of pumice rafted biota in the South- western Pacific (Velasquez et al. 2018). Although tests of the TIB in this research did not provide the most influential explanation for the health and diversity of flora within remnant forests of M. irbyana, it did provide a useful starting point from which to tackle the questions and problems that need solving for this critically endangered ecosystem. As such, I believe the TIB and its central principles such as the SAR have value in the context of ecological research and, at the same, this theory should be continuously improved based on the increasing understanding of the natural world and ability to process vast amounts of data about ecological systems.
6.2 CHAPTER 3
6.2.1 Summary of key outcomes The key outcome of this study was that tests of the TIB and SAR can have continued relevance in understanding the key drivers of community assembly in time and space. Communities forming on the surface of floating
Chapter 6: Discussion 163
pumice clasts were found to adhere to the key tenets of the TIB, namely the
SAR (Velasquez et al. 2018). While incorporating components from the TIB’s subsequent iterations such as the GDM showed that both age and area
(habitat space) were strong predictors of species richness (Whittaker et al.
2008; Velasquez et al. 2018). However, I also examined the change in species richness as a result of climatic zone of collection, which can be considered a test of ecological isolation. I found that the relationships between age and area changed according to the climatic zone encountered and that was most likely explained by a change in species as the biological thresholds of species were reached. For example, as pumice entered cooler water, new species took the place of species needing warmer waters to survive (Velasquez et al. 2018).
6.2.2 Future work and improvements The findings of this study are limited because I did not perform controlled laboratory or field experiments to test the ability of sedentary marine biota to colonise pumice stones through time and space. Controlled microcosm experiments examining pumice artificially and permanently located at a boat harbour and/or in a laboratory would provide greater accuracy for testing the processes underlying theories such as the TIB, GDM and SAR. For example, placing pumice in permanent positions within a boat harbour would allow examination of how changes in community composition altered with season on pumice clasts of varying size (Osman 1978; Anderson
1999).
The study of pumice rafted community assembly is also limited as the communities forming on pumice clast surfaces are very short-lived (Bryan et
164 Chapter 6: Discussion
al. 2012; Velasquez et al. 2018). This is because pumice rafted communities only survive for relatively short timeframes, from pumice formation to stranding on the coastlines of islands and continents (Velasquez et al. 2018).
Stranding of pumice clasts on coastlines can therefore be thought of as a mass-mortality event. Despite this inherent limitation to the study of pumice rafted community assembly, this system provides a very unique opportunity to examine community assembly. This is because with pumice rafted communities I was able to determine the date of habitat formation (i.e. volcano eruption) with high accuracy. Additionally, I knew each pumice clast was devoid of biota initially and then gradually accumulated biota through time and dependant on resultant pumice raft trajectory (Velasquez et al.
2018). Knowledge of the timing of habitat formation and trajectory (based on climatic zone of collection) has provided me with a rare opportunity to examine communities in terms of their age, area and isolation with a high degree of accuracy which is commonly absent in ecological community assessments (Velasquez et al. 2018). In addition, I was also able to document and identify all of the biota which colonised the surfaces of pumice clasts with a high degree of accuracy. Estimation of biodiversity and assessment of the abiotic and biotic processes which influence community assembly are always difficult to measure. Despite the short-lived nature of the pumice rafted community and my inability to determine the exact trajectory of pumice over the open ocean including shallow marine ecosystem encounters and expected increases in propagule pressure.
Examination of pumice rafted communities has provided new information on
Chapter 6: Discussion 165
the processes which govern sessile marine community assembly in time and space.
Future studies on pumice rafting would also benefit from the ability to identify all biota down to the species or genus level to allow for more precise analysis of the numbers and types of species that form these communities. I suggest that key experts (as identified in the acknowledgements for Chapter
3) be contacted and networks established before the collection of pumice in the field so that expert knowledge on the correct preservation of biota for the later correct identification can be conducted.
Further understanding of the genetics of pumice rafted biota, particularly in relation to the corals that have been observed on the surface of pumice clasts and in reefs throughout the Pacific Ocean but are known to have very short dispersal distances, may shed light on how these same species of coral exist in reefs separated by thousands of kilometres. It may be that pumice rafting has provided a dispersal mechanism lasting many hundreds (or even millions) of years for sedentary species such as corals to proliferate in different shallow ecosystem environments throughout this region. Determination of the true extent of the genetic linkages between these disparate reef ecosystems with further data may be important in the current context of climate change and the effect it is having on reef ecosystems worldwide.
Experiments could also be conducted to examine the potential of pumice rafted biota, particularly sedentary species such as corals and lace corals, for both colonisation of new habitats via fragmentation or pumice sinking and overgrowth. This would allow determination of the true relevance
166 Chapter 6: Discussion
of pumice rafting in aiding the colonisation of new habitats with beneficial species.
6.3 CHAPTER 4
6.3.1 Summary of key outcomes The work presented in this chapter showed that the functional traits of biota rafting on the surface of pumice clasts can also be predicted by the central premise of the TIB, the SAR, and by incorporating aspects of subsequent iterations (e.g. age and isolation as proposed by the GDM)
(MacArthur & Wilson 1963; MacArthur & Wilson 1967; Whittaker et al. 2008).
Examination of these data in relation to the climatic context again showed that consideration of context can profoundly influence the number and types of traits present in the communities rafted on the surface of pumice. In addition, this work showed that founder species such as barnacles of the
Lepas genus had a considerable influence on the richness of subsequent community trait composition; the presence of Lepas barnacles was a strong predictor of trait numbers in rafted pumice communities. This conclusion supports the theory that both exploitation and interference competition can be highly influential in contexts often assumed to be dominated by interference competition, such as benthic marine environments (Crawley et al. 1986; Hart
& Marshall 2012).
Area was the most influential predictive variable for determining the abundance of traits comprising communities assembled on the surface of pumice rafts. This finding lends further weight to the use of the lines of evidence contained within the TIB and GDM in the exploration of data
Chapter 6: Discussion 167
relating to isolated habitats. A similar result was found by Whittaker et al.
(2014) in a study exploring the relationship between species richness of spiders and beetles, their functional richness and habitat area within the isolated islands of the Azorean archipelago. Here, species richness was found to be a good predictor of functional richness and both scaled to island area (Whittaker et al. 2014). The next most influential predictors of trait abundance for pumice rafts examined for this PhD research were age and climatic zone. Change in community trait composition altered with climatic zone of collection and differences in the dispersion of pumice rafted traits showed the largest difference was between subtropical and temperate climatic zones. These results were found despite an inability to identify all biota rafted on the surface of pumice clasts and loss of motile species, which may have disembarked upon arrival on the coastlines of islands and continents where collections were made.
