Whole Azorean arthropod diversity:

understanding the trophic relations and

functional diversity at a plot scale

Tese de Doutoramento

Rui Miguel Ricardo Nunes

O R A S CIE N
TI
UR A
A

LU
T
SIC U

CET
U NI V

ES

Doutoramento em
OR

Gestão Interdisciplinar da Paisagem

ER

SI
Ç

DA A
DE DOS

Angra do Heroísmo
2017
Whole Azorean arthropod diversity:
understanding the trophic relations and
functional diversity at a plot scale

Tese de Doutoramento

Rui Miguel Ricardo Nunes

Orientadores
Professor Doutor Paulo Alexandre Vieira
Professor Doutor Pedro Miguel Cardoso
Professor Doutor António Onofre Costa Miranda Soares

Tese de Doutoramento submetida como requisito parcial para obtenção do grau de doutoramento em
Gestão Interdisciplinar da Paisagem.
“The Road goes ever on and on
Down from the door where it began.
Now far ahead the Road has gone,
And I must follow, if I can,
Pursuing it with eager feet,
Until it joins some larger way,
Where many paths and errands meet.
And whither then? I cannot say. "

J.R.R. Tolkien, The Lord of the Rings

 Abstract
Island ecosystems are home to a disproportionate amount of unique floristic and faunistic
diversity, but conversely, islands also host some of the most imperiled habitats and species on Earth.
These island communities are in many cases extremely vulnerable to anthropogenic habitat
disturbance and destruction, and to the introduction of exotic species. Most of the island terrestrial
biodiversity is composed by arthropods, but the processes that structure their communities are still
poorly understood. In order to preserve what is left of these unique insular biotas, our current
knowledge regarding species, communities and habitats, and recovery processes under disturbance
must be expanded, and new possibilities for conservation must be also evaluated.

Taking advantage of the unique characteristics of the canopy fogging (pyrethrum

knockdown) sampling protocols, this thesis investigates for the first time in the Azores archipelago
the impact of defaunation on the reassembly of canopy arthropod communities. A total of 24 native
trees were sampled with insecticidal knockdown in 2014 and 2015, in a native forest patch on
Terceira Island. Between 2015 and 2016 this same protocol was applied to five isolated Azorean
cedar trees on a semi-natural pasture. Regarding the defaunation and recovery processes, changes in
taxonomic (TD) and functional diversity (FD) for the initial communities for the control trees and for
those of the recolonised trees were also investigated and null models created, to ascertain how these
communities differed from randomly assembled ones.

The main objectives of this thesis were: 1) take advantage of the canopy fogging technique
to do an exhaustive quantitative and qualitative study of the arthropod communities present in the
canopies of three native Azorean tree species (Juniperus brevifolia, Ilex perado subs azorica, Laurus
azorica); 2) to study the recovery processes of these communities after the defaunation of the
canopies; 3) to study the arthropod communities present in the canopies of the isolated pasture trees,
evaluating their role as repositories of indigenous fauna and as an element in the interconnection
between extant native forest patches.

In the forest experiment, a total of 21275 arthropod specimens belonging to 75 species were
collected. The community was in general dominated by some highly abundant endemic and to a
certain extent native species. Most exotic species were locally rare, and most likely vagrants. Host
tree species seemed to be of secondary importance in structuring the highly generalist arthropod
community. Regarding functional diversity, there was no apparent saturation of functional trait-
space.

i
 Recolonisation of the defaunated trees was fast and complete, with the recovered arthropod
community being similar to both the initial community or that of the control trees, particularly for
endemic species. In general, functional and taxonomic diversity remained fairly unaltered both in the
initial and recolonised communities and in the control trees. The recovered community also had a
relatively lower proportion of exotic species, also observed as a decreased in both TD and FD for this
group. Recolonisation and recovery seemed to be largely influenced by the structure of the canopies,
the high level of interconnectedness of the canopies and the existing pool of highly abundant
indigenous species. Also observed was that in general these communities had lower values of TD and
FD than what would be expected by random assembly, most likely consequence of a filtering effect
by the structure of the canopies, possibly allied with the fact that the indigenous Azorean fauna is
somewhat depauperate.

In the pasture experiment, a total of 8056 specimens belonging to 58 species were collected.
These communities still retained a high degree of similarity with the forest communities, reinforcing
both the importance of the characteristics of the canopies in structuring the communities and the role
of these trees as repositories of indigenous species. As with the forest communities there was no
apparent saturation of functional trait space. These communities were nevertheless less resilient to
the defaunation events, with the recovered community presenting an increase in the abundance of
native specimens but a decrease in endemics, while simultaneously attracting a higher number of
exotic vagrants. This was also mimicked by a decrease in TD and FD for the endemic species in the
recolonised community, while exotic species had a considerable increase for these parameters. In
these isolated trees, native species seemed to assemble in a random way, while exotic species, which
were apparently suppressed in the initial communities, assembled indistinguishably from a null
community in the recolonised trees.

Overall, this study seems to indicate that the indigenous canopy arthropod communities of
Terceira retain a high degree of resilience towards disturbances and invasion by introduced arthropod
species, in part due to the filtering effect exerted by the structure and characteristics of the canopies.

It also highlights the importance of isolated trees in pasture, and should also have some
future implications on the habitat management and conservation strategies of the increasingly
fragmented forests in the Azores.

Keywords: pyrethrum knockdown, arthropod communities, Macaronesia, community recovery,

canopy arthropods.

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 Resumo
Os ecossistemas insulares albergam uma diversidade faunística e florística únicas e muito
elevada proporcionalmente quando comparada com zonas continentais. No entanto, é também nas
ilhas onde se encontram alguns dos habitats e espécies mais vulneráveis do planeta. Estas
comunidades insulares são em muitos casos extremamente vulneráveis a perturbações
antropogénicas e à destruição dos habitats, bem como à introdução de espécies exóticas. A maioria
da biodiversidade insular terrestre é composta por artrópodes, mas existem ainda diversas lacunas no
conhecimento sobre os processos que estruturam essas comunidades. Assim, de modo a poder
preservar o que ainda resta destes biotas insulares únicos, o nosso conhecimento acerca destas
espécies, das comunidades e dos habitats, bem como dos processos de recuperação após perturbações
têm que ser expandidos e novas alternativas para a conservação devem também ser avaliadas.

Tomando partido das características únicas da amostragem por fumigação com insecticida
das copas, esta tese propõe-se a investigar pela primeira vez nos Açores o impacto da defaunação e a
recuperação das comunidades de artrópodes das copas. Entre 2014 e 2015 foram amostradas através
de fumigação térmica com insecticidas um total de 24 árvores nativas das espécies Juniperus
brevifolia, Ilex perado subs azorica e Laurus azorica, num fragmento de floresta nativa da Terceira.
Em 2014 foram amostradas 16, das quais 15 voltaram a ser amostradas em 2015, em conjunto com
outras oito árvores, fumigadas pela primeira vez, como controlo. Entre 2015 e 2016 o mesmo
protocolo de amostragem foi aplicado a cinco exemplares de Cedro do mato (Juniperus brevifolia),
isolado numa pastagem semi-natural. Três arvores foram fumigadas pela primeira vez em 2015,
tendo voltado a ser amostradas em 2016, em conjunto com mais duas árvores controlo. No que diz
respeito à defaunação e processos de recuperação das comunidades, alterações a nível da diversidade
taxonómica (DT) e funcional (DF) foram investigadas para as comunidades iniciais, para as
comunidades das árvores controlo e para as comunidades das árvores recolonizadas (as árvores
fumigadas pela segunda vez, no ano seguinte). Foram também criados modelos nulos, de forma a
tentar perceber como estas comunidades diferem de comunidades estabelecidas ao acaso.

Os principais objectivos desta tese são então: 1) tomar partido das características da técnica
de fumigação das copas para fazer um estudo quantitativo e qualitativo exaustivo das comunidades
de artrópodes presentes nas copas de três espécies de árvores nativas dos Açores (Juniperus
brevifolia, Ilex perado subs azorica, Laurus azorica); 2) estudar os processos de recuperação destas
comunidades após a defaunação das copas; 3) estudar as comunidades de artrópodes presentes nas
copas de árvores nativas isoladas em pastagens, e simultaneamente avaliar o papel/potencial destas

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árvores como repositórios de espécies indígenas de artrópodes e como elemento de interligação entre
os fragmentos existentes de floresta nativa.

Na experiência da floresta, foram capturados um total de 21275 exemplares de artrópodes,

pertencentes a 75 espécies. A comunidade é, em geral, dominada por algumas espécies endémicas
extremamente abundantes, e em certa medida, também por algumas espécies nativas. A maioria das
espécies exóticas é localmente rara e o mais provável será serem indivíduos errantes. A espécie de
árvores hospedeira aparenta ter uma importância secundária na estruturação da comunidade
constituída maioritariamente por espécies generalistas. No que diz respeito à diversidade funcional,
não há uma aparente saturação do “espaço funcional”.

A recolonização das árvores fumigadas e a recuperação das comunidades foi rápida e total,
sendo a comunidade presente nestas árvores similar à comunidade inicial e à comunidade das árvores
controlo, especialmente no que diz respeito às espécies endémicas. No geral, a diversidade
taxonómica e a diversidade funcional mantiveram-se relativamente inalteradas entre a comunidade
inicial, a comunidade das árvores recolonizadas e a das árvores controlo. A comunidade
reestabelecida apresentou também uma proporção relativamente menor de espécies exóticas,
corroborado pelo decréscimo a nível de DT e DF para este subgrupo da comunidade. A recolonização
das árvores e a recuperação da comunidade parecem ter sido em grande parte influenciadas pela
estrutura das copas, pelo elevado nível de interligação destas e pelo pool de espécies imediatamente
presente, composto maioritariamente por espécies endémicas e nativas de elevada abundância. Foi
também observado que, em geral, estas comunidades possuem valores de DT e DF mais baixos do
que o que seria de esperar se fossem estabelecidas ao acaso, muito possivelmente uma consequência
de um efeito de filtro causado pela estrutura das copas, eventualmente aliado ao facto de a actual
fauna indígena dos Açores ser algo depauperada.

Na experiência da pastagem, foram recolhidos um total de 8056 exemplares de artrópodes,

pertencentes a 58 espécies. Estas comunidades das copas dos cedros de pastagem retêm ainda um
elevado grau de similaridade com as dos cedros da floresta, reforçando quer a importância das
características das copas na estruturação das comunidades de artrópodes, quer o papel destas árvores
como repositório de espécies indígenas. Tal como no caso das comunidades da floresta, não foi
aparente uma saturação do “espaço funcional”. No entanto, estas comunidades das arvores de
pastagem demonstraram ser menos resilientes ao episódio de defaunação, já que a comunidade
reestabelecida apresentou um aumento na abundância de exemplares de espécies nativas,
acompanhado por um decréscimo no que diz respeito a exemplares de espécies endémicas.
Simultaneamente, houve também um aumento no número de espécies exóticas nestas novas

iv
comunidades. Estas alterações nas comunidades reestabelecidas foram acompanhadas por um
decréscimo a nível de DT e DF para as espécies endémicas, e por um aumento considerável destes
parâmetros no que diz respeito às espécies exóticas. Nestas árvores isoladas, as espécies aparentam
estabelecer-se de forma mais ou menos aleatória, ao passo que as espécies exóticas, aparentemente
suprimidas nas comunidades iniciais, após a defaunação recolonizaram as árvores e estabeleceram-se
nas copas de forma indistinguível do que seria de esperar de uma comunidade nula.

No geral, este estudo indica que as comunidades de artrópodes das copas indígenas da
Terceira retêm um elevado grau de resiliência no que diz respeito a perturbações localizadas e a
invasão por parte de espécies exóticas, em parte consequência do efeito de filtro exercido pela
estrutura e características bióticas e abióticas das copas.

Este estudo realça também a importância de arvores nativas, isoladas em pastagem, como
repositórios de fauna e como elementos de interligação, devendo ter implicações para as futuras
estratégias de gestão ambiental e conservação das cada vez mais fragmentadas florestas nativas dos
Açores, bem como no desenvolvimento sustentável da região.

Palavras-chave: comunidades de artrópodes, artrópodes arbóreos, recuperação de comunidade,

Macaronésia, fumigação com piretrinas.

v
Acknowledgments
To my parents

I would like to dedicate this work to my parents. For all their unconditional love and support,
even when that meant having to see me leave again to a far away place, in this case, one of nine
green islands in the middle of the Atlantic Ocean. The same could be said for the rest of my family,
for whom I am so grateful for their love.

This work is also dedicated to the memory of two of the persons that I loved the most in this
world and that passed away during the completion of this work, my grandfathers; Mário Abrantes
Simões Ricardo and Américo Nunes. I regret the distance that prevented me from being able to spend
more time with them, and not being able to see them again, for I still had much to learn from them.

But they live on, for one only dies when it passes from the memories of those that loved
them.

I would also like to thank my friends, both those that I had to leave behind and those that I
made since moving into these islands. I will not name any of you, for you know who you are.

And now I want to thank all those without whom this work would not be possible:

My supervisors, Paulo Borges, António O. Soares and Pedro Cardoso. For their support, for
their patience, for all that I learned from them and for accepting my ideas and stubbornness. For that
I am grateful. To Rosalina Gabriel, Isabel Amorim and François Rigal, for their advice; to Rui Elias
for his advice regarding the native vegetation of the Azores and help with the tree measurements; to
Fernando Pereira (Pardal), a well of dubious humour and sound knowledge regarding the nature of
the Azores; and to Enésima Mendonça, our “mum”, without whom the Azorean Biodiversity Group
would grind to a halt. I must also thank Enésima for the priceless help in organizing the bibliography
and typesetting, together with Celia Lopez and Reinaldo Pimentel. I also wish to thank PestControl,
in the persons of Márcio Cabral and particularly José Serpa, the owner of the thermal fogger, who so
generously lent me the machine for the duration of my fieldwork, and to whom I am greatly
indebted.

A big thank you is also due to those colleagues and interns who helped me in the fieldwork
and in the tedious and never ending task of sorting the arthropod samples. By no particular order:
Lucia Vita-Sastre, Marija Tomasic, Ernö Gergelly, Francisco Presas, Laura Gallardo, Rui Carvalho,
Sofia Terzopoulou, Oscar Garcia, Lucas Lamelas-López, Celia López, Jack Lamb, Will Razey, and

vi
my “spanish angels”, Alejandra Ros Prieto and Helena Marugan. A special mention must also be
made to my supervisor Paulo Borges, for his help in the identification of the specimens.

I would also wish to thank the University of the Azores, Faculdade de Ciências Agrárias e
Engenharia do Ambiente and the Azorean Biodiversity Group for their facilities and equipment.

This work was funded by Fundo Regional para a Ciência – Programa de Bolsas de
Investigação under the grant: M3.1.2/F/035/2011

Any flaws with this work are mine alone and not theirs.

To all, a big thank you.

vii
 Table of contents
ABSTRACT ...................................................................................................................................................................... I

RESUMO ...................................................................................................................................................................... III

TABLE OF CONTENTS .................................................................................................................................................. VIII

TABLE OF FIGURES ........................................................................................................................................................ X

TABLE OF TABLES ....................................................................................................................................................... XIV

CHAPTER 1 GENERAL INTRODUCTION ...................................................................................................................... 1

1.1. CURRENT ARTHROPOD KNOWLEDGE IN THE AZORES ....................................................................................................... 1
CHAPTER 2 MATERIAL AND METHODS ..................................................................................................................... 8
2.1. THE AZOREAN ARCHIPELAGO: GEOGRAPHY AND CLIMATE ................................................................................................ 8
2.2. THE TERRESTRIAL AZOREAN BIODIVERSITY .................................................................................................................... 9
2.3. THE AZOREAN VEGETATION ..................................................................................................................................... 10
2.4. THE HOST-TREE SPECIES:......................................................................................................................................... 11
2.4.1. Juniperus brevifolia (Seub.) Antoine............................................................................................................ 11
2.4.2. Ilex perado Aiton subsp. azorica (Loes.) Tutin ............................................................................................. 13
2.4.3. Laurus azorica (Seub.) Franco ...................................................................................................................... 14
2.5. THE TERCEIRA ISLAND............................................................................................................................................ 14
2.5.1. Terra-Brava study plot ................................................................................................................................. 17
2.5.2. Tree individual’s selection (Native forest) .................................................................................................... 17
2.5.3. Semi-natural pasture study site ................................................................................................................... 21
2.5.4. Tree selection (semi-natural pasture) .......................................................................................................... 22
2.6. CANOPY FOGGING – BRIEF HISTORY AND SUITABILITY OF THE METHOD ............................................................................. 23
2.7. MATERIAL/EQUIPMENT .......................................................................................................................................... 25
2.7.1. Fogger ......................................................................................................................................................... 26
2.7.2. The insecticide ............................................................................................................................................. 27
2.7.3. The collection funnels and bottles ............................................................................................................... 29
2.8. CANOPY FOGGING SAMPLING PROTOCOL ................................................................................................................... 30
2.8.1. Arthropod species identification ................................................................................................................. 33
2.8.2. Data analysis ............................................................................................................................................... 34
CHAPTER 3 REVISION OF AZOREAN CANOPY ARTHROPODS IN NATIVE TREE SPECIES .............................................36
3.1. INTRODUCTION..................................................................................................................................................... 36
3.2. METHODS ........................................................................................................................................................... 37
3.2.1. Location....................................................................................................................................................... 37
3.2.2. Data sets and sampling ............................................................................................................................... 37
3.2.3. Data analyses .............................................................................................................................................. 38
3.3. RESULTS .............................................................................................................................................................. 40
3.4. DISCUSSION ......................................................................................................................................................... 48
CHAPTER 4 CHARACTERIZATION OF THE CANOPY ARTHROPOD FAUNA OF A NATIVE AZOREAN FOREST BY CANOPY
FOGGING 52
4.1. INTRODUCTION..................................................................................................................................................... 52
4.2. METHODS ........................................................................................................................................................... 53
4.2.1. Study site ..................................................................................................................................................... 53
4.2.2. Arthropod dataset ....................................................................................................................................... 53
4.2.3. Data analysis ............................................................................................................................................... 54
4.3. RESULTS .............................................................................................................................................................. 55

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 4.3.1. Abundance patterns .................................................................................................................................... 55
4.3.2. Diversity patterns ........................................................................................................................................ 58
4.3.3. Colonisation status patterns ....................................................................................................................... 60
4.3.4. Indicator species.......................................................................................................................................... 62
4.3.5. Trophic groups patterns .............................................................................................................................. 62
4.3.6. Patterns on species relative abundances .................................................................................................... 63
4.3.7. Patterns in species composition .................................................................................................................. 66
4.4. DISCUSSION ......................................................................................................................................................... 68
4.4.1. Trophic guilds, Araneae and Lepidoptera .................................................................................................... 72
4.4.2. Differences in species composition between trees ...................................................................................... 73
CHAPTER 5 ARTHROPOD RECOLONIZATION PROCESSES IN THE NATIVE FOREST CANOPIES .....................................76
5.1. INTRODUCTION..................................................................................................................................................... 76
5.2. METHODS ........................................................................................................................................................... 79
5.2.1. Study site ..................................................................................................................................................... 79
5.2.2. Data collection ............................................................................................................................................ 79
5.2.3. Arthropod dataset ....................................................................................................................................... 79
5.2.4. Data analysis ............................................................................................................................................... 79
5.3. RESULTS .............................................................................................................................................................. 81
5.4. DISCUSSION ......................................................................................................................................................... 94
CHAPTER 6 ISOLATED AZOREAN CEDAR TREES IN A SEMI-NATURAL PASTURE OF TERCEIRA ....................................98
6.1. METHODS ......................................................................................................................................................... 101
6.1.1. Study site ................................................................................................................................................... 101
6.1.2. Data collection .......................................................................................................................................... 101
6.1.3. Arthropod dataset ..................................................................................................................................... 102
6.1.4. Data analysis ............................................................................................................................................. 103
6.2. RESULTS ............................................................................................................................................................ 104
6.2.1. Forest vs. Pasture cedar trees .................................................................................................................... 105
6.2.2. Recolonization in pasture cedars ............................................................................................................... 111
6.3. DISCUSSION ....................................................................................................................................................... 123
6.3.1. Forest vs. Pasture cedar trees .................................................................................................................... 123
6.3.2. Canopy arthropod recolonization in isolated pasture trees....................................................................... 125
CHAPTER 7 GENERAL CONCLUSIONS .....................................................................................................................129

BIBLIOGRAPHIC REFERENCES .....................................................................................................................................132

APPENDIX I LIST OF ARTHROPOD SPECIES COLLECTED BY CANOPY FOGGING IN THE NATIVE FOREST IN THE YEARS OF
2014 AND 2015. ......................................................................................................................................................... 153

APPENDIX II INDVAL SUMMARY TABLE FROM BALA .................................................................................................. 156

APPENDIX III ..............................................................................................................................................................158

APPENDIX IV .............................................................................................................................................................. 159

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 Table of figures
FIGURE 2-1 MAP OF THE AZORES, WITH TERCEIRA ISLAND SINGLED OUT. INSET WITH THE LOCATION OF THE ARCHIPELAGO
IN THE ATLANTIC OCEAN. ...................................................................................................................... 8

FIGURE 2-2 MAP OF TERCEIRA ISLAND, WITH ITS DIFFERENT NATURE RESERVES, PROTECTED AREAS AND NATURAL
MONUMENTS. TERRA-BRAVA NATURE RESERVE MARKED WITH A RED ARROW (SOURCE: DROTRH 2008). ........ 15

FIGURE 2-3 AVERAGE MONTHLY TEMPERATURES, AVERAGE MAXIMUM AND MINIMUM TEMPERATURES, AND
TEMPERATURE EXTREMES (TOP); AND PRECIPITATION MONTHLY AVERAGES AND DAILY MAXIMUMS FOR ANGRA DO
HEROÍSMO BETWEEN THE YEARS OF 1981 AND 2010 (SOURCE: IPMA 2015). ............................................ 16

FIGURE 2-4 GRID MAP OF THE TERRA BRAVA-B STUDY PLOT, WITH THE APPROXIMATE POSITION OF ALL THE FOGGED TREES
FOR 2014 AND 2015. CF. WITH TABLE 2-1. ........................................................................................... 19

FIGURE 2-5 MAP OF THE SEMI-NATURAL PASTURE IN TERRA BRAVA, WITH THE RELATIVE POSITION OF THE TREES FOGGED
IN 2015 (RED STARS) AND IN 2016 (BLUE STARS). ................................................................................... 21

FIGURE 2-6 CURTIS DYNA-FOG GOLDEN EAGLE MODEL 2610E, SERIES 3 HAND-HELD THERMAL FOGGER. (PHOTO BY THE
AUTHOR) ......................................................................................................................................... 26

FIGURE 2-7 ARRAY OF COLLECTION FUNNELS WITH BOTTLES ATTACHED, SUSPENDED UNDER A CANOPY (PHOTO: GERGELY
ERNO). ........................................................................................................................................... 30

FIGURE 2-8 COLLECTION BOTTLES BEING ATTACHED TO THE SUSPENDED FUNNELS. ON THE BACKGROUND IS POSSIBLE TO
SEE AN I. PERADO SUBS. AZORICA TREE MARKED WITH CONSTRUCTION TAPE. (PHOTO: GERGELY ERNO). ............. 31

FIGURE 2-9 FOGGING OF A L. AZORICA CANOPY, AT THE BEGINNING OF THE 2014 SEASON. (PHOTO: GERGELY ERNO). . 32

FIGURE 3-1. BALA DATASET ALPHA ACCUMULATION CURVES FOR EACH TREE SPECIES. RED - I. PERADO SUBSP. AZORICA;
GREEN - J. BREVIFOLIA; BLUE – L. AZORICA. ........................................................................................... 43

FIGURE 3-2 PROPORTION OF ENDEMIC (E), NATIVE (N) AND INTRODUCED (I) ARTHROPODS FOR EACH TREE SPECIES, AS
TAKEN FROM THE BALA DATASET, IN TERMS OF RELATIVE SPECIES RICHNESS (A) AND RELATIVE ABUNDANCE (C) FOR
THE ENTIRE ARCHIPELAGO, AND OF RELATIVE SPECIES RICHNESS (B) AND RELATIVE ABUNDANCE (D) FOR TERCEIRA. 44

FIGURE 3-3 PROPORTION OF FUNGIVORE (F), HERBIVORE (H), PREDATOR (P), ANTS (P/H) AND SAPROPHYTE (S)
ARTHROPODS FOR EACH TREE SPECIES, AS TAKEN FROM THE BALA DATASET, IN TERMS OF RELATIVE SPECIES RICHNESS
(A) AND RELATIVE ABUNDANCE (C) FOR THE ENTIRE ARCHIPELAGO, AND OF RELATIVE SPECIES RICHNESS (B) AND
RELATIVE ABUNDANCE (D) FOR TERCEIRA................................................................................................ 45

FIGURE 3-4 MODIFIED PRESTON'S OCTAVES HISTOGRAMS FOR THE ENTIRE DATASET OF TERCEIRA (A) AND FOR EACH TREE
SPECIES - I. PERADO SUBSP. AZORICA (B), J. BREVIFOLIA (C) AND L. AZORICA (D), DISCERNING BETWEEN THE
ENDEMIC (GREEN), NATIVE (BLUE) AND INTRODUCED (RED) SPECIES COMPONENTS. ........................................ 46

FIGURE 4-1 RELATIVE ABUNDANCE OF THE SEVERAL ARTHROPOD ORDERS, SORTED BY TOTAL ABUNDANCE, IN EACH TREE
SPECIES AND IN THE COMBINATION OF ALL TREES (ALL). ILEX - I. PERADO SUBSP. AZORICA; JUN - J. BREVIFOLIA; L AU -
L. AZORICA ....................................................................................................................................... 56

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FIGURE 4-2 ALPHA ACCUMULATION CURVES FOR THE FULL SET OF DATA (A), SLOPE OF THE ACCUMULATION CURVE FOR
THE FULL SET OF DATA (B) AND ALPHA ACCUMULATION CURVES FOR EACH TREE SPECIES (C). RED - I. PERADO SUBSP.
AZORICA; BLUE - J. BREVIFOLIA; GREEN – L. AZORICA. .............................................................................. 60