6.3.2 Future work and improvements Limitations of this work stem from the fact that controlled laboratory experiments were not conducted. For example, controlled experiments examining the likelihood of pumice rafted biota to colonise both with and without the presence of Lepas barnacles would help to determine whether a founder effect is present in both pumice- and plastic-rafted communities of the Pacific Ocean (Gil & Pfaller 2016). In addition, experimental invasion of biota into different-sized habitat patches on the surface of pumice clasts could be conducted to examine the role of exploitation competition in benthic marine ecosystems (Hart & Marshall 2012; Hart & Marshall 2013).
168 Chapter 6: Discussion
Future work should consider conducting field experiments to assess the success (or otherwise) of the ability of pumice rafted epibionts to colonise successfully within novel climatic scenarios (i.e. new habitats) and within local species pools (Alexander et al. 2016). As suggested by the study of
Alexander et al. (2016), this work is urgently needed, particularly in light of climate change where dispersal of new species into new habitat areas (as occurs with pumice rafting) may have unforeseen consequences for local native populations (Bryan et al. 2012; Velasquez et al. 2018). At the same time, movement of species via pumice rafting may allow sensitive species
(e.g. certain species of coral), which have been found on floating pumice rafts outside their native range (Velasquez et al. 2018), the chance to survive and escape habitat areas that have exceeded their biological thresholds (e.g. increased water temperature) (Wichmann et al. 2012; Alexander et al. 2016).
This might be tested by modelling the translocation experiments of sessile marine species conducted by Hart and Marshall (2012). In that study, juvenile recruits of sedentary marine invertebrates were superglued into experimentally created habitat gaps of differing sizes within plates that contained established native sedentary communities of nine months age submerged within Manly Boat Harbour, Brisbane, Australia (Hart & Marshall
2012). These experiments showed that biota that can beneficially use limited resources (i.e. exploitation competition) such as habitat space were more competitive invaders in established benthic marine communities (see Hart &
Marshall 2009, 2012; Hart & Marshall 2013). These findings shed light on the competitive effects of different species in relation to habitat area and interspecific and intraspecific competition.
Chapter 6: Discussion 169
6.4 CHAPTER 5
6.4.1 Summary of key outcomes The work of this chapter showed that, in contradiction to the TIB and
SAR, habitat isolation and area were not the most important predictive variables determining remnant forest health in relation to seedling establishment within the critically endangered ecosystem Melaleuca irbyana
(Swamp tea-tree). I found here that seedling abundance was more strongly linked to levels of disturbance that had resulted in death of mature overstory trees, which allowed more light to reach the forest floor (Horn 1985; Beckage
& Clark 2003). I also found that seedling abundance of M. irbyana within M. irbyana remnant forests was related to specific soil characteristics such as reduced nitrogen soil concentrations and acidic soils, which approached alkaline pH levels. The only component of this ecosystem that was shown to correlate with habitat area was the species richness of native herbs present in the understory of M. irbyana remnant forests.
6.4.2 Future work and improvements The study of M. irbyana establishment and associated biodiversity is limited because experiments were not conducted to determine whether disturbance to the canopy resulted in increased establishment of M. irbyana seedlings. Experiments should be conducted in the field and glasshouse to determine the effects of different disturbance regimes on M. irbyana establishment. Results from this PhD research showed that both seedling germination growth and establishment are linked to disturbance, but the key types of disturbance that lead to successful seedling establishment were indeterminable both in this study and another study (see Vickers & Cuong
170 Chapter 6: Discussion
2004) except that seedling establishment was found to require the death of mature overstory trees. Field experiments could examine the difference between simple removal of the understory herbaceous layer and overstory trees and burning of trees to cause mature tree death and removal of understory native and non-native species. This should be coupled with studies of the effect of these practises on the diversity of both native and non-native herbs and species of other tree seedlings, which may germinate from the soil seed bank at the same time as M. irbyana because this study found links between the incidence of both native and non-native herbs and seedlings of other tree species.
Future work on M. irbyana should include examination of the link between the health and productivity of these remnants in relation to ground water connectivity. Coal seam gas extraction is becoming more prevalent in the surrounding remnant farmland, and it is possible that changed hydrological flows could inadvertently cause disruption to the long-term survival of this ecosystem (if this has not had some undetectable impact already).
While habitat size and isolation (key tenets of the TIB) were not found to be a strong explanation of M. irbyana remnant health, it may be that due to the severe level of fragmentation and the degrading processes which dominate the formation of these ecosystem remnants that opposite trends to the TIB might exist (Matthews et al. 2014). While it was not possible to determine the age of forest fragments in the timeframe of this study, it may be worthwhile considering the age of fragmented patches of this ecosystem and its relationship with a future unrealised extinction debt (Tilman et al.
Chapter 6: Discussion 171
1994; Kuussaari et al. 2009). Indications of a future extinction debt for M. irbyana remnant forests are shown by the recent reduction in establishment of seedlings and loss of native diversity (Tilman et al. 1994; Ross et al. 2002;
Whittaker et al. 2008; Kuussaari et al. 2009).
6.5 CONCLUSIONS
Overall, the TIB and SAR were useful starting points that I was able to use to increase my understanding of the fundamental abiotic and biotic processes driving community assembly within two distinct contexts—pumice rafting and remnant forests of M. irbyana. I found that very different processes act within these two insular habitat types to form the resultant biotic communities that exist within them (Whittaker et al. 2005; Laurance
2008). This research has shown that, on the one hand, habitat area and age are helpful predictors of the richness of pumice rafted communities but, on the other hand, habitat area is not related to the establishment of M. irbyana forest seedlings (Ross et al. 2002; Velasquez et al. 2018).
The most parsimonious reason for the predictive power of the SAR for the communities forming in pumice rafts is that these communities exhibit relatively high levels of connectivity (i.e. are not isolated) and are formed from a set of unassisted formative and community assembly processes, including, volcanic eruption resulting in pumice formation and subsequent colonisation by animal and plant propagules as pumice floats through the open ocean (Bryan et al. 2012; Velasquez et al. 2018). In addition, the closer adherence in this system to factors described by the TIB (and later the GDM; see (Whittaker et al. 2008)) and in particular the ‘island-like’ characteristics of
172 Chapter 6: Discussion
each pumice clast. For example each clast has the following properties: i) is formed at the same time and place; ii) comprises similar chemistry; iii) has similar habitat heterogeneity on the surface; and iv) is devoid of biota initially; v) biota colonises the clast gradually; following formative community assembly processes and; vi) a trajectory path with clustered pumice rafts through the open ocean that traverses varying temperatures in proximity to differing levels of source propagules to achieve final community assembly
(Bryan et al. 2012; Velasquez et al. 2018). In addition, I was able to determine accurately the available habitat quantity on each pumice clast and, despite some loss of motile biota, was also able to measure with some accuracy the total richness of epibionts residing on each pumice clast surface
(Bryan et al. 2012; Velasquez et al. 2018).