FIGURE 4-3 RELATIVE SPECIES RICHNESS AND ABUNDANCE OF ENDEMIC (E), NATIVE (N) AND INTRODUCED (I)
ARTHROPODS. ILEX - I. PERADO SUBSP. AZORICA; JUN - J. BREVIFOLIA; L AU - L. AZORICA. ................................. 61

FIGURE 4-4 RELATIVE SPECIES RICHNESS AND ABUNDANCE OF FUNGIVORE (F), HERBIVORE (H), PREDATOR (P) AND
SAPROPHYTE (S) ARTHROPODS. ILEX - I. PERADO SUBSP. AZORICA; JUN - J. BREVIFOLIA; L AU - L. AZORICA. .......... 63

FIGURE 4-5 MODIFIED PRESTON'S OCTAVES HISTOGRAMS FOR THE ENTIRE DATASET (A) AND FOR EACH TREE SPECIES - I.
PERADO SUBSP. AZORICA (B), J. BREVIFOLIA (C) AND L. AZORICA (D), DISCERNING BETWEEN THE ENDEMIC (GREEN),
NATIVE (BLUE) AND INTRODUCED (RED) SPECIES COMPONENTS.THE FOUR GRAPHS ARE SCALED EQUALLY FOR THE Y
AXIS. ............................................................................................................................................... 64

FIGURE 4-6 MODIFIED PRESTON'S OCTAVES HISTOGRAMS FOR ENDEMIC (END), NATIVE (NAT) AND INTRODUCED (INTR)
SPECIES WITH SUPERIMPOSED GAMBIN DISTRIBUTION FITS (BLACK DOTS). THE THREE GRAPHS ARE SCALED EQUALLY
FOR THE Y AXIS ................................................................................................................................. 65

FIGURE 4-7 NONMETRIC DIMENSIONAL SCALING (NMDS) WITH BRAY-CURTIS SIMILARITIES FOR EACH TREE SPECIES.
GREEN - I. PERADO SUBSP. AZORICA; RED - J. BREVIFOLIA; BLUE – L. AZORICA ............................................... 67

FIGURE 5-1 RELATIVE SPECIES RICHNESS (LEFT) AND ABUNDANCE (RIGHT) OF ENDEMIC (END), NATIVE (NAT) AND
INTRODUCED (INTR) ARTHROPODS, FOR EACH YEAR AND FOGGING EPISODE COMBINATION. 2014_1T – TREES
FOGGED IN 2014; 2015_1T – CONTROL TREES FOGGED FOR THE FIRST TIME IN 2015; 2015_2T – TREES INITIALLY
FOGGED IN 2014 AND FOGGED FOR A SECOND TIME IN 2015. ................................................................... 83

FIGURE 5-2 RELATIVE SPECIES RICHNESS (LEFT) AND ABUNDANCE (RIGHT) OF FUNGIVORE (F), HERBIVORE (H), PREDATOR
(P) AND SAPROPHYTE (S) ARTHROPODS, FOR EACH YEAR AND FOGGING EPISODE COMBINATION. 2014_1T – TREES
FOGGED IN 2014; 2015_1T – CONTROL TREES FOGGED FOR THE FIRST TIME IN 2015; 2015_2T – TREES INITIALLY
FOGGED IN 2014 AND FOGGED FOR A SECOND TIME IN 2015. ................................................................... 84

FIGURE 5-3. MODIFIED PRESTON'S OCTAVES HISTOGRAMS FOR THE FOR THE COMMUNITY PRESENT IN THE TREES FOGGED
FOR THE FIRST TIME IN 2014 (2014_1T) AND FOR THE COMMUNITY PRESENT IN THOSE SAME TREES FOGGED FOR
THE SECOND TIME IN 2015 (2015_2T), WITH DISCERNING BETWEEN THE ENDEMIC (GREEN), NATIVE (BLUE) AND
INTRODUCED (RED) SPECIES COMPONENTS. BOTH GRAPHS ARE SCALED EQUALLY FOR THE Y-AXIS. ...................... 85

FIGURE 5-4 RELATIONSHIP BETWEEN TAXONOMIC RICHNESS (TD) AND FUNCTIONAL RICHNESS (FD) FOR THE ENTIRE
COMMUNITY AND FOR SEVERAL SUBSETS. FOR EACH SUBSET, THE GRAPHIC ON THE LEFT (BLACK DOTS) USES THE REAL
VALUES FOR EACH SUBSET, AND THE ONE ON THE RIGHT (BLUE DOTS), THE RAREFIED VALUES OF TD AND TD. TD –
TAXONOMIC DIVERSITY; TDR – RAREFIED TAXONOMIC DIVERSITY; FD – FUNCTIONAL DIVERSITY; FDR - RAREFIED
FUNCTIONAL DIVERSITY. SUMMARY OF REGRESSION RESULTS IN APPENDIX III. ................................................ 88

FIGURE 5-5 RAREFIED TAXONOMIC DIVERSITY (TDR) AND FUNCTIONAL DIVERSITY (FDR) VALUES FOR THE DISTINCT
FOGGING EPISODES. VALUES ARE CALCULATED FOR THE ENTIRE COMMUNITY AND FOR ITS SEVERAL SUBSETS. FOR
EACH SUBSET, THE GRAPHIC ON THE LEFT REFERS TO THE TD, AND THE ONE ON THE RIGHT (COLOURED GREEN) TO
THE FD. SIGNIFICANT DIFFERENCES ARE INDICATED WITH A RED STAR SYMBOL. 2014_1T – TREES FOGGED IN 2014;
2015_1T – CONTROL TREES FOGGED FOR THE FIRST TIME IN 2015; 2015_2T – TREES INITIALLY FOGGED IN 2014
AND FOGGED FOR A SECOND TIME IN 2015. ........................................................................................... 90

xi
FIGURE 5-6 COMPARISON BETWEEN THE TD AND FD OF THE SAMPLED COMMUNITIES AND THAT OF A NULL COMMUNITY.
VALUES ARE CALCULATED FOR THE ENTIRE COMMUNITY AND FOR ITS SEVERAL SUBSETS. FOR EACH SUBSET, THE
GRAPHIC ON THE LEFT REFERS TO THE TD, AND THE ONE ON THE RIGHT (COLORED GREEN) TO THE FD. SIGNIFICANT
DIFFERENCES ARE INDICATED WITH A RED STAR SYMBOL. 2014_1T – TREES FOGGED IN 2014; 2015_1T –
CONTROL TREES FOGGED FOR THE FIRST TIME IN 2015; 2015_2T – TREES INITIALLY FOGGED IN 2014 AND FOGGED
FOR A SECOND TIME IN 2015............................................................................................................... 92

FIGURE 6-1 FOGGING OF A J. BREVIFOLIA TREE IN THE SEMI-NATURAL PASTURE IN 2016. NOTE THE SMALL AND WIND
SHAPED ARCHITECTURE OF THE CANOPY, AND THE ARRANGEMENT OF THE COLLECTION FUNNELS. PHOTO:
ALEJANDRA ROS PRIETO. .................................................................................................................. 102

FIGURE 6-2 RELATIVE SPECIES RICHNESS AND ABUNDANCE OF ENDEMIC (E), NATIVE (N) AND INTRODUCED (I)
ARTHROPODS FOR THE J. BREVIFOLIA TREES FOGGED FOR THE FIRST TIME IN THE FOREST AND IN THE SEMI-NATURAL
PASTURE IN 2015, AND FOR THE HERBACEOUS VEGETATION OF THE PASTURE. JUN_FOR – J. BREVIFOLIA TREES IN
THE FOREST; JUN_PAST – J. BREVIFOLIA TREES IN THE PASTURE; PASTURE – HERBACEOUS VEGETATION.............. 107

FIGURE 6-3. RELATIVE SPECIES RICHNESS AND ABUNDANCE OF FUNGIVORE (F), HERBIVORE (H), PREDATOR (P) AND
SAPROPHYTE (S) ARTHROPODS FOR THE J. BREVIFOLIA TREES FOGGED FOR THE FIRST TIME IN THE FOREST AND IN THE
SEMI-NATURAL PASTURE IN 2015, AND FOR THE HERBACEOUS VEGETATION OF THE PASTURE. JUN_FOR – J.
BREVIFOLIA TREES IN THE FOREST; JUN_PAST – J. BREVIFOLIA TREES IN THE PASTURE; PASTURE – HERBACEOUS
VEGETATION. .................................................................................................................................. 108

FIGURE 6-4 MODIFIED PRESTON'S OCTAVES HISTOGRAMS FOR THE FOR THE COMMUNITY PRESENT IN THE J. BREVIFOLIA
TREES FOGGED FOR THE FIRST TIME IN THE FOREST AND IN THE SEMI-NATURAL PASTURE IN 2015, DISCERNING
BETWEEN THE ENDEMIC (GREEN), NATIVE (BLUE) AND INTRODUCED (RED) SPECIES COMPONENTS. THE GRAPHS ARE
SCALED EQUALLY FOR THE Y AXIS. ........................................................................................................ 109

FIGURE 6-5 PROPORTION OF ENDEMIC (E), NATIVE (N) AND INTRODUCED (I) ARTHROPODS FOR EACH YEAR AND FOGGING
EPISODE COMBINATION. RESULTS ARE PRESENTED IN TERMS OF RELATIVE SPECIES RICHNESS (A) AND RELATIVE
ABUNDANCE (B) FOR THE ENTIRE DATASET, AND OF RELATIVE SPECIES RICHNESS (C) AND RELATIVE ABUNDANCE (D)
WITHOUT THE INTRODUCED SPECIES ECTOPSOCUS BRIGGSI. 2015_1T – TREES FOGGED IN 2015; 2016_1T –
CONTROL TREES FOGGED FOR THE FIRST TIME IN 2016; 2016_2T – TREES INITIALLY FOGGED IN 2015 AND FOGGED
FOR A SECOND TIME IN 2016............................................................................................................. 113

FIGURE 6-6 PROPORTION OF FUNGIVORE (F), HERBIVORE (H), PREDATOR (P), ANTS (P/H) AND SAPROPHYTE (S)
ARTHROPODS, FOR EACH YEAR AND FOGGING EPISODE COMBINATION. RESULTS ARE PRESENTED IN TERMS OF
RELATIVE SPECIES RICHNESS (A) AND RELATIVE ABUNDANCE (B) FOR THE ENTIRE DATASET, AND OF RELATIVE SPECIES
RICHNESS (C) AND RELATIVE ABUNDANCE (D) WITHOUT THE INTRODUCED SPECIES ECTOPSOCUS BRIGGSI. 2015_1T
– TREES FOGGED IN 2015; 2016_1T – CONTROL TREES FOGGED FOR THE FIRST TIME IN 2016; 2016_2T – TREES
INITIALLY FOGGED IN 2015 AND FOGGED FOR A SECOND TIME IN 2016. ..................................................... 114

FIGURE 6-7 MODIFIED PRESTON'S OCTAVES HISTOGRAMS FOR THE FOR THE COMMUNITY PRESENT IN THE TREES FOGGED
FOR THE FIRST TIME IN 2015 (2015_1T), FOR THAT OF THE CONTROL TREES FOGGED FOR THE FIRST TIME IN 2016
(2016_1T) AND FOR THE COMMUNITY PRESENT IN THE RECOLONISED TREES FOGGED FOR THE SECOND TIME IN
2016 (2016_2T), DISCERNING BETWEEN THE ENDEMIC (GREEN), NATIVE (BLUE) AND INTRODUCED (RED) SPECIES
COMPONENTS. A RED STAR INDICATES THE PSOCOPTERA ECTOPSOCUS BRIGGSI. THE GRAPHS FOR THE INITIAL
COMMUNITY AND FOR THE CONTROL TREES ARE SCALED EQUALLY FOR THE Y AXIS. ........................................ 115

xii
FIGURE 6-8 RELATIONSHIP BETWEEN TAXONOMIC RICHNESS (TD) AND FUNCTIONAL RICHNESS (FD) FOR THE ENTIRE
COMMUNITY AND FOR SEVERAL SUBSETS. FOR EACH SUBSET, THE GRAPHIC ON THE LEFT (BLACK DOTS) USES THE REAL
VALUES FOR EACH SUBSET, AND THE ONE ON THE RIGHT (BLUE DOTS), THE RAREFIED VALUES OF TD AND TD. TD –
TAXONOMIC DIVERSITY; TDR – RAREFIED TAXONOMIC DIVERSITY; FD – FUNCTIONAL DIVERSITY; FDR - RAREFIED
FUNCTIONAL DIVERSITY. SUMMARY OF REGRESSION RESULTS IN APPENDIX IV. .............................................. 118

FIGURE 6-9 RAREFIED TAXONOMIC DIVERSITY (TDR) AND FUNCTIONAL DIVERSITY (FDR) VALUES FOR THE DISTINCT
FOGGING EPISODES. VALUES ARE CALCULATED FOR THE ENTIRE COMMUNITY AND FOR ITS SEVERAL SUBSETS. FOR
EACH SUBSET, THE GRAPHIC ON THE LEFT REFERS TO THE TDR, AND THE ONE ON THE RIGHT (COLORED GREEN) TO
THE FDR, EXCEPT FOR INTRODUCED SPECIES, WHERE TD AND FD ARE USED INSTEAD. AN ASTERISK IN THE HEADER
OF THE SUBSET DENOTES THE REMOVAL OF THE INTRODUCED ECTOPSOCUS BRIGGSI. 2015_1T – TREES FOGGED IN
2015; 2016_1T – CONTROL TREES FOGGED FOR THE FIRST TIME IN 2016; 2016_2T – TREES INITIALLY FOGGED IN
2015 AND FOGGED FOR A SECOND TIME IN 2016.................................................................................. 120

FIGURE 6-10 COMPARISON BETWEEN THE TD AND FD OF THE SAMPLED COMMUNITIES AND THAT OF A NULL
COMMUNITY. VALUES ARE CALCULATED FOR THE ENTIRE COMMUNITY AND FOR ITS SEVERAL SUBSETS. FOR EACH
SUBSET, THE GRAPHIC ON THE LEFT REFERS TO THE TD, AND THE ONE ON THE RIGHT (COLORED GREEN) TO THE FD.
AN ASTERISK IN THE HEADER OF THE SUBSET DENOTES THE REMOVAL OF THE INTRODUCED ECTOPSOCUS BRIGGSI.
2015_1T – TREES FOGGED IN 2015; 2016_1T – CONTROL TREES FOGGED FOR THE FIRST TIME IN 2016;
2016_2T – TREES INITIALLY FOGGED IN 2015 AND FOGGED FOR A SECOND TIME IN 2016. ........................... 122

xiii
 Table of tables
TABLE 2-1 SUMMARY TABLE WITH EACH TREE FOGGED IN THE FOREST EXPERIMENT, ITS IDENTIFYING CODE, YEARS OF FIRST
AND SECOND FOGGING (WHEN APPLICABLE), AND SEVERAL INDIVIDUAL METRICS, NAMELY DBH (DIAMETER AT
BREAST HEIGHT) IN CENTIMETERS, TOTAL HEIGHT, CANOPY AREA AND CANOPY VOLUME. SEVERAL L. AZORICA
SPECIMENS HAD MORE THAN ONE MAIN TRUNK; IN THAT CASE ALL DBH’S ARE PRESENTED, WITH THE SUM IN
PARENTHESIS. 1T – FIRST TIME FOGGING; 2T – SECOND TIME FOGGING; EX – CONTROL TREE. ........................... 20

TABLE 2-2 TABLE WITH EACH J. BREVIFOLIA TREE FOGGED IN THE SEMI-NATURAL PASTURE EXPERIMENT, ITS IDENTIFYING
CODE, AND YEARS OF FIRST AND SECOND FOGGING, WHEN APPLICABLE. P - PASTURE; 1T – FIRST TIME FOGGING; 2T
– SECOND TIME FOGGING. ................................................................................................................... 22

TABLE 3-1 SUMMARY TABLE OF THE COLLECTED ARTHROPOD TAXA FROM BALA, LISTING ALL CLASSES AND ORDERS FOUND
IN THE THREE TREE SPECIES FOR TERCEIRA ISLAND, WITH INDICATION OF THE NUMBER OF FAMILIES, SPECIES AND
SPECIMENS IN EACH ORDER. ................................................................................................................. 41

TABLE 3-2 SUMMARY TABLE WITH THE BALA DATASET ARTHROPOD SPECIES RICHNESS (S), ABUNDANCE (N), NUMBER OF
SINGLETONS AND DOUBLETONS, UNIQUES AND DUPLICATES, NUMBER OF TRANSECTS, NUMBER OF SAMPLES AND
DIVERSITY FOR THE TOTAL NUMBER OF SPECIMENS AND FOR EACH INDIVIDUAL TREE SPECIES IN THE ENTIRE
ARCHIPELAGO AND FOR TERCEIRA ISLAND. VALUES IN PARENTHESIS INDICATE THE CORRESPONDING STANDARDIZED
VALUE, OBTAINED FROM SAMPLE BASED ACCUMULATION, AT THE MINIMUM COMMON NUMBER OF 169 SAMPLES IN
TERCEIRA. ILEX - I. PERADO SUBSP. AZORICA; JUN - J. BREVIFOLIA; L AU - L. AZORICA. ...................................... 42

TABLE 3-3 VALUES OF JACKKNIFE 1 ESTIMATED RICHNESS, WITH CORRESPONDING INVENTORY COMPLETENESS, AND VALUE
OF SLOPE AT THE FINAL POINT OF EACH ACCUMULATION CURVE, FOR EACH INDIVIDUAL TREE SPECIES, USING THE
BALA DATASET. ................................................................................................................................ 43

TABLE 3-4 SUMMARY TABLE OF INDVAL RESULTS FROM THE BALA DATASET FOR EACH HOST-TREE, WITH TOTAL NUMBER
OF INDICATOR SPECIES, AND THE NUMBER OF INDICATOR SPECIES BELONGING TO EACH COLONISATION CLASS. AN
EXPANDED VERSION OF THIS TABLE IS PRESENTED IN APPENDIX II. ................................................................ 47

TABLE 3-5 RAREFIED VALUES OF TOTAL Β DIVERSITY, Β REPLACEMENT AND Β RICHNESS BETWEEN THE DIFFERENT TREE
SPECIES IN TERCEIRA ISLAND, USING THE BALA DATASET - FOR THE ENTIRE COMMUNITY, FOR ENDEMIC, FOR NATIVE
AND FOR INTRODUCED SPECIES, . ILEX - I. PERADO SUBSP. AZORICA; JUN - J. BREVIFOLIA; L AU - L. AZORICA. ........ 47

TABLE 4-1 SUMMARY TABLE OF THE COLLECTED ARTHROPOD TAXA, LISTING ALL CLASSES AND ORDERS FOUND, WITH
INDICATION OF THE NUMBER OF FAMILIES, SPECIES AND SPECIMENS IN EACH ORDER. SUBCLASSES OR ORDERS WITH
AN ASTERISK WERE NOT USED FOR FURTHER ANALYSES. ALSO, 379 SPECIMENS BELONGING TO THE REMAINING
ORDERS, THAT WERE NOT POSSIBLE TO IDENTIFY TO A GIVEN MORPHOSPECIES AND WERE THEREFORE EXCLUDED
FROM FURTHER ANALYSES, ARE INCLUDED IN THE TABLE. ............................................................................ 57

TABLE 4-2 SUMMARY TABLE WITH THE ARTHROPOD SPECIES RICHNESS (S), ABUNDANCE (N), NUMBER OF SINGLETONS
AND DOUBLETONS, UNIQUES AND DUPLICATES, NUMBER OF TREES AND OF SAMPLES, AVERAGE NUMBER OF SPECIES
PER TREE, NUMBER OF SPECIES AND SPECIMENS PER SQUARE METER (VALUES IN PARENTHESIS ARE STANDARDIZED AT
18 SAMPLES), DIVERSITY INDICES (FISHER Α, SHANNON-WIENER, SHANNON EXPONENTIAL, SIMPSON, INVERSE
SIMPSON AND PIELOU) FOR THE TOTAL NUMBER OF SPECIMENS AND FOR EACH INDIVIDUAL TREE SPECIES ............ 59

xiv
TABLE 4-3 VALUES OF JACKKNIFE 1 ESTIMATED RICHNESS, WITH CORRESPONDING INVENTORY COMPLETENESS, AND VALUE
OF SLOPE AT THE FINAL POINT OF EACH ACCUMULATION CURVE, FOR EACH INDIVIDUAL TREE SPECIES AND FOR THE
ENTIRE DATASET (TOTAL) ..................................................................................................................... 60

TABLE 4-4 SUMMARY TABLE OF INDVAL RESULTS, WITH INDICATOR SPECIES AND CORRESPONDING HOST TREE, INDICATOR
VALUE, STATISTICAL SIGNIFICANCE OF THE ASSOCIATIONS AND THE FREQUENCY. E - ENDEMIC; N - NATIVE; I -
INTRODUCED. ................................................................................................................................... 62

TABLE 4-5. VALUES OF Α-GAMBIN PARAMETER FOR THE ENTIRE DATASET WITH ASSOCIATED SIGNIFICANCE TESTS VALUES
FOR THE FIT OF THE GAMBIN DISTRIBUTION; AND STANDARDIZED VALUES OF Α-GAMBIN PARAMETER FOR: THE TOTAL
COMMUNITY, FOR THE DIFFERENT TREE SPECIES AND FOR COLONISATION STATUS. THE ASTERISK INDICATES A GOOD
FIT OF THE GAMBIN DISTRIBUTION TO THE DATA. ..................................................................................... 66

TABLE 4-6 RAREFIED VALUES OF TOTAL Β DIVERSITY, Β REPLACEMENT AND Β RICHNESS BETWEEN THE DIFFERENT TREE
SPECIES IN THE STUDY PLOT- FOR THE ENTIRE COMMUNITY, FOR ENDEMIC, FOR NATIVE AND FOR INTRODUCED
SPECIES. ILEX - I. PERADO SUBSP. AZORICA; JUN - J. BREVIFOLIA; L AU - L. AZORICA. ......................................... 68

TABLE 5-1. SUMMARY TABLE WITH THE ARTHROPOD SPECIES RICHNESS (S), ABUNDANCE (N), NUMBER OF SINGLETONS
AND DOUBLETONS, NUMBER OF TREES AND OF SAMPLES, AVERAGE NUMBER OF SPECIES PER TREE, NUMBER OF
SPECIES AND SPECIMENS PER SQUARE METER, FOR THE TOTAL EXTENT OF THE FOGGING EXPERIMENT, AND FOR EACH
YEAR AND FOGGING EPISODE COMBINATION. A TOTAL OF 24 INDIVIDUAL TREES WERE FOGGED DURING THE
EXPERIMENT, BUT IF CONSIDERING THOSE THAT WERE FOGGED FOR A SECOND TIME AS NWE TREES, THAT TOTAL
ASCENDS TO 39 – IN PARENTHESIS IN THE TABLE BELOW. 2014_1T – TREES FOGGED IN 2014; 2015_1T –
CONTROL TREES FOGGED FOR THE FIRST TIME IN 2015; 2015_2T – TREES INITIALLY FOGGED IN 2014 AND FOGGED
FOR A SECOND TIME IN 2015............................................................................................................... 82

TABLE 5-2 RANK ABUNDANCE OF THE TEN MOST ABUNDANT SPECIES, ORDERED BY ABUNDANCE VALUES FOR THE INITIAL
COMMUNITY OF 2014. 2014_1T – TREES FOGGED IN 2014; 2015_1T – CONTROL TREES FOGGED FOR THE FIRST
TIME IN 2015; 2015_2T – TREES INITIALLY FOGGED IN 2014 AND FOGGED FOR A SECOND TIME IN 2015. E –
ENDEMIC; N – NATIVE. ...................................................................................................................... 86

TABLE 5-3 RAREFIED VALUES OF TOTAL Β DIVERSITY, Β REPLACEMENT AND Β RICHNESS BETWEEN THE DIFFERENT YEARS
AND FOGGING EPISODES, FOR THE ENTIRE COMMUNITY, FOR ENDEMICS AND FOR INTRODUCED SPECIES. 2014_1T –
TREES FOGGED IN 2014; 2015_1T – CONTROL TREES FOGGED FOR THE FIRST TIME IN 2015; 2015_2T – TREES
INITIALLY FOGGED IN 2014 AND FOGGED FOR A SECOND TIME IN 2015 ........................................................ 87

TABLE 5-4 SUMMARY OF THE T-TEST SIGNIFICANCE VALUES FOR THE DIFFERENCES BETWEEN THE COMMUNITIES OF THE
DISTINCT FOGGING EPISODES IN MY STUDY AND THAT OF THE EQUIVALENT NULL COMMUNITY. ........................... 93

TABLE 6-1SUMMARY TABLE WITH THE ARTHROPOD SPECIES RICHNESS (S), ABUNDANCE (N), NUMBER OF SINGLETONS AND
DOUBLETONS, NUMBER OF TREES AND OF SAMPLES, AVERAGE NUMBER OF SPECIES PER TREE, NUMBER OF SPECIES
AND SPECIMENS PER SQUARE METER, FOR THE J. BREVIFOLIA TREES SAMPLED FOR THE FIRST TIME IN 2015, BOTH
FOR THE FOREST AND SEMI-NATURAL PASTURE, TOGETHER WITH SOME INFORMATION REGARDING THE ARTHROPODS
COLLECTED ON THE HERBACEOUS VEGETATION OF THE SEMI-NATURAL PASTURE (PASTURE .............................. 106

TABLE 6-2 RANK ABUNDANCE OF THE FIVE MOST ABUNDANT SPECIES IN THE FOREST AND IN THE SEMI-NATURAL PASTURE
TREES FOGGED FOR THE FIRST TIME IN 2015, ORDERED BY ABUNDANCE VALUES FOR THE INITIAL COMMUNITY THE
FOREST J. BREVIFOLIA TREES. E – ENDEMIC; N – NATIVE ......................................................................... 110

xv
TABLE 6-3 RAREFIED VALUES OF TOTAL Β DIVERSITY, Β REPLACEMENT AND Β RICHNESS BETWEEN THE FOREST AND SEMI-
NATURAL PASTURE J. BREVIFOLIA TREES SAMPLED FOR THE FIRST TIME IN 2015. RESULTS ARE PRESENTED FOR THE
ENTIRE COMMUNITY, AND FOR ENDEMIC, NATIVE AND INTRODUCED SPECIES. J_FOR – J. BREVIFOLIA TREES IN THE
FOREST; J_PAST – J. BREVIFOLIA TREES IN THE PASTURE ........................................................................... 110

TABLE 6-4. SUMMARY TABLE WITH THE ARTHROPOD SPECIES RICHNESS (S), ABUNDANCE (N), NUMBER OF SINGLETONS
AND DOUBLETONS, NUMBER OF TREES AND OF SAMPLES, AVERAGE NUMBER OF SPECIES PER TREE, NUMBER OF
SPECIES AND SPECIMENS PER SQUARE METER, FOR THE TOTAL EXTENT OF THE FOGGING EXPERIMENT, AND FOR EACH
YEAR AND FOGGING EPISODE COMBINATION. VALUES IN PARENTHESIS REFER TO THESE SAME METRICS WITHOUT THE
INTRODUCED PSOCOPTERA ECTOPSOCUS BRIGGSI. 2015_1T – TREES FOGGED IN 2015; 2016_1T – CONTROL
TREES FOGGED FOR THE FIRST TIME IN 2016; 2016_2T – TREES INITIALLY FOGGED IN 2015 AND FOGGED FOR A
SECOND TIME IN 2016. .................................................................................................................... 111

TABLE 6-5 RANK ABUNDANCE OF THE FIVE MOST ABUNDANT SPECIES, ORDERED BY ABUNDANCE VALUES FOR THE INITIAL
COMMUNITY OF 2015. 2015_1T – TREES FOGGED IN 2015; 2016_1T – CONTROL TREES FOGGED FOR THE FIRST
TIME IN 2016; 2016_2T – TREES INITIALLY FOGGED IN 2015 AND FOGGED FOR A SECOND TIME IN 2016. E –
ENDEMIC; N – NATIVE, I – INTRODUCED.............................................................................................. 116

TABLE 6-6 RAREFIED VALUES OF TOTAL Β DIVERSITY, Β REPLACEMENT AND Β RICHNESS BETWEEN THE DIFFERENT YEARS
AND FOGGING EPISODES, FOR THE ENTIRE COMMUNITY, FOR ENDEMIC, FOR NATIVE AND FOR INTRODUCED SPECIES
(WITH E. BRIGGSI REMOVED). 2015_1T – TREES FOGGED IN 2015; 2016_1T – CONTROL TREES FOGGED FOR THE
FIRST TIME IN 2016; 2016_2T – TREES INITIALLY FOGGED IN 2015 AND FOGGED FOR A SECOND TIME IN 2016.
................................................................................................................................................... 116

xvi
Chapter 1
General Introduction
Since the early days of naturalist explorations of Hooker (1847) and Darwin (1859), islands
have captured the interest of naturalists and ecologists as places of a unique fauna and flora. Islands
are particularly important in the conservation of biodiversity because, as even if encompassing less
than 5% of the planet’s landmass (Caujapé-Castells et al. 2010), islands are home to a
disproportionate amount of unique diversity (Paulay 1994, Rosenzweig 1995, Losos & Ricklef 2010,
Warren et al. 2015). In fact, 20 of the current 36 biodiversity hotspots are islands or have an
associated island component (Myers et al. 2000).