By contrast, communities of M. irbyana are human-made degraded remnant forests of what were once larger pieces of contiguous forests and other habitat types ((D.E.E.) 2004; T.S.S.C. 2005). These communities are isolated as they remain within a matrix of other land use types (Schemske et al. 1994; Shafer 1995; Matthews et al. 2014). In contrast to the richness of pumice rafts, for M. irbyana questions remain about the biology and driving processes of what was once a much larger ecosystem that has been disrupted and where key disturbance regimes or biotic drivers of regeneration may be supressed or missing (Schemske et al. 1994; Yates & Broadhurst
2002; Hobbs & Yates 2003). I also closely examined the M. irbyana community in relation to the regeneration success of one species M. irbyana and while the SAR did not hold for this habitat specialist, it did provide some predictive power more generally for the richness of native herbs located in
Chapter 6: Discussion 173
the understory of remnant M. irbyana remnant forests (Ross et al. 2002;
Matthews et al. 2014).
Habitat area is a common surrogate used by governments and managers for the preservation of biodiversity and regeneration of rare and endangered species (Kirkpatrick & Gilfedder 1995; Ross et al. 2002; Hobbs &
Yates 2003; Wintle et al. 2018). Use of the TIB and associated lines of thinking in my PhD research, has allowed me to consider the influence of habitat area and isolation alongside other biotic and abiotic factors, in preserving biodiversity and conservation of a rare and endangered plant species (MacArthur & Wilson 1963; MacArthur & Wilson 1967). While it is certain that large areas of wilderness should be conserved to provide insurance for the long-term preservation of biodiversity and habitat specialists including rare or endangered species (Matthews et al. 2014; Wintle et al.
2018). My findings indicate that the quality of habitat, rather than its size, was equally or more important for pumice rafted community assembly and for the preservation of endangered species, such as M. irbyana, than habitat area or degrees of isolation in both of the study systems I examined. For pumice rafting this was evinced by epibiont richness and trait richness increasing through time where abiotic conditions remained relatively stable rather than in relation to increases in habitat area see Velasquez et al. (2018) and
Chapter 4. For M. irbyana, this was evinced by smaller rather than larger habitat patches containing the required disturbance regimes that allowed seedling establishment into the understory (see Chapter 5). This finding provides more evidence in support of the continued conservation and rehabilitation of small remnant habitat areas which may be overlooked in
174 Chapter 6: Discussion
conservation planning (Wintle et al. 2018). While these remnant habitat areas may have unrealised extinction debts, with careful management and restoration, these risks can be mitigated, allowing these habitats to provide conservation of biodiversity and rare and endangered species into the future
(Kuussaari et al. 2009; Wintle et al. 2018).
Through my research into pumice rafted communities, I also found trait richness changed in relation to changes in abiotic climatic conditions see
Velasquez et al. (2018) and Chapter 4. As communities were altered and habitat quality is thought to have deteriorated through time as biota was lost and pumice drifted into cooler or warmer water see Velasquez et al. (2018) and Chapter 4. This finding indicates that consideration of abiotic conditions that cause changes in temperature such as season or floating into cooler or warmer waters can alter the factors influencing marine community assembly in time and space, as predicted by the TIB.
Understanding the key drivers of community assembly in time and space is a common theme for many ecological studies, particularly because understanding of this nature may help in the restoration of degraded ecosystems in future scenarios and their ecosystem services (Cardinale et al.
2012; Fensham et al. 2015; Alexander et al. 2016). As a result, use of theories such as the TIB to increase the scientific understanding of community assembly rules has been conducted in countless studies (e.g.
Lomolino 2000; Whittaker et al. 2005; Warren et al. 2015). Despite limitations
(Gilbert 1980; Laurance 2008), this theory has been and will most likely remain relevant in modern contexts because of its simplicity (Brown &
Lomolino 2000; Lomolino 2000).
Chapter 6: Discussion 175
Appendices
Appendix A
Chapter 1. Supporting information:
Figure S1. Map detailing a) the locations of Home Reef and Havre underwater volcanoes along with general indication of pumice clast collection locations (courtesy of Associate Professor Scott Bryan); and b) the Kermadec Arc, showing the locations of underwater volcanoes including the Havre seamount (adapted from Wunderman 2012).
Appendices 177
Appendix B
Chapter 3. Supporting information: Pumice characteristics expanded
Pumice is essentially a magma foam that is rapidly chilled on eruption and ejection into the atmosphere or water which quenches the magma to glass.
The high proportion of vesicle or bubble spaces in the glass reduces its bulk density so that it is less than water, and allows the pumice stone to float in water. Many of the vesicle spaces in each pumice clast remain unconnected preventing occupation of those spaces by water aiding long-term positive buoyancy. Consequently, the combination of long-term positive buoyancy and resistance to physical/chemical degradation or biological consumption provides countless opportunities for marine epibionts to colonise pumice and undergo mass transit across deep oceans (Thiel & Haye 2006; Bravo et al.
2011).
At a macroscopic scale, pumice appears relatively homogenous. However, significant habitat heterogeneity exists in each clast. First, the foam like texture of pumice greatly increases the surface area for attachment, as well as depressions and holes that offer value as protective spaces such as for newly settled larvae (Bryan et al. 2004; Bravo et al. 2011). Second, based on the way pumice clasts float in water, many clasts are able to maintain stability in the water column with some exhibiting emergent dorsal surface or freeboard directly exposed to sunlight, and a ventral surface fully submerged and shaded (Bryan et al. 2012). Importantly, these two habitat types allow species with different requirements to populate each area, photosynthetic organisms can flourish on dorsal surfaces, and filter feeders on ventral surfaces, thereby promoting greater biodiversity on each clast (Bryan et al.
178 Appendices
2012). Differences in buoyancy (whether maintaining dorsal surface above or below the water line), available habitat space and floating stability between smaller and larger clasts may also influence patterns of species richness that assemble on the pumice casts (MacArthur & Wilson 1967; Osman 1978;
Bravo et al. 2011; Goldstein et al. 2014).
Pumice-producing eruptions can occur worldwide but occur most commonly in the South-western Pacific, with floating pumice arriving every five to ten years on the eastern Australian coastline for at least the last 200 years
(Bryan 1971; Bryan et al. 2004; Bryan et al. 2012). Each pumice clast is a self-contained fragment of pumice stone with variable size and shape. As pumice clasts float through the ocean, they are acted on by abiotic forces including temperature, wind and waves, causing altered trajectories and exposure to changes in temperature and colonising propagules. For example, the raft may remain in the deep ocean isolating it from potential colonising propagules or have close encounters with islands, reefs and other shallow marine ecosystems causing it to be bombarded by colonising populations (Jokiel 1989; Bravo et al. 2011; Bryan et al. 2012). Pumice stones may float (until inevitable stranding on shorelines or sinking due to biofouling or waterlogging) for more than two years and can travel more than
20,000 kilometres (Jokiel 1989; Risso et al. 2002; Bravo et al. 2011; Bryan et al. 2012).
Appendices 179
Appendix C Chapter 3. Supporting Information: Table S1 Pumice stranding collection field sites for both the Home and Havre events, including latitude, longitude and date of collection.
Volcano Sample site Latitude Longitude Sampling date
Home Vava’u islands Tonga 18°S 39'40.34" 174°W 3'15.79" 01/02/2007
Home Marion Reef 19˚S 05.744’ 152˚E 23.449’ 30/04/2007
Home Lamberts Beach 21˚S 04.472’ 149˚E 3.701’ 01/05/2007
Home Lady Musgrave Island 23˚S 54.461’ 152˚E 3.669’ 03/05/2007
Home Agnes Waters 24˚S 12.463’ 151˚E 54.364’ 03/05/2007
Home South Stradbroke 27˚S 49.678’ 153˚E 5.968’ 01/06/2007 Island
Home Broadbeach, Gold 28˚S 07.620’ 153˚E 26.135’ 05/05/2007; Coast, Queensland 27/12/2007; 21/01/2008
Home Duranbah 28˚S 10.005’ 153˚E 33.105’ 05/05/2007
Home Byron Bay, 28˚S 38.334’ 153˚E 37.636’ 05/05/2007 Queensland
Home Shelley Beach, Ballina 28˚S 51.598’ 153˚E 5.795’ 05/05/2007
Havre Bicheno, Waubs 41°S 52'20.11" 148°E 17'57.08" 08/04/2014; Beach, Tasmania 30/04/2014
Havre Schouten Island, 42°S 19'3.91" 148°E 18'55.74" 07/04/2014 Tasmania
Havre Scamander River 41° S 27'41.55" 148°E 15'56.84" 07/04/2014; Mouth, Tasmania 06/06/2014
Havre Flinders Island, 40°S 13'47.24" 148°E 2'23.93" 10/06/2014 Trousers Point Beach, Tasmania
Havre Flinders Island, Emita 39°S 59'55.88" 147°E 53'48.06" 21/06/2014 Foreshore, Tasmania
Havre Safety Cove, Port 43°S 9'45.85" 147°E 51'18.06" 27/06/2014 Arthur, Tasmania
Havre Vomo Island, Fiji 17°S 30'17.01" 177°E 16'1.30" 02/09/2013; 05/09/2013
180 Appendices
Volcano Sample site Latitude Longitude Sampling date
Havre Main Beach, Port 16°S 29'24.15" 145°E 27'54.06" 24/08/2013 Douglas, Queensland
Havre Lowe Isle, The Lowe 16°S 23'2.66" 145°E 33'36.60" 25/08/2013 Isles, Queensland
Havre Shoal Point Beach, 21°S 0'50.77" 149°E 9'26.45" 01/09/2013 Mackay, Queensland
Havre Main Beach, Noosa, 26°S 23’15.97” 153°E 5’16.33” 23/12/2013 Queensland
Havre Prince of Wales 10°S 42’49.40” 142°E 11’54.18” 16/09/2013 Island, Torres Strait
Havre Grassy Head Beach, 30°S 46’49.86” 152°E 59’48.97” 01/01/2014 NSW
Havre Gold Coast, Burleigh, 28°S 5’19.15” 153°E 27’12.78” 30/03/2013; Queensland 28/12/2013
Havre The Spit, Gold Coast, 27°S 56'21.53" 153°E 25'45.77" 12/12/2013 Queensland
Havre North Stradbroke 27°S 25’28.97” 153°E 32’17.20” 01/05/2013 Island, Queensland
Havre Deadman’s Beach, 27°S 25’30.60” 153°E 32’21.62” 01/05/2013; North Stradbroke 05/05/2013 Island, Queensland
Havre Frenchman’s Beach, 27°S 25’38.85” 153°E 32’35.23” 04/05/2013; North Stradbroke 02/07/2013; Island, Queensland 04/08/2013
Havre Main Beach, North 27°S 26'13.72" 153°E 32'32.17" 02/07/2013; Stradbroke Island, 04/08/2013 Queensland
Appendices 181
Appendix D Chapter 3. Supporting Information: Table S2 PERMANOVA test of differences between pumice rafted communities which formed on pumice from different events (Home versus Havre), locations, ages, sizes and climatic zones (trajectories): subtropical (n=4719), tropical (n=161) and temperate (n=70).
Comparison of Pseudo-F P Unique event, location, age, permutations area and climatic zone
Event 58.823 0.0001 9958
area (log.sphere) 28.82 0.0001 9939
area (log.sphere) x 6.551 0.0001 9940 event
age 3.9378 0.0005 9931
location (age x event 3.8539 0.0001 9826 x climatic zone)
climate 2.4565 0.0062 9935
182 Appendices
Appendix E Chapter 3. Supporting Information: Table S3 PERMDISP analysis for the Havre event and climatic zone providing a distance-based test for homogeneity of multivariate dispersions between climatic zones of tropical (n=116), subtropical (n=218) and temperate (n=70) (NB: the number of permutations was set to 9999 for all models).
Climatic zone t value P
Tropical, temperate 3.4288 0.0064
subtropical, temperate 2.5107 0.0243
subtropical, tropical 1.4796 0.187
Appendices 183
Appendix F Chapter 3. Supporting Information: Table S4 Pair-wise comparison tests of pumice rafted epibiont communities by age and separated by event.
Havre
Time of arrival (age) t value P Unique permutations compared
late, early 2.1523 0.0001 9945
late, middle 0.98867 0.4791 9953
middle, early 0.84993 0.6369 9938
Home
late, middle 2.7911 0.0001 9789
late, early 1.2514 0.4154 120
middle, early 1.0534 0.3067 9721
184 Appendices
Appendix G Chapter 3. Supporting Information: Table S5 Counts and presence data for epibiont groupings divided into respective oceanic climatic zones, combined for the two events of Home and Havre. *Despite best efforts these four epibionts were not possible to identify although they had characteristics evident of marine species and also being distinct from other biota, as such they were included in the statistical modelling completed for this paper.