Conversely, islands include also some of the most endangered habitats and species on Earth,
with its native communities being in many cases extremely vulnerable to anthropogenic habitat
disturbance and destruction, and to the introduction of exotic species (Cronk 1997, Sadler 1999,
Dunn 2005, Caujapé-Castells et al. 2010). Approximately 75% of documented animal extinctions
constitute island species (Frankham 1998), and considering the current arthropod diversity, Dunn
(2005) estimates that some 44.000 arthropod species might have become extinct in the last 600 years.

The natural terrestrial ecosystems of the Azores Archipelago have also suffered greatly over
the last 600 years of human settlement (Martins 1993, Triantis et al. 2010a), and there is therefore an
urgent need to preserve what is left of these unique insular biotas. In order to do so, our current
knowledge regarding species, communities and habitats, and recovery processes under disturbance
must be expanded, and new possibilities for conservation must be also evaluated. This will be
particularly urgent in some islands in which there is an ongoing conflict between existing protected
areas and the economic development of the region, given that a large portion of the population is
directly or indirectly dependent on agriculture and cattle production (Cruz et al. 2007, Gil et al.
2018).

1.1. Current arthropod knowledge in the Azores

The Azores are an isolated archipelago, and historically little regard had been given by
naturalists to its fauna and flora, save some early mentions in the works of Gaspar Frutuoso, in the
16th century (Frutuoso 2005a,b), or by other local chroniclers (cf. Vieira 2015). In 1836, on the return
leg of its famous voyage on the Beagle, Charles Darwin went ashore in Terceira, but left little or no
remark regarding the fauna and flora of the island (Keines 1988). This nevertheless spurred some

1
interest about the Azorean archipelago in the international scientific community and in the local
naturalists, of which the prolific work of Francisco Arruda Furtado should be mentioned (see Arruda
1994).

Despite this, there was still a paucity of information regarding the local arthropod
communities notwithstanding some important scientific expeditions like those of Chopard and
Mequignon in 1930 (Vieira 2015) or that of Frey, Storå and Cedercreutz in 1938 (see Tjeder 1948),
or some works by other authors, mainly of a taxonomic nature or species lists (e.g. Drouët 1859,
1861, Simon 1883, Tjeder 1963, Ohm 1969). Vieira (2015) gives a detailed account of the initial
entomological studies in the Azorean archipelago.

This situation has greatly improved in the last twenty years, mainly due to the work of
research groups from the University of the Azores, with many studies on both indigenous and exotic
species having been carried out, such as exhaustive species inventories (Borges et al. 2005b; Borges
et al. 2010), comprehensive biogeographical studies (Whittaker et al. 2008, 2014; Borges & Hortal
2009; Cardoso et al. 2010; Santos et al. 2010; Triantis et al. 2010a,b; Cameron et al. 2013; Aranda et
al. 2014; Carvalho & Cardoso 2014; Carvalho et al. 2015), phylogenetic and evolutionary studies
(Ferreira et al. 2011; Schaefer et al. 2011; Amorim et al. 2012; Rodrigues et al. 2013), or studies
regarding the future effects of climatic changes in the archipelago (Ferreira et al. 2016).

In addition, there were several ecological studies at smaller spatial scales focusing on the
communities of particular taxa, namely arthropods (e.g. Borges et al. 2006; Meijer et al. 2011;
Florencio et al. 2013; Raposeiro et al. 2013, Florencio et al. 2016, Lamelas-López et al. 2017), but
also of bryophytes (e.g. Gabriel & Bates 2005; Aranda et al. 2015) or vascular plants (e.g. Elias &
Dias 2009; Rumeu et al. 2011; Marcelino et al. 2013).

However, there are so far very few studies dealing in detail with the specific biotic
communities associated with each of the indigenous host tree species from the extant Azorean
forests. Among them I would emphasise the works on arthropod canopy community biodiversity and
structure (Markin et al. 1995; Ribeiro et al. 2005; Gaspar et al. 2008; Borges et al. 2008; Ribeiro &
Borges 2010) and those dealing with the effects of herbivory on a specific indigenous host tree
species (Vieira et al. 1993; Silva et al. 1995; Ribeiro et al. 2003).

As such, it is possible to see that despite the considerable amount of studies regarding the
biotic communities of the Azores, there are still several gaps regarding the knowledge of the
diversity and the structure of the arthropod communities associated with Azorean tree canopies,
particularly concerning the way these communities might recover after a disturbance event,

2
hindering conservation efforts regarding the indigenous biodiversity, and also the sustainable
resource management and development (Summervile et al. 2003; Cardoso et al. 2011a) of the region.

Striving to increase the current knowledge about these communities, I proposed myself to
use for the first time in the Azores canopy fogging to sample the arthropod communities present in
three native tree species of significant importance in the natural forests of the Azores.

Canopy fogging (or pyrethrum knockdown) is a fairly unselective technique that allows to
capture a “snapshot” of the community present on the tree at the moment of sampling. Its samples
are a close reflection of the canopy arthropod community, irrespectively of the surface the arthropods
are on, or their activity, dispensing with attractants and avoiding biases connected with activity-based
traps (Stork & Hammond 1997). This technique also has the advantage of generating highly
comparable samples, despite differences in latitude and altitude, in the time of collection, or
differences in forest types and host tree species (Stork & Hammond 1997).

The use of this technique also opens the opportunity for another novelty in the Azorean
archipelago, namely taking advantage of the defaunation of the trees, caused by the sampling
protocol, to study how the arthropods recolonize the canopies of the native trees and how the
community itself recovers from a major local disturbance and extinction.

Given the nature of the doctoral program where I enrolled (Integrated Landscape
Management), I thought it would also be appropriate to study the arthropod communities and these
same recolonization and recovery processes on the canopies of some of the relic trees present in
several anthropogenic habitats of Terceira, particularly in the semi-natural pastures, ascertaining their
importance in the conservation of the indigenous entomological fauna.

3
 This thesis is organized in seven chapters and I summarize below the main objectives in each
one:

Chapter 1
Here I give a brief rationale for my work, my motives and objectives

Chapter 2
In this chapter I give a brief description of the Azorean archipelago and particularly of
Terceira island, its ontogeny, its climate, and of its fauna and flora, with emphasis on the three native
tree species selected for this study, more precisely Juniperus brevifolia (Seub.) Antoine, Ilex perado
Aiton subsp. azorica (Loes.) Tutin and Laurus azorica (Seub.) Franco.

I also do an appraisal of the suitability of the thermal fogging technique to fulfill my

objectives, together with an overview of the history of the use of this technique.

Finally, I give a description of the two study sites where the sampling took place, in
conjunction with the used sampling protocol and some details regarding the equipment and
insecticide solution used, the sorting and identification of the specimens and the statistical analyses
implemented.

Chapter 3

Here I investigate the already existing arthropod data regarding the species present in the
canopies of Juniperus brevifolia, Ilex perado subsp. azorica and Laurus azorica, giving a brief
overview of at the archipelago level, but focusing in Terceira island, to avoid confounding effects
regarding island age, climatic variables, the different degree of anthropic disturbance or other factors
that influence the composition of the arthropod community in each island (Borges 1997, Gaspar et al
2011, Nunes et al. 2015).

The arthropod data was collected between the years of 1999 and 2004 in the context of the
BALA project (Ribeiro et al. 2005, Gaspar et al. 2008).

This chapter will allow a better understanding about the structure and species composition of
the arthropod communities associated with each tree species at island level, as well as an evaluation
of the relative weight of indigenous arthropod species in the canopies.

Therefore, data summarized in this chapter will be a baseline to be compared with the results
obtained by pyrethrum knockdown/canopy fogging in a well preserved forest fragment of Terceira
(Chapters 4, 5 and 6).

4
 Chapter 4
In this chapter, I will use the samples collected by canopy fogging on the 16 trees fogged in
the forest in 2014, together with those of eight extra trees that were also fogged for the first time in
2015, allowing me to:

a) describe in detail the diversity, abundance and spatial patterns of canopy arthropods in one
of the best preserved extant forest patches in Terceira island, including previously less well studied
groups such as Hymenoptera, Diptera, Collembola and Acari;

b) To compare the communities sampled by canopy fogging in a well preserved forest patch
with previous canopy data for Terceira island, with a slight focus on the colonization status of the
species present.

c) to ascertain if these tree species host distinct arthropod communities or if the previously
reported high levels of generalists among the endemic and native arthropod species (Ribeiro et al.
2005) account for a somewhat homogeneous community through the different host-tree species;

Chapter 5
Chapter five aims to study the recovered arthropod canopy communities after fogging,
comparing it with the initial community of those same trees and with that of control trees also fogged
in 2015

I analyze and compare the overall structure of the recolonized community, ascertaining
differences in species composition, abundance and colonization status, taxonomic and functional
diversity and also create null models to investigate how the recovered community would differ from
one that would be assembled purely by stochastic processes.

With this, I will try to validate the following predictions:

a) Given the generalist status of Azorean arthropod species (Ribeiro et al. 2005), a rapid
recolonization process is expected to occur after defaunation leading to the rapid reestablishment of
similar richness, composition and species abundance distribution in canopy arboreal communities;

b) The low diversity and abundance of introduced species in the canopies (see Chapter 4 and
Florencio et al. 2016) suggests that these are vagrants and not a functional part of the community.
Therefore, I expect higher levels of beta diversity for introduced species than for indigenous species
with no increase in species richness as exotic introduced species should be filtered by the
architecture of tree canopies and not by biotic resistance;

5
 c) The fact that the arboreal arthropod fauna is resistant to exotic introduced species
(Florencio et al. 2016,) may imply either a facilitation process in the spread of exotic species after
defaunation (empty niche effect) if the exotics are filtered by competition, or no effect if exotics are
filtered by the architecture and biotic and abiotic conditions in the tree canopies;

d) in addition, the lack of saturation in functional trait space of indigenous arthropod fauna
in Azores (Whittaker et al. 2014) may also imply that the fauna of Azores will be vulnerable to
further colonization and probably invasion of exotic species with new traits during the recolonization
process.

Chapter 6
In here I study some Azorean cedar trees isolated in a semi-natural pasture, first comparing
the arthropod communities present in them with those of other tree Azorean cedars fogged in the
native forest within a short time period. I then proceed to analyze the recolonization of these trees by
the arthropod community. In this process I aim to investigate the ecological importance of these trees
in the ecosystems of Terceira and try to validate the following predictions:

a) Isolated trees in pastures, due to their architecture and biotic and abiotic conditions of
their canopies, can potentially act as an indigenous species repository, maintaining a community
similar to those of the extant native forests, despite the large scale disturbance suffered during the
clearing of the pasture;

b) High elevation semi-natural pastures, with low grazing pressure and insecticide use (cf.
Borges & Brown 2001) are still host to a high proportion of indigenous species (Borges et al. 2008,
Cardoso et al. 2009), with exotic species favoring more disturbed lowland habitats. Therefore, as
with the case of the forest communities, recolonization occurs quickly from the surrounding species
pool, favoring the highly abundant native and endemic species from the nearby forests and
heathland;

c) Even if isolated in a moderately disturbed matrix, the general biotic and abiotic conditions
inside the complex canopies of these high altitude J. brevifolia trees will still favor the native and
endemic species during the recolonization process after the defaunation event, filtering out the
introduced species;

d) The lack of saturation in functional traits of indigenous species may imply lack of
resilience in the case of disturbance of the natural environment (Whittaker et al. 2014), leaving the
indigenous fauna of these isolated canopies vulnerable to further colonization and probable invasion
of exotic species with new traits during the recolonization process.

6
 Chapter 7

Chapter seven gives and overview of the present work and tries to convey to the reader the
particular characteristics of the canopy arthropod communities of the native Azorean forests, as well
as its resilience towards disturbance and invasion.

It will also strive to convey the role that isolated native trees in a moderately disturbed
matrix might have as reservoirs of indigenous arthropod fauna and as stepping stones, increasing the
interconnectivity between the extant patches of native forest.

Additionally, I will also supply in the form of Appendix I a list of all the identified arthropod
species associated with the canopies of J. brevifolia, I. perado subs. azorica and Laurus azorica in
Terceira island, which considering the present rates of biodiversity loss due to global changes could
be a valuable asset for future studies regarding changes in the Azorean ecosystems.

7
Chapter 2
Material and Methods

2.1. The Azorean archipelago: geography and climate

The Azores is an archipelago of volcanic origin, with nine islands and several small islets
and seamounts, located on the North Atlantic, on a WNW-ESE axis, between 37º - 40ºN and 25º -
31ºW. The archipelago extends for 615 km and is located approximately 1300 km West of mainland
Portugal (from Cabo da Roca). The islands form three distinct groups: the Eastern Group (Santa
Maria, São Miguel and the Formigas islets), the Central Group (Terceira, Graciosa, São Jorge, Pico
and Faial) and the Western Group (Flores and Corvo) (Figure 2-1). The islands have different
geological ages, with Santa Maria as the oldest island (6 Ma) and Pico as the youngest (0.27 Ma)
(França et al. 2003; Ramalho et al. 2017). The eastern part of each island tends to be geologically the
oldest (Forjaz 2004) and with the exception of S. Maria most islands have a large portion of their
area with less than 1.0 Ma.

Figure 2-1 Map of the Azores, with Terceira island singled out. Inset with the location of the archipelago in the Atlantic
Ocean.

8
 The archipelago sits on the Azores Plateau, a topographic and gravity high at the 2000 m
bathymetric line, characterized by a complex system of faults and ridges (Pacheco et al. 2003). This
plateau is on a triple plate junction, in the confluence of the North American, Eurasian and African
plates, in the proximity of the Mid Atlantic Ridge. The archipelago sits astride two tectonic plates,
with the westernmost islands, Flores and Corvo located in the North American plate, and the
remaining seven islands on the Azores Microplate, a roughly triangular microplate with complex
borders in the junction of the three aforementioned major tectonic plates (França et al. 2003, Nunes
et al. 2006).

The archipelago’s climate is mild, with high precipitation and high humidity, often reaching
an average annual relative humidity of 95% in the high altitude forests. The climate can be defined as
humid mesothermal with oceanic characteristics, being influenced by the effects of the warm Gulf
Stream. The surrounding ocean also dampens temperature fluctuations, causing low thermal variation
throughout the year (Azevedo et al. 2004). There is a marked seasonal lag in the archipelago. On
average, August is the warmest month and February the coldest, with a mean annual temperature of
17.5ºC. Average annual rainfall ranges from 700 to 1600 annual millimeters on average, reaching
6,300 millimeters on Pico Mountain, in Pico Island. Average annual rainfall increases from the
eastern to the western islands, with Flores and Corvo being the wettest islands and Santa Maria the
driest. The climate is also influenced by the Azores High, a semi-permanent anticyclonic region of
high atmospheric pressure usually found south of the archipelago.

There is a marked climatic stratification in each island, determined by altitude (Azevedo et

al. 2004), with the high elevations being strongly influenced by the prevailing winds and by the
almost constant nebulosity, that originate the montane cloud forest conditions of most remaining
native forests, with very high humidity, frequent showers and fog, and waterlogged soils (Azevedo et
al. 2004).

2.2. The terrestrial Azorean biodiversity

The Azorean terrestrial biota is currently composed by 6199 species and subspecies (about
6147 species), being 455 (414 species) of these endemic to the archipelago (Borges et al. 2010, with
additional updated data for arthropods). A large component of this biota are recent introductions,
with 47% of arthropods (excluding taxa whose colonization status was not possible to determine) and
81% of vascular plants being exotic (Borges et al. 2010, with additional updated data for arthropods).
There are currently 2333 arthropod taxa (269 endemics) reported to the Azores, corresponding

9
roughly to 37% of all terrestrial species. Fungi as a whole are the second most diverse group with
1328 taxa (34 endemics), followed by the vascular plants with 1110 taxa (73 endemics) (Borges et al.
2010). Bryophytes (sensu lato) account roughly for 7.7% of the biota, with 480 taxa, including seven
Azorean endemics. Land snails and slugs (Mollusca) are also a diverse group, with 114 taxa,
including 49 endemics (Borges et al. 2010, with additional updated data). Excluding fresh-water
fishes (13 taxa), all exotic, there are 58 vertebrate species occurring in the archipelago: 11 of which
are mammals (all introduced, except for four species of native bats including the endemic noctule
bat, Nyctalus azoreum Thomas) (Borges et al. 2010). Breeding birds are represented by 43 species,
including 11 endemic subspecies and two endemic species (Oceanodroma monteiroi Bolton et al.
and Pyrrhula murina Godman). Additionally, there are also two exotic species of amphibians and
two exotic species of reptiles (Borges et al. 2010).

2.3. The Azorean vegetation

Extant Azorean native forests are mainly montane cloud forests named as “Juniperus-Ilex
Montane Forests” and “Juniperus Montane Woodlands” (Elias et al. 2011, 2016). These are humid,
evergreen forests characterised by short tree stature, dense crown foliage and high tree density. The
Azorean cedar (Juniperus brevifolia) is the dominant tree in more exposed and wet environments.
Otherwise, the canopy is usually dominated by J. brevifolia and Ilex perado subsp. azorica. At lower
elevations, particularly in less exposed areas, Laurus azorica is also a common species (Elias 2007;
Elias et al. 2011, 2016). These forests are also characterized by a dense cover of mosses and other
epiphytes (Gabriel & Bates 2005) and shaped by several abiotic factors like the shallow soil layer,
fractured and craggy terrain (Ribeiro et al. 2005) and wind speed. Despite some climatic and floristic
differences, the Azores archipelago is included in the Mediterranean Basin Biodiversity Hotspot
(Médail & Myers 2004).

From the work of Frutuoso (2005a, 2005b), compiled from documents, oral tradition and
from its own travels to the islands, it is clear that forests dominated the Azorean landscape at the time
of discovery and settlement of the archipelago in the 15th century. Based on the classical proposal of
Dansereau (1970) the vegetation of the Azores could be divided in six altitudinal belts, characterized
by their dominant species: Morella faya (Ait.) Wilbur (0-300 m); Laurus azorica (300-650 m);
Juniperus brevifolia (450-1100 m); Erica azorica Hochst. ex Seub. (850-1600 m); Calluna vulgaris
(L.) Hull (1600-2200 m) and lichens (2200-2350 m). Palynological studies by Connor et al. (2012,
2013) provided us with some very important information about the recent past and historical native

10
vegetation of two Azorean islands, Pico and Flores. These studies added more evidence that
primitive Azorean vegetation was dominated by trees and that human impact had a strong influence
on the native vegetation. In fact, as a result of less than 600 years of human settlement, more than
95% of the native forest was destroyed by human action (Triantis et al. 2010b; Fernández-Palacios et
al. 2011; Silveira 2013), with most coastal, lowland and submontane forests [dominated by Morella
faya, Picconia azorica (Tutin) Knobl., Laurus azorica and Prunus azorica (Hort. ex Mouillef.) Rivas
Mart. et al.] being replaced by urban and agricultural areas. Most of the islands in the archipelago are
currently dominated in the lower elevations by sown pastures, agricultural fields and orchards,
abandoned fields, coastal habitats and urban areas (Borges et al. 2008) and at mid and higher
elevations by semi-natural pastures used for dairy and cattle farming, together with timber
plantations of exotic species like Cryptomeria japonica (L.f.) D. Don or Eucalyptus sp..

The extant pristine forest continues under threat due to habitat reduction, fragmentation and
invasive plants, with clear impacts on the flora and fauna (Borges et al. 2000; Cardoso et al. 2010;
Triantis et al. 2010b; Terzopoulou et al. 2015), and is now restricted to a few dispersed high-
elevation fragments above 500m altitude, with areas between 4 and 1300 ha (Borges et al. 2005a,
2006; Gaspar et al. 2008), totaling some 6000 ha (Gaspar et al. 2008; Gabriel et al. 2011).

2.4. The host-tree species:

As previously mentioned, Juniperus brevifolia, Ilex perado subsp. azorica and to some
extent Laurus azorica are the dominating tree species in the surviving Azorean native forests and for
this reason they were selected as the host tree species for my study. Despite some new developments
regarding the taxonomy of Ilex perado subsp. azorica, this work follows the nomenclature of Borges
et al. (2010).

2.4.1. Juniperus brevifolia (Seub.) Antoine

Juniperus brevifolia, the Azorean cedar or short-leafed juniper, is a dioecious shrub or tree,
with a trunk bark brown-purple, exfoliating in strips. Leaves are acicular, closely set, with two broad,
white stomatiferous bands on the adaxial surface. Seed cones are subglobose, green and pruinose
while young, dark copper-brown when mature. Seeds are free, ovoid and triquetrous (Adams 2014).
Sequences from nuclear and chloroplast DNA (trnC-trnD spacer) have placed J. brevifolia in a clade
with Juniperus navicularis Gandoger, that is endemic to western coastal areas of mainland Portugal

11
and it seems possible that seeds of J. navicularis-like plants or their ancestor were brought to the
Azores by birds from the Iberian Peninsula (Adams 2014). A study by Rumeu et al. (2011) suggested
that a single introduction event likely occurred from Europe and that genetic differentiation of J.
brevifolia post-dated the emergence of the oldest island (Santa Maria, 6.0 Ma, [Ramalho et al.
2017]).

Presently, two subspecies are recognized (Elias & Dias 2014): (1) J. brevifolia subsp.
maritima is an erect shrub or small tree, with (inverted) pyramidal crown; leaves: 5.6–7.6 × 1.4–1.8
mm; seed cones: 7.9–9.5 mm, ripening in the first year; seeds: 1–3 per seed cone, 4.9–6.3 × 3.5–5.1
mm, germinating from February to May; pollination occurs between January and March;
distribution: Flores, Terceira, Pico, São Jorge and São Miguel (?), below 100 m a.s.l.; and (2) J.
brevifolia subsp. brevifolia is a tree or shrub; leaves: 4.5–6.7 × 1.1–1.5 mm; seed cones: 6.9–8.7 mm,
ripening in the second year; seeds: 2-3 per seed cone, 3.9–5.3 × 2.1–3.7 mm, germinating from
March to June; pollination occurs between March and June; distribution: all Islands, except Graciosa,
usually between 300 m and 1500 m a.s.l. Two varieties have been recognized from the later
subspecies (Elias & Dias 2014): i) J. brevifolia subsp. brevifolia var. brevifolia (the dominant taxa) a
small to medium-sized tree, found mostly between 300 and 1000 m a.s.l., in all islands (except
Graciosa); and ii) J. brevifolia subsp. brevifolia var. montanum a small prostrate shrub, usually found
between 850 and 1500 m a.s.l. in the Islands of Flores, Terceira, Pico, São Jorge, Faial and São
Miguel. Overall, this species has wide ecological amplitude and it can be found from the coast to
1500 m a.s.l. (in Pico Mountain). Therefore, it has the potential to occupy all islands, at all altitude
ranges except Pico (which has a maximum altitude of 2350 m a.s.l.).

Presently, according to Elias (2007), J. brevifolia reaches higher values of abundance and
frequency between 500 and 800 m a.s.l. Between 800 and 1000 m a.s.l. frequency decreases, and
between 1000 and 1500 m a.s.l. abundance also decreases. Low winter temperatures, very high
rainfall, strong and frequent winds explain the decreasing abundance. Above 1500 m it is rarely
found, possibly due to the frequent snow cover during the winter in Pico Mountain. At lower
elevations, namely between 100 and 500 m (especially up to 300 m) it becomes rarer, not only due to
human induced habitat changes but also, in the remaining natural or semi-natural areas, due to the
competition with tree species with higher stature (e.g. Morella faya, Laurus azorica and Picconia
azorica). Furthermore, since J. brevifolia is a pioneer species (Elias & Dias 2009), low frequency
and intensity of gap creating natural disturbances at these low altitude ranges might also explain this
pattern. Below 100 m a.s.l. there is a small increase in abundance and frequency due to the presence
of subsp. maritima in coastal scrubs.

12
 Once present in all islands, this species is now extinct in Graciosa and near extinction in
Santa Maria. In the islands of São Miguel, São Jorge and Faial, J. brevifolia populations have been
greatly reduced or highly fragmented. This decline was due to centuries of human exploitation of
natural resources. It is well-known that the species was used since human settlement for naval and
house construction, for furniture and as fuel (Frutuoso 2005a, b). In addition, extensive dairy farming
in the last decades led to widespread clearing of forests for pasture, further decreasing populations of
J. brevifolia (Silveira 2013). Nevertheless, it is still possible to find pristine Juniperus forests in
Flores, Pico and Terceira (Elias et al. 2011). This species is also found in coastal scrubs, in pioneer
and secondary scrubs and in forested peat bogs (Elias & Silva 2008). It is protected both by national
and international laws and a few studies have been developed to characterize the genetic variability
of the species for conservation and restoration purposes (e.g. Silva 2000; Silva et al. 2011).

2.4.2. Ilex perado Aiton subsp. azorica (Loes.) Tutin

Ilex perado subsp. azorica, the Azorean holly, is a dioecious shrub or small tree with smooth
bark that can grow up to seven meters tall. Leaves are simple, obovate, acute, glabrous and often
spiny, with few forward pointing spines. Leaves up to 6 x 5 cm. Flowers are axillary, actinomorphic
and in fascicles. Petals are white and fused at the base. Corolla up to 5 mm. The is a red, globose
berry with up to 8 mm in diameter. The fruit contains 4-5 seeds. Pollination occurs between April
and May (Schäfer 2002).

This subspecies is endemic to the Azores, being present in all islands (Silva et al. 2010).
Sosa et al. (2013) suggested the taxonomic revision of subsp. azorica in order to recognize this taxon
as an endemic species.

This species can be found scattered in ravines, and in laurel, juniper or Pittospurum forests
between 250 and 750 m (Schäfer 2002) and also in exposed areas, mountain scrubland, Juniperus
forested peat bogs, or boggy Ilex forests. It can also be found in the pioneer vegetation of young lava
flows (Silva et al. 2009). According to Elias et al. (2016), Ilex perado subsp. azorica is one of the
dominant species in Juniperus-Ilex montane forests.

This species is under threat from habitat degradation and fragmentation, changes in land use
and invasion by alien species (Silva et al. 2009). The species is currently only under protection by
the Regional Government Decree (Decreto Legislativo Regional nº 15/2012/A).

13
 2.4.3. Laurus azorica (Seub.) Franco
Laurus azorica, the Azorean laurel, is a dioecious shrub or small tree with a trunk up to 35
cm in diameter and can grow up to 13 meters tall. Young twigs and leaves are densely brown-
tomatose. The leaves are elliptic, oblong or obovate, more or less acute and aromatic. Leaves can be
up to 15 x 6 cm. Inflorescence is subsessile, with actinomorphic pale-yellow flowers. The perianth is
4-lobed, with segments of approximately 4 cm. The fruit is a black ellipsoid berry of 1-2 cm.
Pollination occurs between December and April (Schäfer 2002).

The species is endemic to the Azores and is present in all islands (Silva et al. 2010).

It can be found scattered in ravines and steep slopes. In altitudes up to 850 m it can also be
found in Myrica-Pittosporum forests (Schäfer 2002). It can also be found in lava flows, the margins
of cultivated fields, in mountain scrubland, in laurel, Ilex and Juniperus forests and in forested peat
bogs (Silva et al. 2009). Laurus azorica is the dominant species in Laurus submontane forests being
also very frequent in Juniperus-Ilex montane forests (Elias et al. 2016).

This species is under threat from habitat degradation and fragmentation, changes in land use,
use in forestry and invasion by alien species (Silva et al. 2009). The species is currently only under
protection by the Regional Government Decree (Decreto Legislativo Regional nº 15/2012/A).

2.5. The Terceira Island

Terceira island, located at approximately 38º44’N and 27º12’W, is elongated in the W-E
axis, being roughly 30 km long and 19 km wide, has an area of 402 km2 and a maximum altitude of
1021 m (Serra de Santa Bárbara) (Figure 2-2). The oldest parts of the island have approximately 3.52
Ma, with the most recent lava fields dating from the 1761 eruption of Mistérios Negros, Pico Gordo
and Pico do Fogo (Pacheco et al. 2013). The island is still volcanically active, with fumaroles and
recent underwater eruptions (e.g. the Serreta eruption in 1998-2001; Pacheco et al. 2013, Marques et
al. 2014).

Terceira Island, like the other islands in the archipelago, is the aerial portion of an
underwater mountain that rises from the Azores Plateau, formed by the accumulation of volcanic
deposits. The island is characterized by six main geomorphological features, the five volcanic
complexes of Cinco Picos, Guilherme Moniz, Pico Alto, Santa Bárbara and the basaltic fissural zone,
and by the Lajes Graben. These volcanic complexes correlate with the different stages of the

14
formation of the island (Zbyszewski et al. 1971, Nunes 2014), with what is now the Cinco Picos
complex being the first to emerge above the sea surface, as a great shield volcano.

The island is also greatly influenced by the Terceira Rift, with its main volcanic and tectonic
features following WNW-ESE and NW-SW axes (Machado 1959).

Figure 2-2 Map of Terceira Island, with its different Nature Reserves, Protected Areas and Natural Monuments. Terra-
Brava Nature reserve marked with a red arrow (source: DROTRH 2008).

As with the remaining of the archipelago, climate is mild and humid. August is the warmest
month (mean temp 22.2ºC) and February the coldest (mean temp 13.8 ºC), with a mean annual
temperate of 17.5ºC (data for Terceira/Angra, IPMA 2015). Average rainfall at low altitudes (Angra
do Heroísmo) is of 969 mm/year, while on Serra de Santa Bárbara is of 3000 mm/year. Maximum
rainfall occurs on average in December, January and February and minimum in July (

Figure 2-3).

There is no certain date for the discovery of Terceira island, but the portolan chart of Gabriel
Valsecca from 1439 gives the Azores as discovered in 1427 (Marques 1987, Rodrigues 1995), while
a royal charter of king Afonso V, dated from July 1439 (DGARQ 2016, cf. Rodrigues 1995)
commands the release of livestock in the seven islands of the Azores discovered at the time and

15
allows its settlement. It is certain that Terceira island was discovered after São Miguel and Santa
Maria (Drummond 1981, Frutuoso 2005a), but the dates of its initial settlement are uncertain, having
occurred between 1450 and 1460 (Drummond 1981, Frutuoso 2005a).

Currently the island has a population of over 56437 inhabitants and cattle raising and dairy
farming being the main economic activities, although there has been in the last years a sharp increase
in tourism and tourism related activities Once covered in native forest, 600 years of human presence
left only several isolated forest patches, with some 31% of the island area being covered by
intensively managed pastures (Florencio et al. 2016), while the extant pristine native forest in
Terceira has a total area of only some 2500 ha (approximately 6% of the land area), with most of the
patches being located above the 500 m (Gaspar et al. 2008, Florencio et al. 2016).

Figure 2-3 Average monthly temperatures, average maximum and minimum temperatures, and temperature extremes
(top); and precipitation monthly averages and daily maximums for Angra do Heroísmo between the years of 1981 and
2010 (source: IPMA 2015).

16
 2.5.1. Terra-Brava study plot
A 50 m x 50 m study plot located in the Terra Brava nature reserve (see Figure 2-2) was
established in 2012 for the NetBiome project (Cicconardi et al. 2017; Emerson et al. 2017). The plot
is at 38º 43’ 56.2”N and 27º 11’ 51.1”W and 861 m above sea level (plot centre), facing East, on the
leeward side of a hill. Incline inside the plot was of 14%.

Inside the plot, the Azorean cedar (J. brevifolia) is the predominant tree species, accounting
for 87% of the 294 trees with trunks with more than 10 cm of DBH, followed by Ilex perado subsp.
azorica with 9% of the trees. Average DBH for J. brevifolia inside the plot is 16.50 cm, 15.6 cm for
L. azorica and 14.8 cm for I. perado subsp. azorica. Basal area for J. brevifolia was 23.6 m2/ha,
followed by I. perado subsp. azorica with 1.9 m2/ha, out of a total basal area of 26.6 m2/ha. Average
canopy height in the plot was of 5 m and there were no introduced tree species present (Rui Elias,
unpublished data/personal communication).

The plot was selected for the fogging project due to my previous knowledge of the terrain
and its relative ease of access and movement within, coupled with the presence of many adult
specimens of Juniperus brevifolia and several of Ilex perado subsp. azorica. Laurus azorica was the
least common of tree species of interest to my study in the plot, but it was present in sufficient
number in the plot near its exterior margins. Ease of access and movement in the plot was an
important logistical consideration, owing to the bulky nature of the fogger machine and the amount
and weight of all the necessary material. Another important factor in the selection of the location was
that, in the plot, the trees were present in a more or less single canopy layer, with facilitates the
collection of fogging samples (Adis et al. 1998) and despite the dense and interlocked nature of the
canopies, this plot had enough trees of all three species with sufficient crown demarcation and little
overlapping with neighboring trees, which is also a desirable prerequisite (Adis et al. 1998).

Additionally, the plot is considered to be located in a pristine area (Gaspar et al. 2011) and
was also the location of a long-term arthropod monitoring project with SLAM traps, with monthly
sampling (see Borges et al. 2017 for some preliminary results), allowing to measure temporal and
seasonal fluctuations in the arthropod community.

2.5.2. Tree individual’s selection (Native forest)

The selection of the trees was performed in the late spring of 2013, with the aim of doing a
preliminary study of the insect communities with the use of sticky flight-intercept traps (Rui Nunes,
unpublished data) and then progressed with the pyrethrum knockdown experiment.

17
 Initially I tried to select the trees in a random way, by numbering as many trees as possible
of each species (less for I. perado subsp. azorica and for L. azorica, due to lower abundance) inside
the plot and then selecting seven of each by generating random numbers in R. This approach was
flawed, since many of the trees were not adequate for the experiment and I was forced instead to
select the trees for this study in a non-random way. In fact, the selected trees needed to have a
minimum Diameter at Breast Height (hereafter DBH) of 10 cm, with no neighboring overstory
canopies or developed understory vegetation, and with a minimum of canopy contact with nearby
trees. Due to the closed structure of native Azorean forests, trees with completely isolated canopies
are very difficult, if not impossible to find, so, some compromises had to be made. A total of seven
specimens of each tree species were selected this way.

Following Dias (1996) on tree measuring and general guidelines for canopy fogging (Adis et
al. 1998), I measured the DBH, total height, start of crown height, and two measures of crown
diameter (perpendicular to each other), which, besides giving me some basic morphometrics for each
tree, also allowed me to calculate their canopy areas (as a circle) and volumes (as a cylinder). After
the first fogging events in 2014, my understanding of the intricacies of this technique grew and I
realized that some of the trees that I had non-randomly selected were, for diverse reasons, unsuitable
for my intents. Consequently, new trees with more desirable characteristics were found and selected.
Unfortunately, these were not measured a posteriori, due to a combination of lack of necessary
equipment at the time and posterior oversight. Average height for the selected and fogged trees was
of 4,6 m, with the lower parts of the canopy on average 2.8 m from the ground. Average canopy area
was of 14.7 m2, with a canopy volume of 25.5 m3 (Table 2-1).

To facilitate the mapping of the sample plot, a colored nylon rope was set along the edges of
the plot and marked at five meter intervals with high visibility tape, to create a virtual map grid. The
approximate position of each selected tree was mapped in the grid and was attributed an individual
code (Figure 2-4 and Table 2-1). Simultaneously this code was written on a colored plastic card with
permanent black marker and attached to the trunk or to a main branch of the corresponding tree via
plastic zip ties. Care was taken to test if the marked codes were able to withstand the high humidity
conditions inside the forest.

To aid in finding the individual trees, one or two lengths of white-red construction tape were
also tied to the branches.

18
Figure 2-4 Grid map of the Terra Brava-B study plot, with the approximate position of all the fogged trees for 2014 and
2015. cf. with Table 2-1.

For the 2015 sampling season, three additional specimens of each tree species were selected,
to act as controls, following the same selection criteria. These trees were also selected with the
additional criteria of being as far as possible from the trees fogged in 2014, thus some were located
outside the study plot, but not further than five meters from its edges.

The summer of 2014 was rather unstable in terms of weather conditions, with many days of
wind, heavy fog or showers greatly hindering the fogging attempts and extending the duration of the
sampling period into almost three months. Compounding this issue there were some mechanical
problems with the thermal fogger, which sometimes hindered the attainment of an ideal
concentration of insecticide fog in the canopies and forced me to stop for several days with the
fogging attempts, to take the machine apart and clean or repair several components. The net effect of
these two problems was that I was unable to fog all the trees that I had initially planned to before the
end of the summer/sampling season.

19
Table 2-1 Summary table with each tree fogged in the forest experiment, its identifying code, years of first and second
fogging (when applicable), and several individual metrics, namely DBH (Diameter at Breast Height) in centimeters, total
height, canopy area and canopy volume. Several L. azorica specimens had more than one main trunk; in that case all
DBH’s are presented, with the sum in parenthesis. 1t – First time fogging; 2t – second time fogging; Ex – control tree.
Canopy Canopy volume
Tree species Tree code 2014 2015 DBH (cm) Height (m)
area (m2) (m3)
I. perado I5 1t 2t 15.1 4.06 15.2 20.68
I. perado I8 1t 2t 11.15 3.9 8.4 17.69
I. perado I22 1t 2t 14.7 5.8 13.9 41.56
I. perado I24 1t 2t - - - -
I. perado I25 1t 2t 12.25 4.4 17,7 35.44
I. perado I29 1t 2t 12.9 4.4 9.1 14.98
I. perado IEx 1 - 1t - - - -
I. perado IEx 2 - 1t - - - -
I. perado I20 (IEx 3) - 1t 14.7 5.8 19.6 41.56
J. brevifolia J3 1t 2t 22 4.5 9.5 13.28
J. brevifolia J5 1t 2t 19.4 4.3 10.8 15.38
J. brevifolia J10 1t 2t 18 5 8.6 22.24
J. brevifolia J12 1t 2t - - - -
J. brevifolia J41 1t 2t 25.5 4.8 26.0 51.93
J. brevifolia J50 1t 2t 22 4.5 26.0 33.76
J. brevifolia J52 1t 2t - 3 33.2 46.46
J. brevifolia JEx 1 - 1t - - - -
J. brevifolia JEx 2 - 1t - - - -
J. brevifolia JEx 3 - 1t - - - -
L. azorica L7 1t 2t 10.2 3.6 13.9 15.24
L. azorica L14 1t 2t 10.2+8.0+7. 4.7 8.0 15.28
3 (25.5)
L. azorica L12 1t - 10.5+8.2 5.5 4.0 10.48
(18.7)
L. azorica LEx 1 - 1t - - - -
L. azorica L26 (LEx 2) - 1t 10.4+8.8+6. 4.3 14.2 23.41
1 (25.3)

To this effect, only 16 trees in total were fogged in 2014 (six I. perado, seven J. brevifolia
and three L. azorica). In the 2015 sampling season all these trees were refogged (with the exception
of one L. azorica specimen that died) (Table 2-1). In the 2015 season I also fogged for the first time
the newly selected control trees mentioned above, with the caveat that only eight new trees were
sampled (three I. perado, three J. brevifolia and two L. azorica) (Table 2-1) due to an oversight
magnified by time constraints related with some of the field material.

20
 2.5.3. Semi-natural pasture study site
The third part of my experiment took place in a semi-natural pasture, also in the Terra-Brava
nature reserve.

Several locations were considered for this experiment, but the lack of sufficient trees to
allow for replication and logistic considerations in terms of access were limiting factors. Excessive
distance to the native forest patch was also a consideration, as different abiotic conditions and land
use history could influence comparisons between both faunas. Therefore, I ended up selecting a
small pasture located inside the Terra Brava nature reserve. This study targeted only specimens of the
Azorean cedar, as this was the only tree, of those that I was interested in, that tended to appear
isolated in pastures.

This pasture is about 450 m long, with a maximum width of 100 meters in the area where I
collected my samples. Lengthwise, this pasture is divided by a small ridge, with one third on a South
facing slope and the other two thirds on a South-southeast facing gentle slope. The pasture is
delimited on its S and SSE portions by a road, and on the northern part, by native heathland and
forest (Figure 2-5). This pasture is mainly covered by Anthoxantum odoratum L. and Holcus lanatus
L. (and has several short stature specimens of J. brevifolia, with the canopies clearly shaped by the
trade winds.

Figure 2-5 Map of the semi-natural pasture in Terra Brava, with the relative position of the trees fogged in 2015 (red
stars) and in 2016 (blue stars).

21
 Several trachyte boulders and outcrops dot this pasture, with some Azorean cedars growing
on top, or partially protected by them. At the end of the SSE slope there is also a group of J.
brevifolia trees on the edge of a 2 meter high barrier overhanging the road. This pasture was created
in the eighties, by clearing of native forest (Fernando Pereira, personal communication). From
personal observation, this semi-natural pasture is occasionally used for grazing by “gado-bravo”, the
breed of cattle used in the traditional bull runs of Terceira.

2.5.4. Tree selection (semi-natural pasture)

After terminating the fogging experiments in the forest in August of 2015, three specimens
of J. brevifolia were selected. Taking into consideration the distinct characteristics of the trees
present in the pasture, and the future selection of replicates, I opted for selecting one tree that was
standing alone in the pasture, another on a trachyte outcrop and the last one on the cluster of trees
overhanging the road. In 2016, three extra specimens of J. brevifolia were selected in the same
pasture. In trying to replicate the particular conditions of the trees fogged the previous year, I also
selected an isolated tree in the pasture, another in a trachyte outcrop and one in the same cluster
overhanging the road (Figure 2-5 and Erro! A origem da referência não foi encontrada.). A sudden
shift in the weather conditions prevented the sampling of this last tree.

All trees were of fairly similar heights and canopy volumes, and no less than 10 meters apart
from each other or from the edges with native vegetation. All sampled trees were on the SSE facing
slope of the semi-natural pasture.

Table 2-2 Table with each J. brevifolia tree fogged in the semi-natural pasture experiment, its identifying code, and years
of first and second fogging, when applicable. P - pasture; 1t – First time fogging; 2t – second time fogging.
Tree species Tree code 2015 2016

J. brevifolia JP-1 1t 2t

J. brevifolia JP-2 1t 2t

J. brevifolia JP-3 1t 2t

J. brevifolia JP-4 - 1t

J. brevifolia JP-5 - 1t

22
 2.6. Canopy fogging – Brief history and suitability of the method

Forest canopy arthropod communities are some of the richest on Earth, and until some
decades ago, also one of the least well known (Blanton 1990), a situation only reverted with the first
pioneering studies with pyrethrum knockdown, particularly in tropical forests, where the height of
the trees severely limited access to the canopies by more conventional techniques (Stork &
Hammond 1997). A diversity of methods was used to apply natural pyrethrum compounds or
synthetic pyrethroids to the canopies, like hydraulic spraying (Martin 1966, Gagné & Martin 1968,
Southwood et al. 1982), insecticide smoke canisters (Kikuzawan & Shidei 1966, see also Watanabe
1997) or “true” fogging techniques (Gagné 1979, Erwin 1983a, Stork 1988). Despite being
analogous to “true” fogging, hydraulic spraying and smoke canisters present their own problems,
with spraying having difficulties in penetrating dense clusters of foliage, epiphytes or bark crevices,
and smoking working better on conifers, both being also limited by tree height (Erwin 1990).

The first use of a true insecticidal fog to sample canopy communities was that of Roberts
(1973), although he used Dichlorvos (DDVP), an organophosphate as insecticide. Gagné (1979) was
the first to use a resonant pulse-jet fogger (a Dyna-fog) with pyrethrum synergized with piperonyl
butoxide, being followed by a wealth of other studies using this same principle and with constant
refinements (Erwin 1983b, Adis et al. 1984, Stork 1988). The methods for collecting the falling
arthropods also changed through time, with the first studies using large suspended cloth sheets, or
sheets in the ground (Martin 1966, Roberts 1973, Gagné 1979), with its own set of problems (see
Stork & Hammond 1997). These designs suffered several improvements along the years (Erwin
1983a, b, Allison et al. 1993, Stork & Hammond 1997), with 1m2 funnels with detachable bottoms
being the recommended standard (Adis et al. 1998).

A more detailed account of the history of canopy fogging can be found in Erwin (1983b,
1990).

As a technique, canopy fogging (or pyrethrum knockdown) has the chief quality that its
samples are a close reflection of the canopy arthropod community, irrespectively of the surface they
are on (leaves, branches, flowers or fruits) or their activity. This allows for samples comparable with
each other, despite being from distinct latitudes and altitudes, collected in different times of the year
and along different forest types and host tree species (Stork & Hammond 1997), being well suited for
quantitative and comparative studies (Gruner 2007, Kehlmaier & Floren 2010). It also dispenses with
attractants and other biases connected with activity-based traps. Due to the nature of the fog, this

23
technique also allows the collection of specimens that would be hard to collect by other means
(Hsieh & Linsenmair 2011).

Additionally, if used without a synergist in the insecticide formulation, this technique can
even allow the capture of live specimens (Paarmann & Kerck 1997, Adis et al. 1997), enabling for
the rearing of juveniles, investigation of life history strategies, food preference experiments or
behavioral studies with canopy arthropods (Paarmann & Stork 1987, Paarmann & Paarmann 1997).
These characteristics and the comparable nature of the samples make fogging a particularly useful
tool.

However, this technique also has its disadvantages, in particular its susceptibility to adverse
weather conditions in general and wind in particular (Gagné 1979, Stork & Hammond 1997,
Horstmann et al. 1999, Marske et al. 2007). Due to the small particle size of the fog droplets, these
can be easily carried away and dispersed by the wind, preventing the necessary concentration of
insecticide in the canopy and conversely, the dispersal of insecticide to nearby trees, causing
unwanted mortality and/or sample contamination. Rain or wet foliage also prevent the application of
this technique. Wind can also cause drift in the falling arthropods, especially small, winged
specimens, causing them to miss the collection funnels.

Certain arthropod groups are also less susceptible to be collected using this method, namely
wood-borer, leaf-mining and leaf-rolling species (Adis et al. 1984, Stork & Hammond 1997), as well
as species that live in nests (Adis et al. 1984), under the tree bark, or deep inside crevices and
inflorescences. Scale insects and other phloem feeders are also susceptible to remain attached by
their stylets (Stork & Hammond 1997). Spiders and some Lepidoptera larvae might also stay
suspended by silk threads (Adis et al. 1984, Stork & Hammond 1997). Arthropod fauna that lives in
mosses and epiphytes is also another group that might be underrepresented in fogging samples
(Yanoviak et al. 2003, Grunner 2007)

Finally, this technique can be quite labor intensive, and the costly and bulky equipment are
factors that need to be taken into consideration.

Based on current knowledge, if the minimum technical requirements are achieved,

pyrethrum knockdown is a highly effective technique. In fact, this technique has almost immediate
results, as the majority of the arthropods fall down in the first hour (Adis et al. 1997, Paarmann &
Kerck 1997), or even in the first 20-30 minutes after fogging (Stork 1991, Allison et al. 1993). In
addition, the defaunation effect seems to be almost complete, as indicated by a posteriori visual
inspections that “suggest that few insects are left on the leaves” (Stork 1991), this being confirmed

24
by Erwin (1990). Of course, as pointed out by Basset et al. (1997) no technique alone is a universal
panacea, and it is advisable to conjugate complementary techniques.

Branch beating is one the arthropod collection techniques usually employed in previous
works in the Azores, with good results (Ribeiro et al. 2005; Gaspar et al. 2008), particularly given
the generally low stature of the Azorean trees (Ribeiro et al. 2005). The use of this technique in
conjunction with pyrethrum knockdown had already been suggested by Kuria et al. (2010), or in an
analogous way, by shaking the whole trees (Southwood et al. 1982, Marques et al. 2001). Both
complementary methods were feasible for my work, given the general architecture and stature of the
trees in Azorean native forests. In addition, given the prevalence of epiphytes on the trunks and
branches of native forest trees (Gabriel & Bates 2005), as well as the dense nature of the foliage,
particularly in the case of J. brevifolia, the use of these technique(s) in conjunction with fogging will
help in overcoming the aforementioned limitations of canopy fogging regarding sampling epiphyte
fauna (Yanoviak et al. 2003), or limitations regarding specimens staying attached to the surface of
the leaves or suspended from silken threads.

To sum up, canopy fogging/pyrethrum knockdown is an arthropod sampling technique that

gives us the possibility of taking a “snapshot” of the canopy community as a whole. Additionally,
this method, unlike any other used to sample canopy communities, allows for the (almost) complete
defaunation of the targeted tree (Erwin 1990, Stork 1991), enabling recolonization studies. Also,
given that this study took place inside a protected area, the low physical impact of its
implementation, associated with the very short half-life of the insecticidal agent used are two
desirable characteristics that have to be taken into account (Stork & Hammond 1997).