Oceanic climatic zone temperate subtropical tropical Grand Total Epibiont counts of individuals per clast Lepas spp. #1 0 1098 21 1119 Lepas spp. #2 0 6 5 11 Lepas spp. #3 0 0 4 4 Lepas spp. juveniles (<0.5cm) 47 147 85 279 Acorn barnacles 11 18 7 36 Megabalanus coccopoma 6 0 0 6 Juvenile acorn barnacles 0 13 0 13 Sea anemones 1 30 3 34 Chitons 0 0 1 1 Copepod eggs (denoting presence of copepods) 29 147 39 215 Crabs 0 4 0 4 Shrimp 0 4 0 4 Bristle worms 14 45 10 69 Serpulidae type. #1 9 251 41 301 Serpulidae type. #2 8 12 7 27 Serpulidae type. #3 4 4 8 16 Nudibranchs 0 29 0 29 Amphipods and Copepods 2 57 16 75
Appendices 185
Oceanic climatic zone temperate subtropical tropical Grand Total Ostracods 0 13 0 13 Halobates spp. #1 0 23 0 23 Foram type #1 0 1 4 5 Foram type #2 0 2 47 49 Foram type #3 0 1 33 34 Foram type #4 0 3 18 21 Foram type #5 15 27 26 68 Foram type #6 0 1 11 12 Foram type #7 0 20 4 24 Foram type #8 2 68 0 70 Pteria spp. #1 1 4 3 8 Electroma spp. #1 0 11 0 11 Pinctada margaritifera 0 15 9 24 Litiopa limnophysa 8 673 28 709 Epitoniid spp. #1 0 15 0 15 Rissoidean spp. #1 0 4 0 4 Rissoidean spp. #2 0 0 1 1 Dalia spp. #1 0 1 0 1 Janthia spp. #1 0 1 0 1 Janthia spp. #2 0 1 1 2 Nerita spp. #1 0 1 0 1 Crassostrea spp. #1 0 6 1 7 Crassostrea spp. #2 0 6 0 6 Crassostrea spp. #3 0 1 0 1 Gastropod type #1 0 0 9 9
186 Appendices
Oceanic climatic zone temperate subtropical tropical Grand Total Gastropod type #2 0 0 3 3 Gastropod type #3 0 1 9 10 Gastropod type #4 0 2 9 11 Gastropod type #5 0 0 1 1 Gastropod type #6 0 1 0 1 Gastropod type #7 0 0 5 5 Gastropod type #8 3 0 0 3 Hiatella australis 0 4 4 8 Juvenile Pinctada spp. #1 0 1 6 7 Juvenile Pinctada spp. #2 0 2 0 2 Brachidontes subramosa 0 2 1 3 Anomiid spp. #1 0 3 0 3 Septifer australis 0 2 0 2 Bivavlia type #1 0 1 1 2 Bivalvia type #2 0 0 1 1 Pinctada fucata 0 0 1 1 Sponges 0 14 1 15 Pocillopora spp. #1 0 24 22 46 Acropora spp. #1 1 0 1 2 Porites lobata 1 3 0 4 Juvenile corals (<0.1mm) 0 6 1 7 Brown crustacean (no ID possible)* 1 0 0 1 Pink marine mite (no ID possible)* 0 0 1 1 Grey lifeform (whip-like) (no ID possible)* 1 2 0 3 Clear lifeform, brown margins (no ID possible)* 0 0 1 1
Appendices 187
Oceanic climatic zone temperate subtropical tropical Grand Total
Colonial epibionts - presence data per clast
Bryozoan - Jellyella spp. 65 2107 92 2264 Bryozoan - type #1 0 29 0 29 Bryozoan - type #2 0 0 13 13 Bryozoan - type #3 0 0 2 2 Bryozoan - type #4 0 0 1 1 Bryozoan - type #5 0 0 2 2 Bryozoan - type #6 0 3 0 3 Cyanobacteria - Nostocales spp. #1 70 269 116 455 Cyanobacteria - Rivularia spp. #1 61 849 65 975 Cyanobacteria - Rivularia spp. #2 0 4089 22 4111 Cyanobacteria spp. #4 0 22 0 22 Cyanobacteria - Oscillatoriales spp. #1 0 714 1 715 Caulerpa spp. #1 3 63 0 66 Caulerpa peltata 0 3 0 3 Caulerpa razemosa 0 2 0 2 Caulerpa nammularia 0 5 0 5 Sargassum spp. #2 0 0 9 9 Sargassum flavicans 0 36 0 36 Symploca spp. #1 0 6 0 6 Ceramium spp. #1 0 199 3 202 Ceramium spp. #2 0 2 2 4 Green algae spp. 1 3 0 4
188 Appendices
Oceanic climatic zone temperate subtropical tropical Grand Total Red algae spp. 1 0 0 1 Cladophora spp. #1 0 177 0 177 Chondria spp. #1 0 1 0 1 Corrallina spp. #1 0 1 0 1 Jania spp. #1 0 14 1 15 Polysiphonia spp. #1 0 28 1 29 Hypoglossum spp. #1 0 2 3 5 Callithamnion spp. #1 0 14 0 14 Colpomenia spp. #1 0 1 0 1 Enteromorpha spp. #1 0 0 1 1 Hydrozoa type #1 33 140 46 219 Hydrozoa type #2 7 225 21 253 Hydrozoa type #3 4 3 7 14 Scyphozoa spp. #1 0 3 4 7 Calcareous algae type #1 28 40 40 108 Calcareous algae type #2 30 51 59 140 Calcareous algae type #3 1 1 8 10 Calcareous algae type #4 10 50 17 77 Calcareous algae type #5 2 344 43 389 Calcareous algae type #6 1 10 0 11 Calcareous algae type #7 0 1 0 1 Calcareous algae type #8 1 0 0 1 Calcareous algae type #9 0 1434 1 1435 Calcareous algae type #10 0 22 0 22
Appendices 189
Appendix H Chapter 3. Supporting Information: Table S6 Percent dominance of major epibiont groupings for the combined events of Home and Havre, per pumice clast for the three climatic zones of subtropical (n=4719), tropical (n=161) and temperate (n=70). Epibiont grouping subtropical tropical temperate cyanobacteria total 96.9% 85.7% 100.0% bryozoan total 45.2% 64.6% 92.9% calcareous algae total 37.7% 76.4% 67.1% goose barnacle orange 23.3% 13.0% 0.0% gastropods 15.4% 33.5% 15.7% fleshy algae 10.0% 9.9% 4.3% hydroids 7.4% 37.9% 55.7% serpulid white 5.3% 25.5% 12.9% copepod eggs 3.1% 24.2% 41.4% forams 2.5% 41.0% 24.3% amphipods/copepods 1.2% 9.9% 2.9% bristle worms 1.0% 6.2% 20.0% corals 0.7% 14.9% 2.9% bryozoan (excluding jellyella) 0.7% 8.7% 0.0% anemones 0.6% 1.9% 1.4% nudibranchs 0.6% 0.0% 0.0% halobates eggs 0.5% 0.0% 0.0% sponges 0.3% 0.6% 0.0% acorn barnacles (total) 0.3% 0.0% 8.6% serpulid pink 0.3% 4.3% 11.4% goose barnacle brown 0.1% 3.1% 0.0% serpulid grey 0.1% 5.0% 5.7% crabs 0.1% 0.0% 0.0% goose barnacle purple 0.0% 2.5% 0.0% acorn barnacles (pink) 0.0% 0.0% 8.6%