Besides this, the sheer volume of studies worldwide that have used pyrethrum and the
relevance of their contributions to the better understanding of the canopy communities, attest the
suitability of using this method in my study.

2.7. Material/equipment

I used as insecticide agent a solution of 0.38% pyrethrins with cinerins, synergized with
piperonyl butoxide in clear kerosene, with the commercial name of Pibutrin 33 (Liscampo) and this
was administered via a Curtis Dyna-fog Golden Eagle Model 2610E, Series 3, Electric Start hand-
held thermal fogger (Curtis Dyna-Fog Ltd., Dayton, Ohio, USA).

25
 Square funnels made of clear heavy duty polythene sheeting, with an area of 1 m2 and with
an aperture in the center with a coupling for a 500 mL polyethylene bottle were used to collect the
fogging samples. Branch beating was done with a standard wooden hoe handle. Samples were stored
in 98% ethanol. Despite the low toxicity to humans of the insecticide formulation used, a Vito 757-S
half-mask with 757 A1 filters (Corgaluz, Lobão - Santa Maria da Feira, Portugal), together with
protection goggles, heavy duty rubber gloves and a rubberized raincoat were used as protective gear.
These last two items proved highly impractical in the standard heat and humidity conditions
encountered in the native forest and were quickly discarded. The half-mask and nitrile gloves were
also used whenever handling the insecticide formulation.

2.7.1. Fogger
The Curtis Dyna-fog Golden Eagle Model 2610E, Series 3 thermal fogger (Fig. 2-6) is a
hand-held fog generator that operates on the resonant pulse-jet principle to generate a high velocity
stream of hot gases. The Curtis Dyna-fog Golden Eagle model has been one of a few commercially
available thermal foggers used for canopy fogging studies along the years (Erwin 1983a, 1983b, Adis
et al. 1984, Allison et al. 1993, 1997, Grunner 2007, Marske et al. 2007).

The engine itself consist of a long exhaust tube with a combustion chamber at one end and
an intake valve through where the fuel-air mixture is admitted.

Figure 2-6 Curtis Dyna-fog Golden Eagle Model 2610E, Series 3 hand-held thermal fogger. (Photo by the author)

26
 The insecticide formulation is kept in its own independent reservoir, and during the fogging
procedure is injected midway through the exhaust tube via a nozzle, where the high velocity gases
atomize the formulation instantaneously, with very little formulation breakdown. The formulation is
atomized into very small droplets, resulting in a non-moistening warm fog that rises naturally
through the air due to convection and is able to reach into the cracks and crevices in the bark, dense
foliage and mosses and other epiphyte masses (Otto & Floren 2007, but see Yanoviak et al. 2003).
Formulation output is of approximately 1600 cubic meters per minute
(http://www.dynafog.com/products/insect-vector-control/handheld-thermal/golden-eagle/).

Fog particle size is adjustable and ranges from 0.5 to 50 microns via a regulator. The fogging
was performed with the fog regulator control dial set to ‘5’ (intermediate particle size) (Erwin 1983a,
1983b, Alison et al. 1993, 1997). This setting was also recommended by the device’s owner (Serpa,
personal communication).

The pulse jet engine operates on standard 95 octane gasoline. The initial source of ignition is
a spark plug powered by an electronic ignition system. After original ignition the repeated cycles are
sustained by a glow coil which is an integral to the engine tube assembly, dispensing with the
electrical power source.

The standard power unit of this device consists of eight 1.5V D-batteries, but the original
battery rack had been previously removed by the owner and the wiring altered to work plugged to a
standard 220V outlet via a 12V transformer. This made using the machine in the forest impossible. A
solution was devised by me, using a 12V power pack made from two standard 6V motorcycle
batteries wired in parallel.

2.7.2. The insecticide

As insecticide agent, a solution of 0.38% pyrethrins with cinerins was used, synergized with
piperonyl butoxide in clear kerosene, with the commercial name of Pibutrin 33 (Liscampo).

Pyrethrins are natural organic compounds with a strong insecticidal activity, present in
chrysanthemum flowers and other species from the Asteraceae family (Hitmi et al. 2000), with
pyrethrum being the crude oleoresin extracted from the dried chrysanthemum flowers. Most of the
current industrial production of natural pyrethrum is derived from the Dalmatian chrysanthemum,
Tanacetum cinerariifolium (Trevir.) Sch.Bip., syn.: Pyrethrum cinerariifolium Trevir.,
Chrysanthemum cinerariifolium (Trevir.) Vis. (Hitmi et al. 2000, Grdiša et al. 2009). Pyrethrins are a
set of six structurally related monoterpene esters produced by esterification of two monoterpenic

27
acids (chrysanthemic acid and pyrethric acid) with three ketone alcohols (pyrethrolone, cinerolone,
and jasmolone). The chrysanthemic acid esters are called pyrethrin I, cinerin I, and jasmolin I,
respectively, and the pyrethric acid esters are called pyrethrin II, cinerin II, and jasmolin II (Hitmi et
al. 2000, Isman 2006, Grdiša et al. 2009). Pyrethrins have a neurotoxic action over both the
peripheral and central nervous systems of arthropods, blocking the voltage-gated sodium channels in
nerve axons (Isman 2006). Pyrethrins act by initially stimulating the nerve cells to produce repetitive
discharges, eventually causing paralysis. Only a small fraction of the sodium channels need to be
modified by pyrethrins for the generation of repetitive discharges. After modification of the channels
by pyrethrins, these remain open, as the insecticide impedes channel closing by either inactivation or
deactivation, and the sodium channels retain the ability to conduct Na+. The membrane potential is
shifted so that the nerve cells function in a new state of abnormal hyper-excitability. In arthropods
this produces an incapacitating, but sub lethal effect, known as ‘knockdown’. The amplitude of the
sodium current continues undiminished until the level of hyper-excitability overwhelms the capacity
of the cell to maintain the activity of the sodium pump (Davies et al. 2007). Due to their ability to
induce repetitive firing in axons, type I pyrethrins are good knockdown agents, their action resulting
in restlessness, loss of coordination and hyperactivity of the animal, followed by prostration and
paralysis. The type II compounds cause a pronounced convulsive phase that results in higher
mortality because of the irreversible depolarization of the nerve axons and terminals (Davies et al.
2007).

Piperonyl butoxide (PBO) is a synthetic organic compound used as a synergist in insecticide

formulations. This substance has no pesticidal activity of its own but enhances the potency of the
pyrethrins, allowing for lower concentrations to be used with higher efficiency (National Pesticide
Information Center). The kerosene has the dual purpose of acting as a carrying agent for the
pyrethrins and as a visibility agent, creating a thick cloud of white smoke that aids in directing the
insecticide and in gauging when an optimal concentration of fog is achieved in the canopies.

An insecticide solution with a higher concentration of pyrethrins would have been preferable
(Adis et al. 1997, Stork & Hammond 1997, Adis et al. 1998), but the choice of insecticide solution to
be used in this study was limited by Portuguese and EU legislation (Oliveira & Henriques 2012).

Pyrethrins are becoming one of the most common class of pesticides in use and are gradually
replacing organophosphates and organochlorides due to their low toxicity to humans and low
persistence in the environment. These compounds are arthropod specific and have relatively low
toxicity to most mammals and birds (Otto & Floren 2007), being metabolized in the liver into
harmless compounds and passed out of the organism. Pure pyrethrins are moderately toxic to

28
mammals (rat oral acute LD50 values range from 350 to 500 mg/kg), but technical grade pyrethrins
are much less toxic (approximately 1500 mg/kg) (Isman 2006). Pyrethrins are biodegradable, being
quickly broken down by sunlight and UV radiation (Stork 1991, Hitmi et al. 2000, Horstmann et al.
2005, Otto & Floren 2007, Grdiša et al. 2009, National Pesticide Information Center). They are also
susceptible to contact with air and to changes in pH, as well as having lower toxicity at higher
temperatures (Davies et al. 2007). Pyrethrins in general break down rapidly in water and on soil and
plant surfaces, in the presence of light. Half-lives of pyrethrins on field-grown tomato and bell
pepper fruits of not more than two hours have been reported (Antonious 2004), while half-lives on
soil surfaces are of 12.9 hours (National Pesticide Information Center). Pyrethrin I breaks at a slower
rate in the absence of light, with half-lives of 14 to 17 days being reported (National Pesticide
Information Center). As with the pyrethrins, piperonyl butoxide is quickly broken down in the
presence of sunlight, with a half-life of 3.4 hours in air. In shallow soil exposed to sunlight, half-lives
ranged from one to three days, while without sunlight a typical half-life for piperonyl butoxide in the
soil is of approximately 13 days (National Pesticide Information Center).

2.7.3. The collection funnels and bottles

The collection funnels used in this study were a direct adaptation made by me of the general
design used in other fogging studies (Allison et al. 1993, Stork & Hammond 1997, Schulz & Wagner
2002), following the recommendations for standardization of Adis et al. (1998). They were made of
clear heavy duty polythene sheeting squares, with an area of 1 m2 (Figure 2-7). The corners of each
funnel were reinforced with an extra patch of glued plastic sheet. Each corner had a hole punched in,
to which a brass grommet was set. These four reinforced holes served to pass the suspension ropes.
An aperture in the center of each funnel was then cut, to which a coupling for the collection bottle
was glued with contact glue. These couplings were made from the lids of collection bottles, with the
center removed.

When suspended in the field, some slack was allowed in the suspending ropes, which
combined with the weight of the coupling and of the collection bottle with alcohol at the center,
allowed the plastic sheet to form a smooth, shallow funnel (Fig. 2-7)

The collection bottles used in this work were wide-mouth 500 mL translucent low-density
polyethylene bottles (Normax - Fábrica de Vidros Científicos Lda, Marinha Grande, PORTUGAL).

29
 Figure 2-7 Array of collection funnels with bottles attached, suspended under a canopy (Photo: Gergely Erno).

2.8. Canopy fogging sampling protocol

For logistic reasons, the sequence by which the previously selected trees were fogged
followed the contour of the terrain inside the study plot, starting with the trees that were closer to the
access to the plot. To avoid contamination by nearby fogging, selected trees that were in close
proximity would be fogged together.

As previously stated, the fogging technique is sensitive to weather conditions, and on several
occasions, fogging procedures had to be aborted just prior to fogging or during the setting of the
collection funnels due to sudden rains or to shifting wind conditions. There were also many days in
which despite favorable weather forecasts and good weather conditions in Angra do Heroísmo,
adverse meteorological conditions at the study site prevented any fogging procedure, particularly
during the 2014 season.

Before leaving for the field, the fogger was inspected, the fuel level checked, and then the
machine would be started and left to run for some 30 seconds. As the formulation container was kept
in the study plot, hidden in a crevice and protected from sunlight, the level of insecticide in the
fogger’s reservoir was checked after entering the plot, and replenished if necessary. After these initial
preparations the set up for the fogging procedure would begin. After selecting which trees I would

30
try to fog that given day, their ID labels were checked and the position confirmed on the grid map of
the plot. The collection funnels would be shaken and inspected for debris, and afterwards set under
the canopies of each tree, suspended using nylon ropes from the trunk and branches of the tree to be
fogged and if necessary from nearby trunks, branches or other vegetation or terrain features. Despite
being constrained by the terrain and suitable anchoring points for the ropes that suspended the
funnels, the placement of the collection funnels was performed in a way to maximize coverage of the
canopy area, with these being placed from the trunk outwards (Schulz & Wagner 2002). For sample
standardization, a minimum of four funnels were set under each tree, to a maximum of 9, the
exception being two laurel trees, in which only three funnels were able to be set under the canopies.

Immediately prior to fogging the funnels would be once more inspected for debris or
wandering arthropods, and then the collection bottles were attached to the funnels and filled with
approximately 50 mL of 96% ethanol (Fig. 2-8). A label written in pencil on tracing paper, with the
tree code, sample number and date was inserted in the bottle (this was standard procedure in the 2014
season, but afterwards the label was inserted at the end of the fogging procedure, to facilitate the
identification of the stored samples).

Figure 2-8 Collection bottles being attached to the suspended funnels. On the background is possible to see an I. perado
subs. azorica tree marked with construction tape. (Photo: Gergely Erno).

Ideally fogging should be performed in periods of calm air, with little or no wind (Roberts
1973, Erwin 1983a, Adis et al.1998), In most regions this translates into the dawn and early morning
(Roberts 1973, Floren & Linsenmair 1998, Adis et al. 1998, Marske et al. 2007, but see Mody et al.

31
2003), but the prevailing night showers and morning mists of altitude forests in Terceira island
(Azevedo 1996) precluded this, since fogging should not be done in wet foliage (Adis et al.1998,
Horstmann et al. 1999, Grunner 2007). Therefore, in my fieldwork, fogging would start when the sun
dried the canopies enough to proceed, usually around 11:30-12:00 am and would last usually until
16:00 pm, when rising winds would prevent further fogging and branch beating (Adis et al.1998,
Horstmann et al. 1999).

After a final evaluation of the weather conditions the canopy fogging proper would begin.
Fogging of each individual tree was performed from at least two different directions for a total of
approximately 4 minutes or until the crown was saturated with insecticide fog. If that was the case,
two or three adjacent trees were fogged in succession (Figure 2-9).

Figure 2-9 Fogging of a L. azorica canopy, at the beginning of the 2014 season. (Photo: Gergely Erno).

A minimum drop time of at least 30 minutes was allowed for each fogged tree. During the
drop time all funnels were monitored and the arthropods present (knocked out or otherwise) were
aided to fall into the collection bottles either by tapping the sides of the funnels or with the use of a
soft brush or fallen leaves. After the drop off period was terminated and the fall of arthropods was
over or the drop rate conspicuously decreased, the branches were beaten with a wooden staff and,
when possible, the entire tree was shaken, to dislodge dead or knocked out arthropods from the

32
foliage (Southwood et al. 1982, Marques et al. 2001, Kuria et al. 2010). For the branch beating, the
area of canopy above each funnel was struck three or four times. This would be done from the
ground, or if necessary, by climbing to the first main branch of the tree in question, or to that from a
nearby tree. Similarly, when possible to shake the whole tree, this was performed from the trunk or
by climbing to the first bifurcation and then shaking the main branches.

All fallen arthropods, small leaves, mosses and other plant matter and debris were brushed
into the collection bottle of each funnel. Larger branches, leaves and clumps of moss were shaken
into the funnel, carefully inspected and then discarded. Despite the fact that many studies indicate
that most arthropods fall within the first 30 minutes after fogging, a drop time of two hours is usually
recommended (see Adis et al. 1998). Unfortunately, the time window for fogging presented by
standard field and weather conditions in Terceira precluded a longer allowance for the drop time.
Nevertheless, given all the procedures that took place from the end of the fogging until removing and
closing the collection bottle and that ideally two or three trees were being processed in tandem,
meant that the effective total drop time was of approximately 60 to 70 minutes for each sample.

The bottles were then decoupled from the funnels, topped up with 96% ethanol and taken to
the facilities of the University of the Azores, where they were stored while awaiting to be
processed/sorted. For logistical reasons, most samples from 2014 had to be transferred from the
polyethylene bottles into mason jars, for storage.

Fogging procedures were preformed usually with the help of one or two field assistants,
which in a day with exceptionally good weather conditions meant that it was possible to fog up to
four trees, before rising evening winds or logistic constraints precluded further sampling.
Occasionally this was also performed by me alone, which in that case translated into generally only
one tree being fogged in one day.

The sampling protocol for the J. brevifolia trees in semi-natural pasture was similar to the
protocol for the forest, with the exception of some small adaptations, that will be detailed in the
appropriate chapter.

2.8.1. Arthropod species identification

All the sorting and identification was performed in the facilities of the University of the
Azores, using a Leica MZ16 manual stereomicroscope. The processing of each individual sample
started with separating all arthropods (and specimens from other taxa like Annelida or Gastropoda,
despite not being considered in my study) from all plant matter and organic and inorganic debris

33
present in the bottle. This “clean” sample was then either put into a plastic tube with 96% ethanol
and stored in a refrigerator while awaiting to be sorted, or was immediately sorted to orders and then
to morphospecies. For most of this study, I followed a parataxonomy approach sensu Oliver &
Beattie (1993), in which all adult and juvenile specimens were identified to a given morphospecies,
while excluding all individuals that were not possible to identify or whose classification into
morphospecies was dubious. In a third stage a trained taxonomist (Paulo A. V. Borges) corrected all
the splitting and lumping errors and identified the species. Taxonomic nomenclature followed Borges
et al. (2010) checklist. Additionally, due to lack of expert knowledge about these groups, specimens
of Isopoda, Acari, Collembola, Diptera and Hymenoptera were not identified to morphospecies and
were also excluded from most of the analysis, the exception being some basic comparisons of
abundance at higher taxa level (in Chapters 3 and 4). I also performed a tentative characterization of
the Hymenoptera into Recognizable Taxonomic Units (RTU’s), but lack of specialist confirmation
precluded the use of these in further analysis and only some basic comparisons at order level were
performed. The specimens from these taxa were nevertheless counted and stored for future reference.

For most Azorean arthropod taxa, identification of juvenile/immature specimens was

possible due to the relatively low species richness of the archipelago and the long standing
experience of PAVB (see also Ribeiro et al. 2005; Gaspar et al. 2008). All the specimens are stored in
the University of Azores Insect Collection “Dalberto Teixeira Pombo” (Terceira, Azores).

2.8.2. Data analysis

The description of the specific statistical analyses for each research question is presented in
detail in each single chapter. In this section I will just give some general criteria employed
throughout the manuscript.

For several of the analyses the arthropods were grouped into three colonisation categories:
endemic (present only in the Azores), native non-endemic (henceforth “native” for simplification;
species that, although not endemic, arrived to the islands by natural means), and introduced species,
following the criteria of Borges et al. (2010). Native status was given to the taxa without a reliable
identification, except when the genus or family was known to be dominated by exotic species in the
Azores (based on Borges et al. 2010). Additionally, each species was assigned to a functional group
(predator, herbivore, saprophyte, fungivore). Data for this trophic classification was available in the
databases of the Azorean Biodiversity Group, having been previously collated from extensive
literature search of ecological information and from taxon experts.

34
 Regarding tourists (sensu Moran & Southwood 1982), one may identify three types of edge
effects leading to the presence of species that are not part of the sampled communities (Scharff et al.
2003; Cardoso et al. 2008):

1. phenological edge effects - individuals that are mature outside the normal breeding
season and show in the time-frame of the sampling;

2. methodological edge effects - individuals that inhabit microhabitats not adequately

accessed with the sampling methods used;

3. spatial edge effects - individuals that prefer habitats not present in the study area and that
are vagrants inside the plots.

A few species in the samples could be considered habitat tourists, as these species are mainly
soil dwellers or species that inhabit other habitats like pastures and grasslands. These were
nevertheless kept in the analyses, as I could not ascertain if these species would or would not interact
with the other species present in the canopies, and/or use the canopies as shelter.

35
Chapter 3
Revision of Azorean Canopy Arthropods in native tree species

3.1. Introduction

Azores are known by their low number of indigenous species (endemic and native non-
endemic) of most taxonomic groups, in comparison with the other Macaronesian archipelagos
(Borges et al. 2005b). Moreover, the Azores are probably the archipelago of Macaronesia where the
damages caused by historical anthropogenic ecosystem changes are the most apparent (Borges &
Hortal 2009; Cardoso et al. 2010; Triantis et al. 2010a, b; Connor et al. 2012, 2013). Such changes
are thought to have caused already the extinction of numerous endemic species, particularly in the
most disturbed islands, where few and minute native forest patches remain (Cardoso et al., 2010;
Terzopoulou et al. 2015). As a consequence, the knowledge of the current distribution and abundance
of terrestrial Azorean biotas is a critical step to set conservation programs on the native forest
ecosystem (see e.g. Gaspar et al. 2011). Due to the work of several research groups from the
University of the Azores in the last twenty years, many archipelagic studies on both indigenous and
exotic species have been carried out (see Chapter 1 and references therein).

However, there are very few studies so far dealing in detail with the biotic communities
associated with each of the indigenous host tree species that structure the extant Azorean forests, as
seen in the previous chapter.

I will do a brief revision of the existing knowledge on the biotic communities associated
with the three structurally important native trees of the Azores archipelago that I selected for my
study, namely Juniperus brevifolia (Seub.) Antoine, Ilex perado Aiton subsp. azorica (Loes.) Tutin;
Laurus azorica (Seub.) Franco.

The main objectives of this chapter are:

a) to describe in some detail the diversity, abundance and spatial patterns of canopy
arthropods associated with the canopies of three native Azorean trees, with a special focus on
Terceira island, taking advantage of the standardized data collected with the BALA project in 1992-
2002 and 2003-2004 (e.g. Ribeiro et al. 2005; Gaspar et al. 2008),

36
 b) to establish a baseline, in order to compare the island arthropod canopy pool data with the
data obtained in by work with canopy fogging in a forest fragment in Terceira island, a technique not
hitherto applied in the archipelago.

Also, given the current rates of biodiversity loss due to global changes (e.g. invasive species,
habitat erosion and fragmentation, climatic changes), with all their impacts on the ecosystems and
associated communities (Butchart et al. 2010, Hooper et al. 2012). I feel that additionally, this will
be an useful asset for future researchers and conservation practitioners, offering a set of data that may
be used to compare and evaluate future changes in the native Azorean ecosystems and associated
species composition.

3.2. Methods

3.2.1. Location
The Azores archipelago. Sampling for the BALA project took place in seven islands of
Azores (excluding Graciosa and Corvo) (see more details is Gaspar et al. 2008).

For this chapter, I will use data pertaining to the islands were there were standing
populations of one or more of the native tree species of interest, namely:

Juniperus brevifolia - São Miguel, Terceira, São Jorge, Pico, Faial and Flores;

Ilex perado Aiton subsp. azorica - São Miguel, Terceira, São Jorge, Pico, Faial and Flores;

Laurus azorica - Santa Maria, São Miguel, Terceira, Pico, Faial and Flores.

3.2.2. Data sets and sampling

The arthropod data set consists of the results from the BALA project (Biodiversity of
Arthropods of Laurisilva of the Azores), an extensive and standardized sampling protocol applied to
native vegetation areas in the years of 1992-2002 and 2003-2004 (Borges et al. 2005a; Ribeiro et al.
2005; Gaspar et al. 2008; with more details at http://islandlab.uac.pt/projectos/ver.php?id=65). Each
forest fragment included a minimum of four 150 m long transects (the number of transects being
dependent on the forest fragment area); in each transect the two or three most common trees and
shrubs were sampled every 15 metres (for a total of 10 replicates per transect), using canopy beating
(pitfall traps were part of the BALA protocol but were not analysed in the present study, but see

37
Borges et al. 2005a; Gaspar et al. 2008). For that purpose, a stick and a cloth collector tray, in the
shape of an inverted pyramid with a bag at the end, was used. As is to be expected, the three tree
species were not present on all of the transects, nor in all islands. As such, for this particular subset of
data, each forest fragment included between one and sixteen transects. For a more detailed
description of the sampling protocol see Ribeiro et al. (2005) and Gaspar et al. (2008). For J.
brevifolia 16 forest fragments were sampled, for a total of 74 transects and 740 samples, for I.
perado subs. azorica 14 forest fragments totaling 45 transects and 449 samples, and for L. azorica,
13 fragments, with also 45 transects and 450 samples.

All samples and identified species are deposited in the EDTP – Entomoteca Dalberto
Teixeira Pombo, University of Azores, Angra do Heroísmo, Portugal. Occurrence data was digitized
in the ATLANTIS database (http://www.atlantis.angra.uac.pt/) and available also in the Azores
Bioportal (http://azoresbioportal.uac.pt/).

Focus will fall on the data sets from Terceira island, with a brief overview of the general data
for the Azorean archipelago.

3.2.3. Data analyses

For this study, all adult and juvenile specimens identified to a given morphospecies were
considered, while excluding all individuals that were not possible to identify or whose classification
into morphospecies was dubious. The identification of juvenile/immature specimens was possible for
the Azorean fauna due to the relatively low species richness of the archipelago and the long standing
experience present in the Azorean Biodiversity Group. For some of the analysis the arthropods were
grouped into three colonisation categories: endemic (present only in the Azores), native non-endemic
(“native” for simplification from now on; including species that, although not endemic, arrived to the
islands by natural means), and introduced species, after the criteria of Borges et al. (2010). Each
species was also assigned to a functional group (predator, herbivore, saprophyte, fungivore). Data for
trophic guild and feeding mode were collated from an extensive literature search of ecological
information, including manuscripts with the first descriptions of the species, first species records for
the Azores, brief notes, and ecological studies among others. Information was also obtained from
experts who have identified the specimens or from experts of a given taxonomic group when
information for a particular species was not available. For the few taxa identified to morphospecies,
information of the nearest taxonomic resolution was considered.

38
 In the case of Terceira island, to avoid pseudo-replication, when transects were sampled in
more than one year, replicates were excluded, in a way as to balance the data chronologically.
Additionally, Terceira was the only island in which some transects had more than 10 samples due to
some additional experiments (see Gaspar et al. 2014). As such, and to normalize with the other
islands, when transects had more than 10 samples, all samples past the first ten were excluded from
the analysis.

All statistical analyses were implemented in R version 3.3.3 (R Core Team, 2017), with the
exception of some basic calculations and graphics that were performed in LibreOffice spreadsheet
(The Document Foundation). The data from the entire archipelago was only analyzed at a cursory
level, as the differences in habitat and species assemblages that exist between the islands make it less
relevant for the present study.

Datasets were analyzed for the entire community and for the individual tree species.

Species accumulation curves were calculated for the datasets using the BAT package
(Cardoso et al. 2016). As an indication of the completeness of the inventory, the final slope of the
accumulation curve (the first derivative of the curve at the end point) (Cardoso et al. 2011b) was also
calculated with the BAT package. The Jackknife1 estimator was used for evaluating the inventory
completion, as this estimator was proven to be the most suitable for several datasets, including for
Azorean arthropod data (Hortal et al. 2006).

To assess if any of the arthropod species collected could be considered as indicator of a

given tree species, the Dufrêne-Legendre indicator value (Dufrêne & Legendre 1997) was calculated
for each species, using the labdsv package (Roberts 2016).