190 Appendices
Appendix I Chapter 3. Supporting Information: Table S7 Percent dominance of major epibiont groupings for the combined events of Home and Havre, per pumice clast for the three climatic zones of subtropical (n=4719), tropical (n=161) and temperate (n=70). Epibiont grouping Havre Home cyanobacteria total 100.0% 96.3% bryozoan total 76.7% 43.8% calcareous algae total 59.6% 37.6% goose barnacle orange (type 1) 8.9% 23.8% gastropods 29.5% 14.8% fleshy algae 4.7% 10.4% hydroids 48.6% 5.5% serpulid white 13.6% 5.4% copepod eggs 28.3% 2.2% forams 28.5% 1.9% amphipods/copepods 6.0% 1.1% bristle worms 15.6% 0.1% corals 7.7% 0.1% bryozoan (not jellyella) 0.0% 1.0% anemones 5.0% 0.3% nudibranchs 0.0% 0.6% halobates eggs 0.0% 0.5% sponges 1.5% 0.2% acorn barnacles (total) 1.5% 0.3% serpulid pink 6.7% 0.6% goose barnacle brown (type 2) 2.7% 0.0% serpulid grey 4.0% 0.0% crabs 0.0% 0.1% goose barnacle purple (type 3) 1.0% 0.0% acorn barnacles (pink) 1.5% 0.0%
Appendices 191
Appendix J Chapter 3. Supporting Information:
Figure S2. Histogram of pumice clast sizes calculated as both a sphere and a prism.
192 Appendices
Appendix K Chapter 3. Supporting Information:
Figure S3. nMDS of pumice rafted community composition by location for two events Home (red-coloured right-hand cluster) and Havre (blue- coloured left-hand cluster).
Appendices 193
Appendix L Chapter 4: Supporting Information: Table S8 Functional trait feeding guilds for the Havre pumice raft
Common name Kingdom/ Class Order or Lowest Carni Herbi Omni Filter Graz Scav Pred Para Bore Phot Algal Phylum clade taxonomic vore vore vore er enge ator sitic r osyn sym grouping r theti biont c Chiton Mollusca Polyplacopho Neoloricata Chiton spp. √ √ ra
* Mollusca Gastropoda Caenogastrop Litiopa √ √ oda limnophysa
* Mollusca Gastropoda Hypsogastrop Rissoidae √ √ oda
Bristle worms Annelida Polychaeta Amphinomid √ √ √ ae
194 Appendices
Common name Kingdom/ Class Order or Lowest Carni Herbi Omni Filter Graz Scav Pred Para Bore Phot Algal Phylum clade taxonomic vore vore vore er enge ator sitic r osyn sym grouping r theti biont c
* Ostracod egg Arthropod Ostracoda unknown Ostracoda √ √ √ casings a
Mollusca Gastropoda Caenogastrop Naticidae √ √ √ oda
Violet snails Mollusca Gastropoda Caenogastrop Janthinidae √ √ oda
Serpulid worms Annelida Polychaeta Serpulidae Possible √ √ (with calcareous Hydroides tube) spp. and Spirobranch us spp.
* Goose barnacles Arthropod Maxillopoda Pedunculata Lepas spp. √ √ a
Appendices 195
Common name Kingdom/ Class Order or Lowest Carni Herbi Omni Filter Graz Scav Pred Para Bore Phot Algal Phylum clade taxonomic vore vore vore er enge ator sitic r osyn sym grouping r theti biont c
* Acorn barnacles Arthropod Maxillopoda Sessilia Sessilia √ √ (general) a
Titan acorn Arthropod Maxillopoda Sessilia Megabalanu √ √ barnacle a s coccopoma
Copepod/Amphipod Arthropod Malacostraca Amphipoda & Amphipoda √ √ √ a Isopoda & Isopoda
* Lace coral Bryozoa Gymnolaema Cheilostomata Malacosteg √ √ ta a
196 Appendices
Common name Kingdom/ Class Order or Lowest Carni Herbi Omni Filter Graz Scav Pred Para Bore Phot Algal Phylum clade taxonomic vore vore vore er enge ator sitic r osyn sym grouping r theti biont c Seaweed Chlorophy Ulvophyceae Ulvales Enteromorp √ ta ha spp.
Coral Cnidaria Anthozoa Scleractinia Porites √ √ √ lobata
Coral Cnidaria Anthozoa Scleractinia Pocillopora √ √ √ spp.
Coral Cnidaria Anthozoa Scleractinia Acropora √ √ √ spp.
Sea firs Cnidaria Hydrozoa Leptomedusa Leptomedus √ √ e ae
Appendices 197
Common name Kingdom/ Class Order or Lowest Carni Herbi Omni Filter Graz Scav Pred Para Bore Phot Algal Phylum clade taxonomic vore vore vore er enge ator sitic r osyn sym grouping r theti biont c Sea anemones Cnidaria Anthozoa Actiniaria* Calliactis √ √ √ polypus
Cyanobacteria Cyanobact Nostocales Rivularia √ eria spp. and some others
Seaweed Eukaryota Florideophyc Ceramiales Ceramium √ eae spp.
Forams Foraminife Unknown Unknown Foraminifer √ √ √ ra a
Black-lip pearl Mollusca Bivalvia Pterioida Pinctada √ √ oyster margaritifer a
Akoya pearl oyster Mollusca Bivalvia Pterioida Pinctada √ √ fucata
198 Appendices
Common name Kingdom/ Class Order or Lowest Carni Herbi Omni Filter Graz Scav Pred Para Bore Phot Algal Phylum clade taxonomic vore vore vore er enge ator sitic r osyn sym grouping r theti biont c Deck mussel Mollusca Bivalvia Mytiloida Septifer √ √ australis
* Australian Rock Mollusca Bivalvia Veneroida Hiatella √ √ Borer australis
Mollusca Gastropoda Electroma √ √ spp.