To assess the distribution of species abundances for the arthropod community as a whole as
well as for the different colonisation status, and for the distinct tree species, binning of the arthropods
species into modified Preston's octaves was performed using the third method described in Gray et
al. (2006), using the R package gambin (Matthews et al. 2014).

Beta diversity calculations were performed using the R package BAT (Cardoso et al. 2015).
Total differentiation between each tree species (βtotal, the inverse of the Jaccard similarity index)
was divided into its species replacement (βrepl) and species richness differences (βrich) components
(Carvalho et al. 2012) using the same R package, randomized at the minimum common denominator
and with 1000 iterations. This was done for the community as a whole and for each colonisation
class.

39
 3.3. Results

For the entire Archipelago 58152 specimens were collected in the tree canopies,
corresponding to 232 species (Table 3-2), representing four Classes, 18 Orders and 80 Families. Of
all the collected species, 64 were considered endemic, 81 native and 87 were introduced in the
archipelago. Hemiptera was the overall most species rich order, followed by Araneae, while in terms
of abundance the situation was inversed.

Most of the species were rare in the samples, with 146 (63%) having 10 or less individuals.
Noticeable was also the relatively high proportion of singletons and doubletons, accounting for
approximately 42% of the species present (Table 3-2). On the other hand, the ten most abundant
species accounted for 65% of all collected specimens. The endemic moth Argyresthia atlanticella
Rebel (Lepidoptera: Yponomeutidae) was the single most abundant species, with 9798 specimens,
followed by the endemic canopy sheet weaver Savigniorrhipis acoreensis Wunderlich (Araneae,
Lyniphiidae) and the native mesh web weaver Lathys dentichelis (Simon) (Araneae, Dyctinidae),
with 7137 and 5286 specimens collected, respectively.

For the entire Terceira island, 22273 specimens were collected in the tree canopies,
corresponding to 135 species (Table 3-1). These belonged to three Classes, 15 Orders and 62
Families. Of all the collected species, 39 were considered endemic, 47 native and 49 were
introduced. Overall, Araneae was the most species rich and abundant order, followed by Hemiptera
and Lepidoptera (Table 3-1).

40
Table 3-1 Summary table of the collected arthropod taxa from BALA, listing all classes and orders found in the three tree
species for Terceira island, with indication of the number of families, species and specimens in each order.
Class/Order Families Species Specimens

Arachnida

Pseudoscorpiones 1 1 1

Opiliones 1 1 9

Araneae 12 34 9811

Diplopoda

Julida 1 1 38

Insecta

Microcoryphia 1 2 120

Ephemeroptera 1 1 1

Blattodea 1 1 1276

Psocoptera 7 12 635

Hemiptera 15 28 6823

Thysanoptera 2 6 15

Neuroptera 1 1 185

Coleoptera 9 20 212

Trichoptera 1 1 2

Lepidoptera 8 25 3076

Hymenoptera 1 1 69
(Formicidae)

Totals 62 135 22273

In Terceira, following the trend for the Azorean archipelago, most species were rare in the
samples, with 83 (61%) having 10 or less individuals. Once more, there was also a relatively high
proportion of singletons and doubletons in the samples, accounting for approximately 43% of the
species present (Table 3-2). The ten most abundant species accounted for 68% of all collected
specimens. With 3204 specimens, the endemic canopy sheet weaver Savigniorrhipis acoreensis
(Araneae, Lyniphiidae) was the most abundant species, followed by the native mesh web weaver
Lathys dentichelis (Araneae, Dyctinidae) with 7137 specimens and by the conifer aphid Cinara
juniperi (De Geer) (Hemiptera, Lachnidae), with 1910 specimens collected.

41
 In Terceira there was a profound imbalance in the sampling effort between the distinct tree
species, with J. brevifolia having the highest number of individuals (13657) and comparatively high
species richness, but at the same time it had more than double the number of samples than I. perado
subs. azorica.

When standardizing the number of samples, a more homogeneous set of richness and
abundance values was obtained (Table 3-2).

Table 3-2 Summary table with the BALA dataset arthropod species richness (S), abundance (N), number of singletons
and doubletons, uniques and duplicates, number of transects, number of samples and diversity for the total number of
specimens and for each individual tree species in the entire archipelago and for Terceira island. Values in parenthesis
indicate the corresponding standardized value, obtained from sample based accumulation, at the minimum common
number of 169 samples in Terceira. Ilex - I. perado subsp. azorica; Jun - J. brevifolia; Lau - L. azorica.
Azores Terceira

Ilex Jun Lau Total Ilex Jun Lau Total

Transects 45 74 45 17 34 (17) 27 (17) 78

Samples 449 740 450 169 340 (169) 270 (169) 780

S 141 162 139 232 76 107 (83) 84 (73) 135

N 12102 36731 9319 58152 3338 13659 5276 22273

(6786) (3310)

Singletons 43 44 42 63 26 39 (25) 23 (18) 44

Doubletons 13 20 13 35 6 5 (7) 7 (8) 14

Uniques 27 42 26

Duplicates 8 7 5

Regarding the three distinct tree species in Terceira, even after standardization J. brevifolia
was the tree species that accumulated the highest abundance and number of species. As with the
general trend, proportion of singletons and doubletons was high in all tree species, but being lower in
L. azorica (35.7%), even after standardization (35.6%) (Table 3-2). I. perado was the tree species
with a higher proportion of species with 10 or less specimens present (67%), contrary to L. azorica
(60%), while the weight of the dominant species was higher in J. brevifolia, where the ten most
abundant species accounted for 85% of the specimens, and was lower in L. azorica, were the ten
most abundant species accounted for 71% of the collected specimens.

42
 The alpha accumulation curve for each tree species (Fig. 3-1) showed that the sampling
effort was adequate to collect a sizable portion of the arthropod communities present in the canopies,
each accumulating species at a fairly similar rates. Low values of the final slopes (the first derivative
of the curves on their final point) for each accumulation curve indicated that inventory completeness
was adequate (Table 3-3).

Figure 3-1. BALA dataset alpha accumulation curves for each tree species. Red - I. perado subsp. azorica; Green - J.
brevifolia; Blue – L. azorica.

Calculating the inventory completeness using the Jackknife 1 estimator confirmed that
inventory completeness was in general adequate, with J. brevifolia having the lowest inventory
completeness (73.3%) and L. azorica the highest (78.5%%) (Table 3-3).

Table 3-3 Values of Jackknife 1 estimated richness, with corresponding inventory completeness, and value of slope at the
final point of each accumulation curve, for each individual tree species, using the BALA dataset.
I. perado J. brevifolia L. azorica

Jackknife 1 102 146 107

Completeness 74.5% 73.3% 78.5%

Slope 0.008 0.003 0.005

43
 Analyzing the proportion of endemic, native and introduced species present in each tree
species, both in the entire archipelago and in Terceira island, it was possible to observe that species
richness was more or less evenly distributed amongst the three colonisation categories, with each
accounting for roughly one third of the species present (Fig. 3-2). Nevertheless, some variation was
observed. At the Azores level, the proportion of introduced species was higher in both I. perado and
L. azorica, while J. brevifolia trees in general had a higher proportion of native species, with a
decrease in the relative number of introduced ones. In Terceira, introduced species accounted for
roughly 30% of the species present in I. perado and J. brevifolia, while I. perado canopies also had
the highest proportion of endemic species. L. azorica was the tree whose canopies, in general,
accumulated a higher proportion of introduced species.

Figure 3-2 Proportion of endemic (E), native (N) and introduced (I) arthropods for each tree species, as taken from the
BALA dataset, in terms of relative species richness (a) and relative abundance (c) for the entire archipelago, and of
relative species richness (b) and relative abundance (d) for Terceira.

Regarding abundances, it was quite conspicuous the very low proportion of specimens from
introduced species present in the canopies of J. brevifolia, either in the whole archipelago or in
Terceira island, as these accounted for 4% of the collected specimens. On the other hand, I. perado
was the tree species with the highest proportion of specimens from introduced species in its canopies,
both in Terceira and in the Azores in general. Also at both scales, L. azorica was the tree species with

44
a lower proportion of endemic specimens. Nevertheless, a Kruskal-Wallis test indicated that none of
the above differences were statistically significant (p-value > 0.05).

Regarding the trophic classes, there was a remarkable constancy in the proportion of each
group in terms of species richness and in terms of abundance, both for the entire archipelago and for
Terceira alone (Fig. 3-3). However, there were nevertheless some slight variations regarding
abundances. At the archipelago level, the crowns of I. perado had a slightly higher proportion of
saprophyte specimens present, while on L. azorica 60% of the specimens collected were herbivores,
something also observed in Terceira island. For Terceira, it was also conspicuous the higher
proportion of predators in J. brevifolia, accounting for 60% of the collected specimens. As above,
none of these differences were statistically significant (p-value > 0.05).

Figure 3-3 Proportion of fungivore (F), herbivore (H), predator (P), ants (P/H) and saprophyte (S) arthropods for each
tree species, as taken from the BALA dataset, in terms of relative species richness (a) and relative abundance (c) for the
entire archipelago, and of relative species richness (b) and relative abundance (d) for Terceira.

Binning the species present in in the island and in each tree species, it was possible to
observe that the canopy community as a whole was composed by many rare species and few
intermediately and truly abundant ones (Fig. 3-4). This general pattern was replicated in each
individual tree species, although in L. azorica there seemed to be a slightly higher proportion in

45
intermediately abundant species. The low number of truly abundant species in I. perado was most
likely derived from the unequal sampling effort.

Figure 3-4 Modified Preston's octaves histograms for the entire dataset of Terceira (a) and for each tree species - I.
perado subsp. azorica (b), J. brevifolia (c) and L. azorica (d), discerning between the endemic (green), native (blue) and
introduced (red) species components.

Considering the colonisation status, the high proportion of locally rare introduced species
was conspicuous, particularly in L. azorica, which in general also had a constant presence of
introduced species in all abundance classes. On the contrary, in the case of J. brevifolia all the
abundant species were either endemic or native (Fig. 3-4). Considering the species in the first quarter
of the octaves as locally rare, 62% of the species present in I. perado could be considered rare. This
proportion was lowest in L. azorica, with 58% of the species being locally rare.

Taking the Indicator value as an indication of specialization, J. brevifolia was the tree
species that had the highest number of associated arthropod species (Table 3-4). Considering the
colonisation status, for both J. brevifolia and I. perado, roughly half of the associated specialist
species were endemic, with natives accounting for a quarter and introduced species for the other
quarter. Two of the species specialized in J. brevifolia were of uncertain status regarding
colonisation.

46
Table 3-4 Summary table of IndVal results from the BALA dataset for each host-tree, with total number of Indicator
species, and the number of indicator species belonging to each colonisation class. An expanded version of this table is
presented in Appendix II.
Host tree Species Endemic Native Introduced

I. perado 8 4 2 2

J. brevifolia 21 9 5 5

L. azorica 10 2 8 0

Interestingly, all but two of the species that could be considered L. azorica specialists were
natives.

As a whole, dissimilarities between the communities present in the three distinct tree species
were intermediate, with no particular distinction between tree species (Table 3-5). These differences
were mainly explained by species turnover.

Table 3-5 Rarefied values of Total β diversity, β Replacement and β Richness between the different tree species in
Terceira island, using the BALA dataset - for the entire community, for endemic, for native and for introduced species, .
Ilex - I. perado subsp. azorica; Jun - J. brevifolia; Lau - L. azorica.
All Endemic Native Introduced

β-total Ilex Jun β-total Ilex Jun β-total Ilex Jun β-total Ilex Jun

Jun 0.44 - Jun 0.31 - Jun 0.50 - Jun 0.64 -

Lau 0.42 0.46 Lau 0.26 0.27 Lau 0.33 0.48 Lau 0.64 0.63

β-Repl Ilex Jun β-Repl Ilex Jun β-Repl Ilex Jun β-Repl Ilex Jun

Jun 0.37 - Jun 0.12 - Jun 0.41 - Jun 0.27 -

Lau 0.40 0.40 Lau 0.12 0.21 Lau 0.30 0.41 Lau 0.24 0.60

β-Rich Ilex Jun β-Rich Ilex Jun β-Rich Ilex Jun β-Rich Ilex Jun

Jun 0.08 - Jun 0.18 - Jun 0.07 - Jun 0.38 -

Lau 0.02 0.06 Lau 0.18 0.03 Lau 0.04 0.07 Lau 0.40 0.02

47
 Considering the different colonization classes, for endemic species, dissimilarities in the
communities of the different trees were lower and explained equally by species turnover and in
differences in terms of the number of species present, except in the case of J. brevifolia and L.
azorica, where species turnover was the main cause of the observed dissimilarities. For native
species, dissimilarities between the communities of the tree species were higher that when
considering only the endemic species, particularly J. brevifolia and the other two tree species. These
differences seemed to be mainly caused by species turnover. For introduced species, dissimilarities
between the communities were higher, but with no particular distinction between tree species. These
dissimilarities were explained by both differences in the number of species present and by species
turnover, except for L. azorica and J. brevifolia, where species turnover was the main explaining
factor.

3.4. Discussion

There is a large body of studies regarding arthropod canopy communities, encompassing a

wide range of habitats and spectrum of host plants (Stork 1991; Winchester 1997; Kuria et al. 2010).
In many of these studies there is a remarkable constancy in the proportions of certain functional
groups and orders (Moran & Southwood 1982; Krüger & McGavin 2001) and the most abundant and
diverse orders in this study (Araneae, Hemiptera, Lepidoptera) also tend to be amongst the most
abundant and diverse in other parts of the world (Stork 1991; Floren & Linsenmair 1997).
Nevertheless, the fact that hyperdiverse and biologically important groups like Hymenoptera and
Diptera, that can be extremely abundant and diverse on tree canopies (Guilbert 1997; Kitching et al.
1997, Horstmann et al. 1999, 2005, Veijalainen et al. 2012) were not considered in the BALA
protocol (except for ants), can somewhat hamper direct comparisons.

General patterns regarding species richness and abundance in the present study agree with
general patterns observed in previous studies for the communities of arthropods in Azorean native
forests (see Ribeiro et al. 2005; Gaspar et al. 2008). In all instances Araneae, Hemiptera, Lepidoptera
and Coleoptera account for more than 75% of the species recorded.

Spiders were previously reported as the most abundant order overall (Gaspar et al. 2008) and
also the one with the highest ratio of juveniles to adults (Gaspar et al. 2008). This is also true in the
case of the present study, given the preponderance of J. brevifolia in the samples, an architecturally
complex tree that has been shown to have a propensity to accumulate species in general and spiders
in particular (Ribeiro et al. 2005; Ribeiro & Borges 2010). This high number of juvenile spiders,

48
most of them of indigenous species, shows that source populations are building up and completing
their life cycle on the Azorean cedar, taking advantage of the structural complexity of the host tree to
protect their postures and juveniles (see e.g. Borges et al. 2008).

The relatively high proportion of singletons found in the present study is also in accordance
with previous findings (Gaspar et al. 2008). The amount of singletons for Terceira is considerably
higher than in the aforementioned study, but it is still lower than the values reported for herbivore
singletons in canopies given in Ribeiro et al. (2005). Additionally, the overall percentage of rare
species as given by binning the species into octaves (60%) was similar to the results obtained by
Ribeiro & Borges (2010) for J. brevifolia trees (60% of rare species). As with Ribeiro & Borges
(2010), many rare species accumulate in the canopies of J. brevifolia, but also in those of the other
two tree species. For native and introduced arthropod species, it may be the case that these have
greater dispersal capabilities than the endemic ones and thus, could more easily end up as habitat-
tourists (Borges et al. 2008). Most introduced species are certainly habitat-tourists, the majority
being present in low abundances, indicating that the core populations are outside the natural forests.
It is also possible that this high number of (most likely) locally rare species could be a result of
undersampling and/or a combination of phenological, methodological and spatial edge effects
(Scharff et al. 2003; Cardoso et al. 2008).

Concerning the functional groups of the collected specimens, both the present study and
Gaspar et al. (2008) agree on the dominance of predators and herbivores, in terms of abundance and
species richness, with these accounting, on all instances, for more than 80% of the individuals or
species (respectively) and, mainly in terms of species richness being the proportions of the different
functional groups quite constant through the archipelago. This is not dissimilar from the figures
given by Winchester (1997) for temperate coniferous forests or by Krüger & McGavin (2001) for
tropical savanna's, and agrees with patterns of functional group proportion constancy in other parts of
the world (Moran & Southwood 1982; Stork 1987, 1991). At archipelago level, herbivorous
arthropods were slightly more diverse and abundant than predators, but J. brevifolia trees in Terceira
(for abundance) deviate from this pattern. Borges et al. (2008) also found more predator than
herbivore species on their samples from Terceira. One of the possible reasons might be the
propensity of the azorean cedar to accumulate spiders (Ribeiro & Borges 2010). For herbivores,
especially chewers, lower diversity might also be related with the reduced number of food choices
available on J. brevifolia (see Winchester 1997).

Looking at the colonisation status of the collected specimens, the present results are
substantially different from those of previous studies that take into account both, ground and canopy

49
arthropods. Borges et al. (2010, with additional updated data) gives 269 endemic arthropods for the
Azores, out of a total of 2070 species and subspecies with a well defined colonisation status,
amounting to approximately 13% of endemics, reporting also 47% of introduced arthropod species,
while Florencio et al. (2013) reports 13.5% of endemics and 55% of introduced species. Other
studies give figures of approximately 25% of endemic species and 33% of introduced species
(Borges et al. 2006, Gaspar et al. 2008). Most of these results contrast with those of the present
study, as the percentage of endemic species on the canopies was never below 30% at both scales,
whereas the percentage of introduced species had variation, but in Terceira, except for L. azorica,
was also below 30%.

Figures for abundance of endemic and introduced species agree in general with Gaspar et al.
(2008), where almost 50% of endemics and 11% of introduced species were reported. The Azorean
cedar is the exception to this, as in the present study the percentage of introduced species on J.
brevifolia canopies was extremely low, with less than 4% of specimens being of introduced species.

In previous studies investigating different habitats in the Azores, some of them with a higher
degree of anthropic disturbance, or even on the epigean soil arthropod communities of the extant
native forests (Borges et al. 2006, Gaspar et al. 2008; Cardoso et al. 2009; Meijer et al. 2011;
Florencio et al. 2013), there is usually a high abundance and richness of introduced species. Only the
canopies of the native tree species, particularly those of J. brevifolia, seem to remain resistant to the
establishment and dominance by introduced species. The data seems to indicate that introduced
species are able to disperse to the forest canopies either from the ground strata or from nearby
disturbed habitats (Borges et al. 2008), but that, for now, are unable to gain a foothold and colonise
this habitat.

This pattern has been observed for the canopies of several native host tree species (Ribeiro &
Borges 2010), and can be due to the fact that the canopies in the native forest, with their higher
diversity and abundance of native and endemic species, could represent a habitat with less empty
ecological niches, or that introduced generalist species are unable to properly access the nutritional
resources present, to find shelter or the appropriate reproductive conditions. It can also be that this
pattern is caused by the climatic harshness of the constant conditions of high humidity in the
canopies of the Azorean high altitude forests remnants (cf. Grimbacher & Stork 2007) or by the
intrinsic and structural characteristics of the trees (cf. Mody et al. 2003).

Concerning the particularly low abundance of introduced species present in the canopies of
J. brevifolia trees, this pattern might be a consequence of the high structural complexity of its

50
canopies and its high predator (spider) load (Ribeiro & Borges 2010), or even due to some sort of
hitherto unknown chemical deterrent, since trees of the genus Juniperus, as well as many other
Cupressaceae, are known to produce several essential oils and other substances that are toxic or
repellent to arthropods (Carroll et al. 2011; Abad et al. 2013; Athanassiou et al. 2013), therefore
favoring the presence of indigenous (particularly specialists like Cinara juniperi) and inhibiting the
colonisation by introduced species.

Moderately high values of species turnover and of imbalances regarding the number of
species present in the distinct tree species are to be expected, given the different nature of the trees,
but also due to the fact that the data used in the present study was collected across the extant patches
of native forests, with varying degrees of isolation from each other. Even so, it must be pointed out
that the endemic species component was more homogeneous across the three tree species.

51
Chapter 4
Characterization of the canopy arthropod fauna of a native Azorean
forest by canopy fogging

4.1. Introduction

Canopy communities are usually species rich and complex, with most species being more or
less interlinked in complex food webs (Moran & Southwood 1982). Trees provide food and shelter,
and are architecturally complex, creating opportunities for niche diversification (Moran &
Southwood 1982). In addition, trees and their canopies are easily defined and delimited (Southwood
& Kennedy 1983, Kruger & McGavin 1997), acting as discrete ecological units that can are easier to
sample more completely and accurately and with greater replication than other complex habitats
(Moran & Southwood 1982).

As seen in Chapter 3, the Azorean arthropod fauna is relatively well studied, being the focus
of exhaustive species inventories (Borges et al. 2005; Borges et al. 2010), as well as the basis for a
high number of works in the last couple of decades, particularly in native forests (reviewed in Borges
et al. 2011), but also other land-use types (see Cardoso et al. 2009; Florencio et al. 2016). Despite
these studies, there are still several gaps regarding the knowledge of the diversity and structure of the
arthropod communities associated with the canopies of Azorean trees, which hinders the
conservation of biodiversity and sustainable resource management (Summerville et al. 2003;
Cardoso et al. 2011a). Canopy fogging can help closing some of these knowledge gaps, since as
already discussed in Chapter 2, this technique is fairly indiscriminate and good at capturing most of
the community present in the canopies, being quite adequate for quantitative (Kehlmaier & Floren
2010) and comparative studies (Gruner 2007), having thus the potential to increase the current
knowledge about the Azorean arthropod communities.

There are several wide scoped canopy fogging studies (e.g. Moran & Southwood 1982,
Stork 1991, Floren et al. 2014) but most focus on a certain arthropod taxon (e.g. Wagner 1997,
Schulz & Wagner 2002, Veijalainen et al. 2012), or a given host tree species (Basset 1991, Krüger &
McGavin 1997, Marques et al. 2001). Most of these relate to tropical areas (e.g. Erwin 1983a, Adis
et al. 1984, Stork 1991, Allison et al. 1993), with some taking place in temperate climates (e.g.
Winchester 1997, Otto & Floren 2007, Hsieh & Linsenmair 2012) or other biomes (Krüger &
McGavin 1997, Kuria et al. 2010). Few have taken place in island habitats (e.g. Gagné 1979, Gruner

52
2007, Marske et al. 2007) and even fewer have taken place in the Macaronesia (Stüben et al. 2010),
with none, until now, being performed in the Azores.

In this work, I applied for the first time in the Azores a canopy fogging protocol with the aim
of performing a characterization of the canopy arthropod communities associated with the three
structurally important native Azorean trees described in Chapter 2, namely Juniperus brevifolia
(Seub.) Antoine, Ilex perado Aiton subsp. azorica (Loes.) Tutin and Laurus azorica (Seub.) Franco.

Being the first fogging study done in the Azores, besides the direct results of the present
study, I also aim to create a baseline for future canopy fogging studies in the archipelago and a
database that would allow easier comparisons with other oceanic islands and regions where similar
studies have already been implemented. Additionally, this study could act as a stimulus to begin
similar studies in the other Macaronesian archipelagos.

The main objectives of this chapter are: i) to describe in detail the diversity, abundance and
spatial patterns of canopy arthropods in one of the best preserved extant forest patches in Terceira
island, including previously less well studied groups such as Hymenoptera, Diptera, Collembola and
Acari; ii) To compare the communities sampled by canopy fogging in a well preserved forest patch
with previous canopy data for Terceira island, with a slight focus on the colonisation status of the
species present; and iii) to ascertain if these tree species host distinct arthropod communities or if the
previously reported high levels of generalists among the endemic and native arthropod species
(Ribeiro et al. 2005) account for a somewhat homogeneous community through the different host-
tree species.

4.2. Methods

4.2.1. Study site

Terceira Island, in the Azores Archipelago. The sampling took place in the Terra Brava
Nature Reserve, on the study plot described in Chapter 2.

4.2.2. Arthropod dataset

All the arthropods collected by pyrethrum knockdown in conjunction with branch beating
(as described in Chapter 2) in fifteen trees (six Ilex perado subsp. azorica, seven Juniperus brevifolia
and three Laurus azorica) fogged for the first time in 2014 and in the eight trees (three specimens of

53
each of I. perado subsp. azorica and J. brevifolia and two of L. azorica) fogged for the first time in
2015.

4.2.3. Data analysis

Unless stated otherwise all statistical analyses were implemented in R version 3.3.3 (R Core
Team, 2017). Some basic calculations and graphics were also performed in LibreOffice spreadsheet
(The Document Foundation). Datasets were analyzed for: a) the entire community and b) for the
individual tree species.

Since abundance and richness data did not have a normal distribution even after logarithmic
transformation, non-parametric Analysis of variance (Kruskal–Wallis rank sum test) was performed
to identify potential differences between the three tree species regarding the aforementioned species
richness and abundance, and also the colonisation status of the specimens and the trophic guild
composition.

Common indices of diversity were calculated for the three trees following partially the Hill
series: species richness (S) (q=0 Hill number); Shannon-Wiener (H´); Fisher alpha and Pielou
evenness (Magurran 2004) as well as the second and third Hill numbers (q=1, exponential of
Shannon's entropy and q=2, inverse Simpson) (Hill 1973, Chao et al. 2014). Hill numbers were
calculated using the package SpadeR (Chao et al. 2015).

Being a relatively easy metric to assess and compare among communities, species density
(the number of species per sampling unit) (Gotelli & Colwell 2001, Schonberg et al. 2004), was also
calculated for my samples, along with specimen density, a fairly universal metric in canopy fogging
studies (e.g. Stork 1991, Floren & Linsenmair 1997, Watanabe 1997)

To assess if any of the arthropod species collected could be considered as indicator of a

given tree species, the Dufrêne-Legendre indicator value (Dufrêne & Legendre 1997) was calculated
for each species, using the labdsv package (Roberts 2016).