Mollusca Bivalvia Mytiloida Brachidonte √ √ s subramosus
Seaweed Ochrophyt Phaeophycea Fucales Sargassum √ a e
Sponges Porifera Porifera √ √
*
Appendices 199
Common name Kingdom/ Class Order or Lowest Carni Herbi Omni Filter Graz Scav Pred Para Bore Phot Algal Phylum clade taxonomic vore vore vore er enge ator sitic r osyn sym grouping r theti biont c Calcareous algae Rhodophy Florideophyc Corallinales Coralineace √ ta eae a
200 Appendices
Table S9 Functional trait reproductive guilds for the Havre pumice raft
Common name Kingdom/ Class Order or clade Lowest Asexu Sexua Dioeci Prota Simult Spaw Brood Fragm Motile Telepl Phylum taxonomic al l ous ndrou aneou ning er enter larvae anic grouping s s larvae herma herma phrodi phrodi te te Chiton Mollusca Polypl Neoloricata Chiton spp. √ √ √ √ √ √ acoph ora
* Mollusca Gastro Caenogastropoda Litiopa √ √ √ poda limnophysa
* Mollusca Gastro Hypsogastropoda Rissoidae √ √ √ poda
Bristle worms Annelida Polych Amphinomi √ √ √ √ √ √ √ aeta dae
* Ostracod egg Arthropod Ostrac unknown Ostracoda √ √ √ √ casings a oda
Appendices 201
Common name Kingdom/ Class Order or clade Lowest Asexu Sexua Dioeci Prota Simult Spaw Brood Fragm Motile Telepl Phylum taxonomic al l ous ndrou aneou ning er enter larvae anic grouping s s larvae herma herma phrodi phrodi te te Mollusca Gastro Caenogastropoda Naticidae √ √ √ √ √ √ poda
Violet snails Mollusca Gastro Caenogastropoda Janthinidae √ √ √ √ √ √ poda
Serpulid worms Annelida Polych Serpulidae Possible √ √ √ √ √ √ √ (with calcareous aeta Hydroides tube) spp. and Spirobranch us spp.
* Goose barnacles Arthropod Maxill Pedunculata Lepas spp. √ √ a opoda
* Acorn barnacles Arthropod Maxill Sessilia Sessilia √ √ √ (general) a opoda
202 Appendices
Common name Kingdom/ Class Order or clade Lowest Asexu Sexua Dioeci Prota Simult Spaw Brood Fragm Motile Telepl Phylum taxonomic al l ous ndrou aneou ning er enter larvae anic grouping s s larvae herma herma phrodi phrodi te te Titan acorn Arthropod Maxill Sessilia Megabalan √ √ √ barnacle a opoda us coccopoma
Copepod/Amphipo Arthropod Malac Amphipoda & Amphipoda √ √ √ d a ostrac Isopoda & isopoda a
* Lace coral Bryozoa Gymn Cheilostomata Malacosteg √ √ √ √ olaem a ata Seaweed Chlorophy Ulvop Ulvales Enteromorp √ √ √ √ √ ta hycea ha spp. e
Coral Cnidaria Antho Scleractinia Porites √ √ √ √ zoa lobata
Appendices 203
Common name Kingdom/ Class Order or clade Lowest Asexu Sexua Dioeci Prota Simult Spaw Brood Fragm Motile Telepl Phylum taxonomic al l ous ndrou aneou ning er enter larvae anic grouping s s larvae herma herma phrodi phrodi te te Coral Cnidaria Antho Scleractinia Pocillopora √ √ √ √ √ √ √ zoa spp.
Coral Cnidaria Antho Scleractinia Acropora √ √ √ √ √ √ zoa spp.
Sea Firs Cnidaria Hydro Leptomedusae Leptomedu √ √ √ √ zoa sae
Sea Anemones Cnidaria Antho Actiniaria* Calliactis √ √ √ √ √ √ √ zoa polypus
* Cyanobacteria Cyanobac Nostocales Rivularia √ √ √ teria spp. and some others
204 Appendices
Common name Kingdom/ Class Order or clade Lowest Asexu Sexua Dioeci Prota Simult Spaw Brood Fragm Motile Telepl Phylum taxonomic al l ous ndrou aneou ning er enter larvae anic grouping s s larvae herma herma phrodi phrodi te te Seaweed Eukaryota Florid Ceramiales Ceramium √ √ √ √ eophy spp. ceae Forams Foraminif Unkno Unknown Foraminifer √ era wn a
Black-lip pearl Mollusca Bivalvi Pterioida Pinctada √ √ √ √ oyster a margaritifer a
Akoya pearl oyster Mollusca Bivalvi Pterioida Pinctada √ √ √ √ a fucata
Deck mussel Mollusca Bivalvi Mytiloida Septifer √ √ √ √ a australis
* Australian rock Mollusca Bivalvi Veneroida Hiatella √ √ √ √ borer a australis
Appendices 205
Common name Kingdom/ Class Order or clade Lowest Asexu Sexua Dioeci Prota Simult Spaw Brood Fragm Motile Telepl Phylum taxonomic al l ous ndrou aneou ning er enter larvae anic grouping s s larvae herma herma phrodi phrodi te te Mollusca Gastro Electroma √ √ √ poda spp.
Mollusca Bivalvi Mytiloida Brachidonte √ √ √ √ a s subramosus
Seaweed Ochrophyt Phaeo Fucales Sargassum √ √ √ √ a phyce ae Sponges Porifera Porifera √ √ √
* Calcareous algae Rhodophy Florid Corallinales Coralinnine √ √ √ √ ta eophy acea ceae
*Images courtesy of Denis Reik
206 Appendices
Appendix M Table S10. Results of model comparison using Akaikie information criterion (AICc) values to identify factors explaining variations in functional trait richness for separate feeding and reproductive trait modalities found on Havre pumice rafts in relation to the fixed effects of age and habitat area and separated into climatic zones (where sth = subtropical, t = tropical and ct = temperate stranding locations). Most of these models were run using a binomial distribution; where this was not the best fit, a normal distribution was used.