Species accumulation curves were calculated for the datasets using the BAT package
(Cardoso et al. 2016). As an indication of the completeness of the inventory, the final slope of the
accumulation curve (the first derivative of the curve at the end point) (Cardoso et al. 2011b) was also
calculated with the BAT package. The Jackknife1 estimator was used for evaluating the inventory
completion, as this estimator was proven to be the most suitable for several datasets, including
Azorean arthropod data (Hortal et al. 2006).

54
 To assess the distribution of species abundances for the arthropod community as a whole as
well as for the different colonisation status, and for the distinct tree species, binning of the arthropods
species into modified Preston's octaves was performed using the third method described in Gray et
al. (2006), using the R package gambin (Matthews et al. 2014). This package was also used to
calculate the corresponding α gambin values. To compensate for the imbalance in the sampling effort
regarding the different tree species, α gambin values were also calculated standardized at a value
slightly inferior to the minimum common number of specimens in the set and rerun 100 times. For
the tree species, calculations were standardized at 1000 specimens (3000 for the total) and, at 300
specimens for the colonisation status.

Nonmetric Multidimensional Scaling (Kruskal 1964) was applied to the data at a sample
scale (with Bray-Curtis coefficient), through R software and packages vegan (Oksanen et al. 2015)
and ade4 (Dray & Dufour 2007). Statistical significance in the dissimilarity between trees was
assessed through an analysis of similarities (ANOSIM) (Clarke 1993).

Beta diversity calculations were performed using the R package BAT (Cardoso et al. 2015).
Total differentiation between each tree species (βtotal, the inverse of the Jaccard similarity index)
was divided into its species replacement (βrepl) and species richness differences (βrich) components
(Carvalho et al. 2012) using the same R package.

4.3. Results

4.3.1. Abundance patterns

In total, 27,684 arthropod specimens were collected in the 23 trees. Acari, Araneae and
Collembola were the most abundant orders, with Acari alone accounting for roughly 40% of all
collected specimens. When considering only the Insecta, the orders Diptera and Hymenoptera were
the most abundant, followed by Coleoptera, Hemiptera and Microcoryphia (with this last one being
represented by a single endemic species) (Table 4–1).

The general patterns of abundance at order level were common to the three host-tree species,
even if L. azorica accumulated relatively more Diptera and less Hymenoptera specimens than the
other two tree species. Isopoda (Crustacea) was another taxon that appeared in relative higher
abundance in this tree species (Fig. 4–1). Nevertheless, differences between the tree species were
never significant (Kruskal-Wallis chi-squared = 1.59, df = 2, p = 0.45).

55
Figure 4-1 Relative abundance of the several arthropod orders, sorted by total abundance, in each tree species and in the
combination of all trees (All). Ilex - I. perado subsp. azorica; Jun - J. brevifolia; Lau - L. azorica

In the case of the Hymenoptera, some of 50 RTU’s were identified in the samples, making
them the most speciose order, with more morphospecies than all other identified Insecta taxa
combined. All collected Hymenoptera belonged to Parasitica, with Braconidae, Ichneumonidae,
Pteromalidae, Eulophidae and Encyrtidae being the most abundant and species rich families.

56
Table 4-1 Summary table of the collected arthropod taxa, listing all classes and orders found, with indication of the
number of families, species and specimens in each order. Subclasses or orders with an asterisk were not used for further
analyses. Also, 379 specimens belonging to the remaining orders, that were not possible to identify to a given
morphospecies and were therefore excluded from further analyses, are included in the table.
Class/(Subclass)/Order Families Species Specimens
Malacostraca
Isopoda * 1 1 146
Arachnida
(Acari) * - - 11855
Pseudoscorpiones 2 2 10
Opiliones 1 1 46
Araneae 11 23 7415
Diplopoda
Chordeumatida 1 1 27
Julida 1 1 1
Chilopoda
Lithobiomorpha 1 1 8
Entognatha
(Collembola) * - - 2637
Insecta
Microcoryphia 1 1 682
Blattodea 1 1 240
Psocoptera 5 6 562
Hemiptera 9 11 706
Thysanoptera 1 1 182
Neuroptera 1 1 14
Coleoptera 5 12 737
Lepidoptera 4 7 364
Diptera * - - 1097
Hymenoptera * ≈ 10 ≈ 50 955
Total - - 27684
Total (minus taxa 44 69 10994
marked with *)

Excluding Diptera, Hymenoptera, Collembola, Acari and Isopoda, a total of 10,617

arthropod specimens were collected and identified to species level, belonging to 69 species, 44
families and 14 orders (Table 4–1). The numbers of specimens showed a 15-fold variation between
trees and the number of species a threefold variation. These numbers were lower when considering
same species trees, but even so, there was a sevenfold variation in the number of specimens between

57
specimens of I. perado subsp. azorica. The average arthropod density was of 96 specimens per
square meter and the mean number of species per tree was of 25 ± 6.0. This density increased to
118.8 specimens/m2 when adding Diptera and Hymenoptera, and to 249.4 specimens/m2 if Acari and
Collembola were also considered. In all situations, arthropod densities were always slightly higher in
I. perado subsp. azorica and lower in L. azorica, but not statistically different (Kruskal-Wallis chi2 =
2.46, df = 2, p = 0.29).

4.3.2. Diversity patterns

Among the fully-analyzed dataset, Araneae was the most diverse and abundant order, with
23 species and 7,370 identified specimens. The most species rich family among all arthropods was
Linyphidae (Araneae), followed by Staphylinidae and Curculionidae (Coleoptera), Lygaeidae
(Hemiptera) and Geometridae (Lepidoptera). An endemic linyphid spider, Savigniorrhipis
acoreensis, was also the single most abundant species, with 3,113 specimens. Regarding the relative
species richness per order, there were no significant differences between tree species (Kruskal-Wallis
chi2 = 0.27, df = 2, p = 0.87), the same being true for relative abundances (Kruskal-Wallis chi2 =
1.42, df = 2, p = 0.49)

The proportions of singletons and doubletons were high in the samples, particularly for J.
brevifolia and I. perado subsp. azorica. The average number of species per tree was higher in I.
perado subsp. azorica and lower in L. azorica. but these differences were not statistically significant
(Kruskal-Wallis chi2 = 1.76, df = 2, p = 0.41). On the other hand, species density was similar on all
tree species, even if slightly higher in I. perado subsp. azorica (Kruskal-Wallis chi2 = 3.18, df = 2, p
= 0.20). This tree species is also the one that accumulates the highest number of specimens per
square meter, while L. azorica presented significantly lower arthropod densities than the other two
tree species (Kruskal-Wallis chi2 = 6.38, df = 2, p = 0.04; post-hoc: L. azorica x I. perado – W = 592,
p = 0.01; L. azorica x J. brevifolia – W = 592, p = 0.049) (Table 4-2).

58
Table 4-2 Summary table with the arthropod species richness (S), abundance (N), number of singletons and doubletons,
uniques and duplicates, number of trees and of samples, average number of species per tree, number of species and
specimens per square meter (values in parenthesis are standardized at 18 samples), diversity indices (Fisher α, Shannon-
Wiener, Shannon Exponential, Simpson, Inverse Simpson and Pielou) for the total number of specimens and for each
individual tree species
I. perado J. brevifolia L. azorica Total
Trees 9 10 5 24
Samples 43 50 18 111
S (q=0) 54 (42.6) 56 (40.6) 40 (40) 69 (42.8)
N 4562 (1903.3) 4869 (1752.7) 1186 (1186) 10617 (1725)
Singletons 13 17 7 18
Doubletons 6 6 7 4
Uniques 14 17 8 18
Doubletons 6 8 6 5
Average species per 26.3 ± 5.8 24.8 ± 4.2 21.4 ± 7.8 24.67 ± 5.7
tree
Species per m2 15.7 ± 4.8 14.0 ± 4.4 14.2 ± 5.2 14.7 ± 4.7
Specimens per m2 106.1 ± 61.4 97.4 ± 58.5 65.9 ± 44.1 95.6 ± 58.6
Fischer α 8.606 8.876 7.989 9.885
Shannon-Wiener 2.591 2.436 2.598 2.592
Shannon Exponential 13.343 11.427 13.437 13.356
(q=1)
Inverse Simpson 8.396 6.338 8.837 7.755
(q=2)
Pielou evenness 0.649 0.605 0.704 0.612

The Hill diversity indices q1 and q2 were lower in J. brevifolia, while being simultaneously
the host tree most influenced by dominant species, although the values for the several measured
indices were in general rather similar for the three host-tree species and for the canopy arthropod
community as a whole (Table 4–2).

The alpha accumulation curve for the totality of collected samples (Fig. 4–2a) showed that
the sampling effort was adequate to collect a large portion of the arthropod communities in the
canopies. The same being true when looking to the corresponding graphical representation of the
accumulation curve slope (Fig. 4–2b). This is also true for the different host tree species (Fig. 4–2c),
each accumulating species at a similar rate. All became slightly asymptotic, this tendency being
clearer in L. azorica, despite the lower number of samples. Low values of the final slopes (the first
derivative of the curves on their final point) for each accumulation curve indicated that inventory
completeness was adequate (Table 4–3).

59
Figure 4-2 Alpha accumulation curves for the full set of data (a), slope of the accumulation curve for the full set of data
(b) and alpha accumulation curves for each tree species (c). Red - I. perado subsp. azorica; Blue - J. brevifolia; Green –
L. azorica.

Calculating the inventory completeness using the Jackknife 1 estimator confirmed that
inventory completeness was in general adequate. For the entire community, almost 80% of the
expected species were collected, with J. brevifolia having the lowest inventory completeness (76.7%)
and L. azorica the highest (85.1%) (Table 4–3).

Table 4-3 Values of Jackknife 1 estimated richness, with corresponding inventory completeness, and value of slope at the
final point of each accumulation curve, for each individual tree species and for the entire dataset (Total)
I. perado J. brevifolia L. azorica Total
Jackknife 1 67 73 47 87
Completeness 80.6% 76.7% 85.1% 79.3%

Slope 0.003384 0.003232 0.006491 0.001834

4.3.3. Colonisation status patterns

In terms of colonization status, roughly 45% of the collected species were endemic, while
25% were introduced. This general pattern of species richness was conserved when considering the
individual host-tree species, albeit with some small non-significant differences (Fig. 4–3), with L.

60
azorica trees having a slightly lower proportion of introduced species (Kruskal-Wallis chi2 = 2.17, df
= 2, p = 0.34). Considering the abundance, the situation changed, with almost 80% of all collected
specimens belonging to endemic species, with the five most abundant species overall being endemic
and encompassing 65% of all collected arthropod specimens. Conversely, only 3.5% of all collected
specimens belonged to introduced species. This same pattern was conserved when considering the
distinct tree species, but with L. azorica having a slightly higher proportion of specimens from
introduced species (5%) and a lower one of natives, while in J. brevifolia only 3% of the collected
specimens where of introduced species (Fig. 4–3). Notwithstanding, these differences were never
significant (Kruskal-Wallis chi2 = 1.37, df = 2, p = 0.50).

Figure 4-3 Relative species richness and abundance of endemic (E), native (N) and introduced (I) arthropods. Ilex - I.
perado subsp. azorica; Jun - J. brevifolia; Lau - L. azorica.

Most endemic species were highly abundant in the canopies, with only six species occurring
as singletons, of which one species was likely a habitat tourist. Fifteen species were present in all
host-tree species, including all the highly abundant endemic species. For native non-endemic species
the pattern was similar, with 12 out of the 22 species occurring in L. azorica, I. perado subsp.
azorica and J. brevifolia. In this case, all the singletons could be considered habitat tourists. This
picture is reversed for the introduced species, since half of the species occur in only one tree species
and of these, eight species appear as singletons, of which three were likely habitat tourists.

Out of the ten most abundant species, eight were endemic and seven were present in all
sampled trees. The introduced spider Ero furcate (Villers), although not as abundant as the other nine
species was also present in all sampled trees. Also worth mentioning is the native salticid Macaroeris
cata (Blackwall), that despite having only 74 specimens, was present in 20 of the 24 trees.

61
Savigniorrhipis acoreensis, the most abundant species in this study, was present in 110 out of 111
samples, while Acorigone acoreensis (Wunderlich) and Gibbaranea occidentalis Wunderlich were
also present in more than 90% of the samples, with this last species being only the sixth most
abundant one. The native curculionid Pseudophloeophagus tenax (Wollaston) should also be
mentioned as, with the exception of one individual collected in I. perado subsp. azorica, it was
present exclusively on J. brevifolia trees (in all of them).

4.3.4. Indicator species

The Dufrêne-Legendre indicator values (IndVal) observed that some arthropod species
seemed to be specialists on a given host-tree, mainly on I. perado subsp. azorica and J. brevifolia
(Table 4–4).

Table 4-4 Summary table of IndVal results, with Indicator species and corresponding host tree, indicator value, statistical
significance of the associations and the frequency. E - Endemic; N - Native; I - Introduced.

Indicator Species Host tree IndVal p-value Frequency

Calacalles subcarinatus (E) I. perado 0.67 0.001 58
Sancus acoreensis (E) I. perado 0.41 0.018 31
Zetha vestita (N) I. perado 0.37 0.040 1
Cheiracanthium erraticum (I) I. perado 0.15 0.021 1
Cinara juniperi (N) J. brevifolia 0.52 0.001 1
Pseudophloeophagus tenax (N) J. brevifolia 0.49 0.001 4
Elipsocus brincki (E) J. brevifolia 0.47 0.003 104
Savigniorrhipis acoreensis (E) J. brevifolia 0.45 0.020 94
Pinalitus oromii (E) J. brevifolia 0.42 0.006 101
Trioza laurisilvae (N) L. azorica 0.30 0.007 23
Hoplothrips corticis (N) L. azorica 0.09 0.033 1

4.3.5. Trophic groups patterns

In terms of trophic groups, circa 50% of the species and 75% of the collected specimens
were predators, mainly spiders (23 species; 7370 specimens), with herbivores comprising 30% of the
species and just 11% of the collected specimens (Fig. 4–4). Once more, this general pattern applies to
individual host-tree species, but with some small variations. L. azorica trees had a slightly higher

62
number of species of herbivores and conversely less number of predator species. I. perado subsp.
azorica trees, on the other hand, had a slightly higher relative abundance of predators. These
differences were, once more, not statistically significant (Abundance: Kruskal-Wallis chi2 = 0.62, df
= 2, p = 0.74; Species richness: Kruskal-Wallis chi2 = 0.55, df = 2, p = 0.76).

Figure 4-4 Relative species richness and abundance of fungivore (F), herbivore (H), predator (P) and saprophyte (S)
arthropods. Ilex - I. perado subsp. azorica; Jun - J. brevifolia; Lau - L. azorica.

4.3.6. Patterns on species relative abundances

Grouping the species into modified Preston’s octaves (Fig. 4–5) it shows that the canopy
community as a whole was composed by many rare species and few intermediately and truly
abundant ones. An α-gambin value of 1.38 indicated that the SAD of this community followed a
logseries in shape (Table 4–4). This was also true if considering the arthropod community associated
with the canopies of J. brevifolia (α-gambin = 1.16). The canopy community of I. perado subsp.
azorica had a bimodal distribution, with many rare species and few truly abundant ones, but also
with several intermediately abundant ones. α-gambin did not fit this distribution properly (chi2 =
14.25; p = 0.16). For the canopies of L. azorica, the community appeared to be composed of several
rare and intermediately abundant species, with very few abundant species, following a lognormal
distribution (α-gambin = 2.69) (see Table 4–5).

If considering the species in the first quarter of the octaves as being truly rare in the
community (Gaston 1994), we have that 35 out of 69 or that 50% of the species were rare in the
community. By the same token, both I. perado subsp. azorica and J. brevifolia accumulated a large
portion of truly rare species (52 and 54%, respectively), while 39% of the species in L. azorica were
truly rare (Fig. 4–5).

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Figure 4-5 Modified Preston's octaves histograms for the entire dataset (a) and for each tree species - I. perado subsp.
azorica (b), J. brevifolia (c) and L. azorica (d), discerning between the endemic (green), native (blue) and introduced
(red) species components.The four graphs are scaled equally for the Y axis.

It was also conspicuous the high proportion of singletons from introduced species on J.
brevifolia, while in all tree species the highly abundant arthropod species are mainly endemic, with
the remaining ones being natives.

Regarding just the distinct colonisation status, a more complex multimodal pattern was
observable for the endemic species, with many rare species, but also with many species of
intermediate abundance, and also most of the truly abundant species (Fig. 4–6). The introduced
species followed a clear logseries (α-gambin = 1.26) and for native species, the poor fit of the model
(α-gambin = 2.43; chi2 = 9.08, p = 0.43) prevented classifying the shape of the SAD as being a
lognormal (see also Table 4–5). Again considering the octaves in the first quarter for each
colonisation status, we had that 44% of the endemic species and 45% of the native species could be
considered rare in their shares of the community, while 55% of the introduced species were also truly
rare when considering this portion of the canopy community.

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Figure 4-6 Modified Preston's octaves histograms for endemic (End), native (Nat) and introduced (Intr) species with
superimposed gambin distribution fits (black dots). The three graphs are scaled equally for the Y axis

Standardizing the samples and repeating these procedures gave us a slightly different
scenario, as shown in Table 4–5. For the entire community and for each tree species with the
exception I. perado subsp. azorica, the values of the standardized α-gambin parameter were
relatively close to the non standardized ones.

Regarding the colonisation classes, and despite the low number of minimum common
specimens between colonization classes generating a larger standard error for the α-gambin
parameter, the values of α-gambin were similar to the non standardized ones, except for the endemic
species, where the very high value of standardized α-gambin might be a reflection of the complex,
multimodal nature of this component of the community.

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Table 4-5. Values of α-gambin parameter for the entire dataset with associated significance tests values for the fit of the
GamBin distribution; and standardized values of α-GamBin parameter for: the total community, for the different tree
species and for colonisation status. The asterisk indicates a good fit of the GamBin distribution to the data.
Tree species Non standardized Standardized

α-gambin Significance test α-gambin

Total 1.38 Chi2 = 22.89; p = 1.70 ± 0.32

0.018 *

Ilex 1.52 chi2 = 14.25; p = 2.13 ± 0.55

0.162

Juniperus 1.16 Chi2 = 26.77; p = 1.59 ± 0.37

0.003 *

Laurus 2.69 Chi2 = 7.89; p = 0.342 2.49 ± 0.28

Colonisation Class Non standardized Standardized

α-gambin Significance test α-gambin

Endemic 1.99 Chi2 = 33.13; p-value 6.21 ± 2.74

= 0.001 *

Native 2.43 Chi2 = 9.08; p-value = 2.41 ± 1.16

0.43

Introduced 1.26 Chi2 = 13.23; p-value 1.38 ± 0.31

= 0.04 *

4.3.7. Patterns in species composition

The first three axes of the NMDS had a stress value of 0.15 indicating that three dimensions
were enough to give an acceptable representation of our data. Figure 4–7 shows I. perado subsp.
azorica and J. brevifolia clumped together, with L. azorica slightly apart. It was possible to observe
that the trees shared a large portion of the arthropod community, even if some dispersion was
noticeable (indicating some heterogeneity in the samples in terms of species composition). Applying
the same procedure for endemic and for native species alone, a tightening of the clusters was
noticeable, along with the dilution of the separation between L. azorica and the other trees, indicating
an even higher proportion of shared species. For native species the situation was distinct, with the
NMDS ordination revealing differences in the communities associated with L. azorica and J.

66
brevifolia. On the other hand, dispersion was low, suggesting a more homogeneous distribution of
the arthropods species in the samples associated with each tree species.

Testing the visual assessment of the NMDS ordination with an Analysis of Similarities
(ANOSIM), I confirmed the low dissimilarity between the communities of the three host tree species
(ANOSIM R2 = 0.17; p = 0.001). The same applied when considering only the endemic species, with
the lower R2 value indicating lower dissimilarities in the communities and a more homogeneous
distribution of the arthropod species (ANOSIM R2 = 0.11; p = 0.003). As mentioned, the NMDS
ordination for native arthropods gave a better discrimination between tree species, but the still
relatively low R2 indicated low dissimilarities between them (ANOSIM R2 = 0.20; p = 0.001).

Figure 4-7 Nonmetric Dimensional Scaling (NMDS) with Bray-Curtis similarities for each tree species. Green - I.
perado subsp. azorica; Red - J. brevifolia; Blue – L. azorica

Considering all specimens, dissimilarities between the communities present in the three
distinct tree species were intermediate, with no particular distinction between tree species (Table 4–
6). These differences were mainly explained by species turnover.

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Table 4-6 Rarefied values of Total β diversity, β Replacement and β Richness between the different tree species in the
study plot- for the entire community, for endemic, for native and for introduced species. Ilex - I. perado subsp. azorica;
Jun - J. brevifolia; Lau - L. azorica.
All Endemic Native Introduced

β-total Ilex Jun β-total Ilex Jun β-total Ilex Jun β-total Ilex Jun

Jun 0.40 - Jun 0.25 - Jun 0.50 - Jun 0.54 -

Lau 0.36 0.41 Lau 0.29 0.33 Lau 0.38 0.52 Lau 0.54 0.45

β-Repl Ilex Jun β-Repl Ilex Jun β-Repl Ilex Jun β-Repl Ilex Jun

Jun 0.34 - Jun 0.19 - Jun 0.40 - Jun 0.43 -

Lau 0.33 0.33 Lau 0.25 0.29 Lau 0.13 0.35 Lau 0.33 0.33

β-Rich Ilex Jun β-Rich Ilex Jun β-Rich Ilex Jun β-Rich Ilex Jun

Jun 0.05 - Jun 0.09 - Jun 0.08 - Jun 0.09 -

Lau 0.04 0.06 Lau 0.05 0.05 Lau 0.27 0.19 Lau 0.17 0.15

Regarding the different colonisation classes, for endemic species, dissimilarities in the
communities of the different trees were relatively low and were mainly caused by species turnover.
For native species, dissimilarities in the community were rather high, particularly between those of J.
brevifolia and the other tree species. For J. brevifolia, this difference was mainly explained by
species turnover, while the dissimilarities between native species between L. azorica and I. perado
were mostly caused by differences in the number of species present. In the case of introduced
species, dissimilarities between the tree species were also rather high, and mainly explained by
species turnover.

4.4. Discussion

There is currently a very high degree of standardization and recommendations regarding

canopy fogging studies (see Adis et al. 1998), which allows for comparable studies and results.
Nevertheless, local constraints, different temporal and spatial scales, variations on the fogger and
fogging technique applied or the use of different formulations of pyrethroid insecticide, in many
cases constrained by market availability or national laws should be taken into consideration when

68
comparing different studies. Adding to this, many canopy fogging studies focus only on one or few
arthropod taxa like beetles (Allison et al. 1993, Floren & Linsenmair 1998) or ants (Floren et al.
2002, Floren et al. 2014) making comparisons more challenging. In addition, to consider is the fact
that in the current study the branches were beaten after fogging the canopies [which is usually
unfeasible in the tropics due to the great height of the tree crowns, but see Marques et al. (2001)]
possibly increasing the numbers of collected species. Tests done in other regions indicate that few or
almost no arthropods remain in the crowns after fogging (Erwin 1990, Stork 1991). However, for the
Azorean forest, due to its closed/complex structure and vast epiphyte layer, branch beating was
necessary, since during the sorting process many small sized specimens, particularly spiders were
found lodged among dense masses of J. brevifolia leaves or in the epiphytic mosses and would not
have been collected by fogging alone (see Yanoviak et al. 2003).

Comparing the abundances of specimens per square meter, the present results are inside the
range of those from tropical forests (although at a fraction of the average number of species per tree)
(Stork 1991, Floren & Linsenmair 1997). However, arthropod densities in Azores are in general
lower than those from other biomes like savannas (Krüger & McGavin 1997) or temperate climates,
which usually have very high arthropod densities per square meter (see Watanabe 1997 for a
comprehensive listing).

Overall, relative abundances and diversity of the several orders were more akin to those of
temperate forests, with spiders taking some of the roles of canopy ants and being the dominant taxon
(Basset 1991, Hsieh & Linsenmair 2011), followed by Diptera, Hymenoptera, Coleoptera and
Hemiptera (not necessarily by that sequence). Proportions of mites and springtails were also in
accordance with results in other parts of the world (see Watanabe 1997).

Looking at the general patterns of abundance and species richness, my findings also agree
with those of previous works in the Azorean archipelago and have similarities with general patterns
for temperate forests, with low species richness and the dominance of a few very abundant species
(Stork 1991, Basset 1991), despite the present community having lower densities than what would be
the case for a temperate forest (see Watanabe 1997). The proportion of singletons and doubletons
were also within those of previous works in Terceira (Gaspar et al. 2008), but slightly lower that
those from Chapter 3.

According with previous studies (Ribeiro et al. 2005, Gaspar et al. 2008), Araneae,
Hemiptera, Lepidoptera and Coleoptera were the most abundant and diverse taxa recorded. Spiders
(including the endemic linyphid Savigniorrhipis acoreensis, which accounts for almost one third of

69
the specimens in my samples belonging to named species) had been previously reported as the most
or one of the most abundant orders in native Azorean forests (Ribeiro et al. 2005, Gaspar et al. 2008,
Nunes et al. 2015), but not at the magnitude present in our samples. Linyphiidae was also found to
be the most abundant spider family in fogging samples from the Canary Islands (Stüben et al. 2010).