Trait modality Climatic zone Effect df logLik AICc Delta Weight Binomial or normal distribution Full or reduced model
Carnivore Cool temperate age 5 -26.9 64.7 0.0 0.6 binomial F area 6 -26.2 65.7 0.9 0.4 age x area 4 -30.3 69.1 4.4 0.1 subtropical age 5 -84.3 178.8 0.0 0.4 binomial F area 6 -83.6 179.7 0.8 0.3 age x area 4 -86 180.1 1.3 0.2 tropical null model* binomial F herbivore cool temperate age 6 -20.8 55 0.0 0.4 binomial F area 4 -23.2 55.1 0.1 0.4 age x area 5 -22.7 56.4 1.4 0.2 subtropical age 4 -79.0 166.2 0.0 0.6 binomial F area 5 -78.8 167.9 1.7 0.3 age x area 6 -78.7 169.9 3.7 0.1 tropical null model* binomial F omnivore cool temperate** age 6 -120 253.3 0.00 0.6 normal F area 5 -122.2 255.4 2.0 0.2 age x area 7 -119.9 255.7 2.4 0.2 subtropical age 7 -407.4 829.3 0.0 1 normal F
Appendices 207
Trait modality Climatic zone Effect df logLik AICc Delta Weight Binomial or normal distribution Full or reduced model
area 6 -413.7 839.8 10.5 0.0
tropical age 7 -256.8 528.7 0.0 0.8 normal F area 6 -259.5 531.8 3.1 0.2
algal symbiont cool temperate null model* binomial F subtropical null model* binomial F tropical null model* binomial F filter feeder cool temperate** age 6 -20.8 54.9 5 0.0 0.4 binomial F area 4 -23.2 55.1 0.1 0.4 age x area 5 -22.7 56.36 1.4 0.2 subtropical age 5 -64.1 138.6 0.0 0.5 normal F area 6 -63.4 139.3 0.7 0.4
age x area 4 -66.9 141.9 3.4 0.1 tropical null model* binomial F grazer cool temperate age 6 -55 0.0 20.8 0.4 binomial F area 4 -55.1 23.2 0.1 0.4
208 Appendices
Trait modality Climatic zone Effect df logLik AICc Delta Weight Binomial or normal distribution Full or reduced model
age x area 5 -22.7 56.4 1.4 0.2 subtropical age 4 -79.0 166.2 0.0 0.6 binomial F area 5 -78.8 167.9 1.7 0.3 age x area 6 -78.7 169.9 3.7 0.1 tropical null model*
scavenger cool temperate age 5 -26.9 64.7 0.0 0.6 binomial F area 6 -26.2 65.7 0.9 0.4 age x area 4 -30.3 69.1 4.4 0.1 subtropical null model* binomial F
tropical null model* binomial F predator cool temperate age 5 -28.7 68.3 0.0 0.5 binomial F area 6 -27.9 69.2 0.9 0.3 age x area 4 -31.6 71.7 3.4 0.1 subtropical age 6 -82.7 177.8 0.0 0.7 binomial F area 5 -84.8 179.9 2.2 0.2 age x area 4 -87.2 182.5 4.7 0.1 tropical null model* binomial F photosynthetic cool temperate** age 7 -85.2 186.1 60.0 0.7 normal F area 5 -89.7 190.4 4.3 0.1
Appendices 209
Trait modality Climatic zone Effect df logLik AICc Delta Weight Binomial or normal distribution Full or reduced model
age x area 6 192.7 8 6.6 0.0 subtropical age 7 -297.8 610.1 0.0 1 normal F area 6 -302.0 616.4 6.3 0.0 tropical neither binomial or normal distribution fit the data – so models discarded
asexual cool temperate** age 7 -131.7 279.3 0.0 0.9 normal F area 6 -135.3 283.9 4.6 0.1 age x area 5 -138.3 287.6 8.3 0.0 subtropical null model* binomial F tropical neither binomial or normal distribution fit the data – so models discarded sexual cool temperate age 6 -132.7 278.8 0.0 0.4 normal F area 7 -131.6 279 0.2 0.4 age x area 5 -134.9 280. 8 2.0 0.2 subtropical age 7 -458.8 932.2 0.0 1 normal F
tropical age 6 -255.8 524.4 0.0 0.6 normal F area 7 -255.4 525.9 1.5 0.3 age x area 5 -258.1 526.8 2.5 0.2 dioecious cool temperate null model* binomial F subtropical age 6 -99.6 211.5 0.0 0.6 binomial F area 4 -102.5 213.3 1.7 0.2
210 Appendices
Trait modality Climatic zone Effect df logLik AICc Delta Weight Binomial or normal distribution Full or reduced model
age x area 5 -101.5 213.4 1.9 0.2 tropical null model* binomial F protandrous hermaphrodite cool temperate null model* binomial F
subtropical age 6 -97.3 207 0.0 0.6 binomial F area 5 -99.1 208.4 1.4 0.3 age x area 4 -101.1 210.4 3.4 0.1
tropical area 4 -36.7 81.8 0.0 0.6 binomial F age 5 -36.4 83.3 1.5 0.3 age x area 6 -36.1 85.0 3.2 0.1 simultaneous hermaphrodite cool temperate null model* binomial F subtropical area 4 -95.3 198.8 0.0 0.5 binomial F age 5 -95 200.3 1.5 0.3 age x area 6 -94.2 200.8 2.0 0.2 tropical area 4 -60.0 128.4 0.0 0.5 binomial F age 5 -59.6 129.8 1.4 0.3 age x area 6 -58.7 130.2 1.9 0.2 spawner cool temperate null model* binomial F
Appendices 211
Trait modality Climatic zone Effect df logLik AICc Delta Weight Binomial or normal distribution Full or reduced model
subtropical age 5 -84.1 178.5 0.0 0.5 binomial F area 6 -83.1 178.6 0.1 0.5 age x area 4 -86.7 181.6 3.0 0.1 tropical age 4 -52.3 113.0 0 1 binomial F fragmenter cool temperate** age 7 -87.4 190.7 0.0 0.5 normal F area 5 -90.3 191.6 0.9 0.3 age x area 6 -90.2 193.7 3.0 0.1 subtropical null model* binomial F tropical null model* normal F
motile larvae cool temperate** neither binomial or normal distribution fit the data – so models discarded
subtropical age 5 -64.5 139.3 0.0 0.5 binomial F area 6 -63.6 139.6 0.3 0.4
age x area 4 -67.0 142.2 2.9 0.1 tropical age 4 -26.7 61.7 0.0 0.4 binomial F area 5 -25.9 62.3 0.6 0.3
212 Appendices
Trait modality Climatic zone Effect df logLik AICc Delta Weight Binomial or normal distribution Full or reduced model
age x area 6 -25.4 63.6 1.9 0.2 *A null model is where the random effects (location of pumice clast collection and date of collection) explained the data to the same degree as the fixed effects (age and area).
Appendices 213
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