Two notable breaks with previous results are the Coleoptera and the Lepidoptera.
Coleoptera, despite not having the relative abundance that they have in other Macaronesian
archipelagos or worldwide (e.g. Erwin 1983a, Stork 1991, Allison et al. 1993, Wagner 1997), were
the most abundant insect order in my samples (Hymenoptera, Diptera and Collembola excluded).
This contrasts with previous studies that indicate that the beetle communities of the Azores are, in
general, characterized by relatively high species richness but very low abundances (Gaspar et al.
2008, Amorim et al. 2012, Terzopoulou et al. 2015, Nunes et al. 2015). This discrepancy with the
data presented in the previous chapter is not easy to explain. Short term seasonal effects are unlikely
as this relatively high abundance was observed in my data in both years and along different sampling
intervals, but the time elapsed between the BALA sampling and my own means that this difference
being part of a longer temporal trend cannot be ruled out. It might also be due to some biotic and
abiotic factors particular to our sampling plot, since the Terra-Brava fragment where the present
study took place is one of the most pristine in Terceira (Borges et al. 2017) and previous works also
included less well preserved fragments of native forest. Another possibility might be that the BALA
protocol has some limitations regarding the sampling of the arboreal communities of native and
endemic Coleoptera from Terceira and the Azores in general. In fact, the high abundance observed in
beetles was due to only two endemic species, the rove-beetle Atheta dryochares Israelson and the
weevil Callacales subcarinatus (Israelson) (see Appendix I). A. dryochares is a very small predatory
beetle and lives associated with different substrates in the Azorean trees, including lichens associated
with tree bark. C. subcarinatus is also a small species that is associated with bark, and consequently
the abundance of both species may have been underestimated with BALA protocol, that targeted
mostly tree leaves. This calls for the importance of using a combination of sampling methods when
performing the inventory or monitoring of arthropod communities (see Cardoso 2009) and also
illustrates the ability of canopy fogging of collecting some cryptic species not easily sampled by
other means (Hsieh & Linsenmair 2011).

Lepidoptera are noteworthy for being present in my samples at a much lower abundance and
diversity from what had been previously reported for this taxon, both for adults and for juveniles,
particularly of adult specimens, as these were an important component of the arthropod communities
in the native forests of the Azores (Gaspar et al. 2008, Nunes et al. 2015, Chapter 3). The low

70
abundance of Lepidoptera could be due to some local phenomenon, but an ongoing parallel study in
the same site with SLAM traps indicates that this should not be the case, as this taxon was quite
abundant in those samples during both years (Rui Nunes, unpublished data). A more likely scenario
is that adult Lepidoptera are not immediately knocked out by the insecticide agent and are able either
to avoid the initial cloud or to fly for a short distance before being knocked out and thus miss the
collecting funnels, but this fails to explain the low numbers of juveniles and, will be further
discussed below.

Another taxon that needs to be mentioned are the Hymenoptera. Worldwide this is one of the
most speciose insect orders (Sharkey 2007), and that seems to be the case for the present samples as
well, with apparently as many RTU’s as all other identified insect (morpho)species combined, but for
a matter of rigor, and for the inability to identify the Hymenoptera reliably into true species, they
were excluded from further analyses. Also, the exclusion in this work of another hyperdiverse and
biologically important group like Diptera will preclude some direct comparisons with previous
studies. Nevertheless, a rough analysis at higher taxon level shows that both orders are an important
component of the canopies in the studied trees, which is in accordance with studies elsewhere (Erwin
1983a, Guilbert 1997, Horstmann et al. 1999, Veijalainen et al. 2012). A more detailed analysis of
the importance of Hymenoptera and Diptera in the Azorean canopy communities, as well as the
quantification of the actual species richness species and even what proportion of species are
indigenous to the archipelago will have to be postponed to a future study.

Regarding the colonisation status of the collected specimens (Acari, Collembola, Diptera,
Hymenoptera and Isopoda excluded), the relative proportions of endemic, native and introduced
species are similar to those seen in the previous chapter, with each colonisation class accounting for
roughly one third of the species, but in terms of relative abundances the figures change, with
endemic species accounting for most of the collected specimens. Greater abundance of endemic
species in the canopies of native forests in relation to native and in particular to introduced species
was expected, as this is reported from previous works (Gaspar et al. 2008, Nunes et al. 2015,
Florencio et al. 2016, Borges et al. 2017), but the very low abundance of introduced specimens was
quite conspicuous (but see Nunes et al. 2015). This might be due to some form of biotic resistance
(sensu Elton 1958) of the arthropod community of native the forests canopies towards invasion.
Other factors such as the harsh conditions present in native forest canopies, the relative isolation of
the extant native forest patches or other hitherto unknown factors related with host-tree physiology
and architecture (Florencio et al. 2016) might also be the cause of the apparent inability of the exotic

71
species in establishing a foothold in the native forests. Nevertheless, the exotic Mimetidae Ero
furcata seems to be relatively widespread in the canopies, even if at low abundances.

4.4.1. Trophic guilds, Araneae and Lepidoptera

As also seen in the previous chapter, and in previous studies in the Azores (Gaspar et al.
2008, Nunes et al. 2015), there is usually a constancy regarding the proportions of functional groups
around the world, with herbivores being generally the most abundant group, followed by predators,
and with detritivores and fungivores being minority groups (Moran & Southwood 1982; Stork 1987,
1991; Krüger & McGavin 2001). But, in my samples predators make a disproportionate component
of the community, both in terms of abundance and species richness. Borges et al. (2008) had also
found more predator than herbivores species in samples from Terceira, while other samples from J.
brevifolia trees had also hinted at a higher than abundance of predators for Terceira (Nunes et al.
2015), but not at the magnitude observed with the current study. It had been advanced that the
propensity of J. brevifolia to accumulate spiders (Ribeiro & Borges 2010) could be a cause for this
high number of predators, but this does not seem to be the case, as this pattern is transversal to the
three host-tree species in the present study. Hypothetically, chemical defenses and lower palatability
or nutritional value on part of the host tree species could also be the cause of lower diversity and
abundance amongst herbivores (Winchester 1997, Abad et al. 2013, Athanassiou et al. 2013), but this
does not seem to be the case (see Chapter 3).

But the causes for the high ratio of predators are, on the other hand, uncertain. A short term
seasonal effect is unlikely, as previously mentioned for beetles, because this pattern was observed in
both years of the study, with distinct time intervals for the sampling period. But looking at the ratios
for the entire island (Chapter 3), it is possible to see that there was also a higher abundance of
predators in the canopies of J. brevifolia in relation to the other groups. This agrees with previous
studies regarding the propensity of J. brevifolia to accumulate spiders (Ribeiro et al. 2005, Ribeiro &
Borges 2010) and might, at least partially, explain the proportion of predators observed, in the
following manner: a) there is a high level of interconnectedness of the canopies in the forest, making
it probable that these act like one continuous habitat, not unlike the “horizontal highways” of Erwin
(1990) and b) as mentioned in Chapter 2, the azorean cedar is the dominant tree species in the plot.
Therefore, one might suppose that there could be a degree of homogenization in the structure of the
community associated with the different tree species, this being heavily influenced by the community
usually associated with J. brevifolia, with its higher abundance of predators.

72
 Low numbers of fungivores were to be expected, as these usually live cryptic lifestyles, for
which fogging might not the most adequate method (cf. Stork & Hammond 1997). Also, only living
trees were targeted in my samples, reducing the amount of available resources for this group.

Returning to the topic of the low numbers of Lepidoptera, and linking it with high ratio or
predators to prey, one can also put forward a hypothesis. It is well established that, particularly in the
tropics, ants exert a high predation pressure over lepidoptera larvae, and other slow moving
arthropod juveniles (Floren et al. 2002). Ants are absent from the Azorean native forests (if due to
biogeographical constraints or to recent extinctions is out of the scope of this work), and as reported
elsewhere, spiders replace ants in the role of predators (Basset 1991), becoming the dominant
predators in the canopies (Ohmart & Voight 1981, Basset 1991), with linyphids being one of the
important families in temperate climates (see Basset 1991), as is also the case with my data. Besides
being generalist predators, several spider families (Linyphiidae among them) have been reported as
predators of Lepidoptera larvae and egg masses (Clark et al. 1994, Miliczky & Calkins 2002,
Pfannenstiel 2008), together with rove-beetles (Clark et al. 1994), another abundant predator family
in our samples. Adding the Hymenoptera, one of the most abundant and the most diverse order in
our samples, particularly the Ichneumonoidea, known parasitoids of Lepidoptera larvae and the
Chalcidoidea, parasitoids of the immature stages of 12 insect orders (Gibson 1993), we have in this
community an immense predatory pressure over the Lepidoptera and other herbivorous taxa. In fact,
it is common to see Lepidoptera in the spider webs in these forests. Therefore, this high predatory
pressure caused by spiders, parasitic wasps and other predators has been reported in other parts of the
world to greatly reduce the abundance but not the diversity of Lepidoptera larvae (Stork 1991, Floren
& Linsenmair 1997, 1998, Horstmann et al. 1999) and possibly also other prey species, which is
similar to what is observed in the present samples.

As a caveat, it might also be that all these trophic group patterns are a consequence of the
forest fragment’s specific biotic or abiotic factors or even part of a long term disturbance, but that is
something that cannot be addressed without further studies.

4.4.2. Differences in species composition between trees

Previous works in the Azores considered J. brevifolia (out of the three host tree species of
this study) to be the host tree species that accumulated more abundance and species richness at the
Azores scale (Ribeiro et al. 2005, 2010). Our results seem to contradict this, with Ilex perado subsp.
azorica being the tree that accumulates slightly more number of species and abundance. The fact that
Terra-Brava site hosts one of the largest population or large individuals of Ilex perado subsp. azorica

73
from Azores may explain this result. Laurus azorica hosted less specimens than the other two, even
after accounting for the differences in sampling effort. Nevertheless, none of these small variations
were significant, the same being true when considering the colonisation status or the trophic groups
of the species that inhabit them.

The most abundant endemic arthropod species were well represented in all tree species,
together with most native species, with only some arthropod species hinting at a clear host
preference, which is in agreement with previous works in the archipelago that suggests that the
majority of the indigenous arthropod community is composed of generalist species (Ribeiro et al.
2005).

Spiders were also less abundant in L. azorica, maybe a consequence of the more open and
less complex crown architecture of this tree species (Ribeiro et al. 2010). On the other hand, Acari
and Collembola abundance was rather constant in all three species, which was to be expected, as
these taxa feed mainly on plant debris and tend to live in the ample soil and epiphyte layers of the
forest canopies, being therefore relatively independent of the host tree species itself (Watanabe
1997).

NMDS ordination and allied ANOSIM confirmed that the communities of the three host tree
species were very close to each other, even if the communities of Azorean laurel were set slightly
apart from the others. These differences are even smaller if only endemic species were considered,
which was also confirmed when observing the low differences in beta diversity between trees for
endemic arthropods.

Beta diversity in the sampled forest patch were in general similar to the results observed for
the entire island in the previous chapter, indicating again, relatively low dissimilarity between the
communities of the distinct tree species, especially in the case of endemic species, with species
turnover being the main factor of variation in species composition between the tree species although
the difference in the number of species was also a factor between L. azorica and I. perado, when
considering native species. Contrary to what was observed for the island, in my samples,
dissimilarities between the trees in terms of introduced species were mainly due to species turnover.

This agrees with the general idea of a community dominated by several highly abundant and
generalist species and some locally rare species, together with a few specialists and several habitat
tourists.

A brief comment regarding the canopy fogging, the final slope values and the adequate
values of species inventory completeness estimates, give a good account of the technique with

74
approximately 80% of the estimated species present being collected. Comparing with BALA data
from five Natural Forest Reserves in Terceira (Chapter 3), I was able to collect in the present study
20 out of 35 endemic species previously reported for for J. brevifolia in Terceira, plus one more
species not collected in BALA, and 17 out of 39 native species reported for this tree species with
four additional species not previously collected. For I. perado subs. azorica, I collected 21 endemic
species out of the 32 reported, plus three new ones, while for natives I was able to collect 12 out of
23 previously reported species plus three additional ones (Chapter 3). In the case of L. azorica, and
despite the low representation in my samples, I was still able to collect 17 out of 27 previously
endemic species, plus an additional one and for natives I was also able to collect 12 out of 27
reported species, with an additional native species not found in L. azorica during BALA (Chapter 3).

Additionally, the advantages of canopy fogging for quantitative studies of the canopy
communities were also quite apparent, as the sampling of 24 trees in my experiment wielded roughly
half the number of specimens collected in the entire BALA project for Terceira island, and as it will
be seen in the next chapter (Chapter 5) the totality of specimens collected by fogging in the forest
plot were roughly equal to those from BALA in Terceira (Chapter 3), even if the number of species
was much smaller, which is not unexpected given that the BALA project collected samples over a
much wider and diverse area than that of my study plot.

75
Chapter 5
Arthropod recolonization processes in the native forest canopies

5.1. Introduction

Of the many canopy fogging studies aimed at increasing the knowledge of the canopy
arthropod communities (see Chapter 2 on methods and references therein), only a few have
investigated the recolonisation and recovery processes of the arthropod communities after
defaunation events (e.g. Erwin 1990, Stork 1991, Azarbayjani et al. 1999, Mody et al. 2003), and in
many cases do so targeting specific taxa (Floren & Linsenmair 1998, Horstmann et al. 1999) or
testing the efficacy of insecticides on commercial plantations (Loch 2005).

Other studies about the recovery of arthropod communities are those related with the
application of insecticides on agricultural fields (Duffield & Aebischer 1994, Duffield et al. 1996),
but due to large differences in terms of habitat and scale, the simple transposition of these approaches
to the canopies of native forests of the Azores, can only offer a tangential insight into the recovering
processes therein.

Recolonization, in the true sense of the word, will occur by immigration of species and
individuals into the canopy from the surroundings (Stork 1991, Trumper & Holt 1998), but faunal
recovery might also occur from species/individuals surviving the fogging and multiplying or from
egg masses protected from the insecticide (Stork 1991, Trumper & Holt 1998). Besides this, the
interaction with other factors, like predator-prey interactions, can also affect the recovery of the
community (Duffield et al. 1996, Loch 2005). Studies with pesticides on agricultural fields also
identified particular spatial patterns of recovery for predator and prey species that are also influenced
by edge effects (Duffield & Aebischer 1994, Duffield et al. 1996).

The recovery process is time dependent. The time interval between the initial fogging and
some form of community recovery can be as short as ten days (Erwin 1990), or even just one day
(Floren & Linsenmair 1998). Some recoveries however can be a much longer process. For instance,
Stork (1991) reports total recovery of the arthropod fauna after two months in oaks in the UK, while
Mody et al. (2003) reports total recovery in savanna trees after one year and Horstmann et al. (1999)
found the recovered communities in Malaysia indistinguishable from the original ones after a period
of 3-4 years, but not after 7-19 months. The recovery can also be dependent on biodiversity patterns,
that is, total recoveries in terms of abundance or species richness are many times disharmonious,

76
with high species turnover, and with large differences in terms of rank abundances, when compared
with the initial communities (Floren & Linsenmair 1997, Azarbayjani et al. 1999, Loch 2005). These
studies also reveal that different groups of arthropods or even closely related groups recover at
different rates and in distinct ways (Loch 2005). Moreover, even if the community recovers at a
higher taxonomic level, at lower levels the situation might be different (Floren & Linsenmair 1997,
1998, Azarbayjani et al. 1999). The taxa evaluated can also affect the perception of the
recolonisation and recovery rates, as seen in the case of hyper-diverse beetle communities in the
tropics, or other in the case of a taxon like spiders, that in some cases seem to be less influenced by
the tree characteristics (Azarbayjani et al. 1999, Mody et al. 2003).

There is also evidence that, at least in some habitats, not only the characteristic of the tree
species, but of the individual tree itself might influence its associated community and its subsequent
recovery (Mody et al. 2003).

It is also apparent that in the tropics, at least for communities or for particular taxa that are in
situation of non-equilibrium, or for communities composed mainly of hyper-diverse, rare species,
faunal recovery follows in general stochastic patterns. In temperate forests dominated by few very
abundant species (Basset 1991 and references therein), or in some cases, in disturbed habitats (Rigal
et al. 2018), faunal recovery seems to follow more deterministic patterns, with values of taxonomic
diversity lower on the recovered communities than those that would be expected in randomly
assembled ones (Floren & Linsenmair 1998, Rigal et al. 2018).

Regarding insular biotas, despite our current knowledge of island biogeography and patterns
of species diversity and abundance, knowledge concerning corresponding patterns of functional
diversity (FD) are still scarce (Whittaker et al. 2014). Island biotas are in general disharmonious,
with vacant niches, and are a product of one or more dispersal events and associated barriers, and
posterior in situ speciation and diversification (Warren et al. 2015). These biotas are also particularly
susceptible to recent contact with humans and all the derived anthropogenic changes, in particular
habitat destruction and the introduction of new potentially invasive species (Sax et al. 2002). These
insular communities also have limited functional diversity, probably derived from the several filters
encountered during their formation, or as consequence of recent, human mediated extinctions
(Cardoso et al. 2010; Terzopoulou et al. 2015), which also leaves them more susceptible to invasion,
with the input of new functions brought by introduced species (Whittaker et al. 2014).

As such, besides allowing for the pioneering study of the effects of defaunation and of the
subsequent recolonisation processes, my work presents also an opportunity to analyze the functional

77
diversity at a local/fine scale (see e.g. Whittaker et al. 2014 for a regional approach), and to evaluate
the effects of recolonisation and recovery processes over the taxonomic and functional diversity of
the canopy arthropod community in native Azorean trees. Ribeiro et al. (2005) showed that the
Azorean canopy fauna is dominated by generalist species (see also Chapters 3 and 4 of this thesis).
Moreover, Florencio et al. (2016) demonstrated that Azorean arboreal arthropod fauna is resistant to
exotic species. Borges et al. (2008) and Matthews et al., (2014) showed that those exotic species are
rare in the community and dominated by tourist species adapted to other habitats in the surrounding
land-use matrix. Concerning functional diversity, Whittaker et al. (2014) showed that the addition of
new species in the community, increase functional richness in a similar amount with no signs of
saturation, exotic species adding new functions. Based on these previous results one may predict
when comparing before and after defaunation:

Given the generalist status of Azorean arthropod species (Ribeiro et al. 2005), a rapid
recolonization process will occur after defaunation leading to the rapid reestablishment of similar
richness, composition and species abundance distribution in canopy arboreal communities;

The low diversity and abundance of introduced species in the canopies (see Chapter 4 and
Florencio et al. 2016) suggests these are vagrants and not a functional part of the community, hence I
expect higher levels of beta diversity than for indigenous species with no increase in species richness
as exotics should be filtered by the architecture of tree canopies and not biotic resistance;

The fact that the arboreal arthropod fauna is resistant to exotic species (Florencio et al. 2016)
may imply either a facilitation process in the spread of exotic species after defaunation (empty niche
effect) if the exotics are filtered by competition, or no effect if exotics are filtered by the architecture
and biotic and abiotic conditions of the tree canopies;

In addition, the lack of saturation in functional trait space of indigenous arthropod fauna in
Azores (Whittaker et al. 2014) may also imply that the fauna of Azores will be vulnerable to further
colonization and probably invasion of exotic species with new traits during the recolonization
process. This would also imply an increase in FD in the recolonised community, especially for the
introduced species.

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 5.2. Methods

5.2.1. Study site

Terceira Island, in the Azores Archipelago. The sampling took place in the Terra Brava
Nature Reserve, on the study plot described in Chapter 2.

5.2.2. Data collection

All arthropods were collected using the canopy fogging protocol described in Chapter 2.

5.2.3. Arthropod dataset

All the arthropods were collected by pyrethrum knockdown in conjunction with branch
beating (as described in Chapter 2) on 24 native Azorean trees, namely the fifteen trees (six Ilex
perado subsp. azorica, seven Juniperus brevifolia and three Laurus azorica) fogged for the first time
in 2014 and then fogged for the second time in 2015 (except for one L. azorica specimen that died),
plus the eight trees (three specimens of each of I. perado subsp. azorica and J. brevifolia and two of
L. azorica) fogged for the first time in 2015 to act as controls (see Chapter 2 for further details).

5.2.4. Data analysis

All statistical analyses were implemented in R version 3.3.3 (R Core Team, 2017), with
some basic calculations and graphics being performed in LibreOffice spreadsheet (The Document
Foundation).

Some basic community metrics comparing the different years and fogging episodes (if it was
the first or the second time that a given tree was fogged) were calculated using the procedures
described in Chapters 3 and 4.

The R package gambin (Matthews et al. 2014) was used to assess the distribution of species
abundances for the arthropod community between years and fogging episodes, with the binning of
the arthropods species into modified Preston's octaves following the third method described in Gray
et al. (2006). This was done taking into consideration the colonisation status (Endemic, Native and
Introduced) of the species.

79
 The BAT package (Cardoso et al. 2015) was used to calculate both Taxonomic Diversity
(TD) and Functional Diversity (FD) for the conjunction of year and fogging episode.

TD is equivalent to species richness, while calculations of FD are based on a functional tree

(Petchey & Gaston 2002, 2006), which measures the FD of a community as the total branch length of
a tree linking all species represented in such community. This functional tree was created using first
the cluster package (Maechler et al. 2017) to compute all the pairwise dissimilarities (distances)
between observations, with the Gower distance as metric, and then creating the functional tree itself
by using the UPGMA agglomeration method (Sokal & Michener 1958) of hierarchical clustering.
The traits matrix consisted of categorical and continuous morphological trait variables of ecological
significance, namely: i) body length, ii) type of food ingested, iii) method of acquiring food, iv)
mode of ingesting the food, v) diel activity and vi) habitat type. All traits were equally weighted and
juveniles were also included in the matrix, and discriminated from adults when justified (for
juveniles of Lepidoptera and Neuroptera, basically). The species traits used were in the Azorean
Biodiversity Group database and were collated from an extensive literature search of ecological
information, first descriptions and from taxon experts (Gaspar unpublished, Whittaker et al. 2014,
Rigal et al. 2018). Some (three) species collected in my study were recorded for the Azores after the
elaboration of this database, and therefore all categorical traits were extrapolated based on the
information for the corresponding genus and/or family.

All the analyses were performed for the entire community, discerning between year and
fogging episode, but also for several subsets of it: a) colonisation status, b) adults and juveniles, c)
predators and non predators, d) spiders only, e) with the exclusion of singletons and doubletons, and
f) with the exclusion of locally rare species (with less than 10 individuals). As a side-note, I opted to
use “non-predators” instead of the more logical “herbivores” due to the very low abundance of this
last trophic group in my samples.

TD and FD were calculated for the full dataset and also rarefied by the minimum common
abundance per tree, but given the imbalance in terms of number of fogged trees, number of samples
and in abundance between trees years and fogging episodes, only the rarefied datasets were used for
the calculations regarding TD and FD.

In the case of the introduced species, due to the extremely low number of specimens present
in each tree, no rarefaction was performed as this would lead to a great loss of information, and the
actual TD and FD was used.

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 The Kruskal-Wallis rank sum test was performed to identify potential differences between
factors (first or second fogging per year), both in terms of taxonomic and functional diversities, using
the rarefied datasets.

If differences were present, a Wilcoxon signed rank test (Wilcoxon 1945) was performed on
pairs of factors, to ascertain which ones were different.

To evaluate if in any factor, or group of factors, the community was a subset with higher or
lower taxonomic and/or functional diversity that what would be expected by chance, a null model
was created. For this model random assemblages (null assemblages) were remodeled, in which
modeling was based on the species richness of the total arthropod assemblage collected by fogging.
All species were pooled together, rarefied and randomly reordered 1000 times. The average alpha
diversity from these null assemblages was then estimated. To calculate the deviation in the observed
communities from what would be expected by chance, the average expected values of alpha diversity
were subtracted from the observed values of alpha diversity. The graphical distribution of the
simulations was analyzed visually, while the significance of this deviation was ascertained through
sets of paired t-tests. The same procedure was used to evaluate functional diversity, using the
previously created functional tree.

Besides pooling the entire community, species were also pooled using other subsets and the
corresponding null assemblages created, repeating the procedure and analyses described. These
additional subsets were the same mentioned above.

See Strauß et al. (2016) for further details on the inspiration for the null model used.

Like in previous chapters, Beta diversity calculations were performed using the R package
BAT. Total differentiation between each year and fogging regime was divided into its species
replacement (βrepl) and species richness differences (βrich) components (Carvalho et al. 2012) using
the same R package. As with the previous chapters, this was performed for the entire community and
for colonisation status. To account for the differences in sampling effort, beta diversity calculations
were performed rarefied at the minimum common denominator and with 1000 iterations.

5.3. Results

A total of 21,275 specimens, belonging to 75 species were collected in the two years of this
study, of which 10,658 specimens belonging to 55 species were collected in the trees fogged for a
second time in 2015. Table 5–1 summarizes the diversity and abundance information regarding the

81
collected specimens, per year and fogging episode, along with some other relevant metrics. This total
excludes the arthropods belonging to the taxa that were not identified to species level (Hymenoptera,
Diptera, Acari, Collembola and Isopoda), by the motives presented in Chapter 2.

Table 5-1. Summary table with the arthropod species richness (S), abundance (N), number of singletons and doubletons,
number of trees and of samples, average number of species per tree, number of species and specimens per square meter,
for the total extent of the fogging experiment, and for each year and fogging episode combination. A total of 24
individual trees were fogged during the experiment, but if considering those that were fogged for a second time as nwe
trees, that total ascends to 39 – in parenthesis in the table below. 2014_1t – trees fogged in 2014; 2015_1t – control trees
fogged for the first time in 2015; 2015_2t – trees initially fogged in 2014 and fogged for a second time in 2015.
Fog/Year 2014_1t 2015_1t 2015_2t Total
Trees 16 8 15 24(39)
Samples 73 38 68 179
S 56 53 55 75
N 5534 5083 10658 21275
Singletons 13 14 11 14
Doubletons 2 5 6 8
Average species per 22.9±5.7 28.1±4.0 25.9±3.5 21.1±4.9
tree
Species per m2 13.3±4.4 17.2±4.2 16.6±3.0 15.4±4.2
Specimens per m2 75.8±47.3 133.8±60.5 156.7±77.4 118.6±72.6

Despite some differences regarding the number of fogged trees or the number of collected
samples, the number of species was similar between the different fogging events. The total number
of specimens collected was considerably lower in 2014 that in the same trees from 2015 (2015_2t),
as was the number of specimens in the control trees (2015_1t), but allowing for differences in the
number of samples, these become roughly equivalent. The average number species per tree in 2014
was lower than the one from the control trees (Kruskal-Wallis chi2 = 6.02, df = 2, p = 0.049; 2014_1t
x 2015_1t: W = 26, p = 0.02). Species density (species per m2) was significantly different between
the years and fogging episodes (Kruskal-Wallis chi2 = 28.51, df = 2, p = 6.64e-7), with the samples
from 2014 having considerably lower values than those from 2015 (2014_1t x 2015_1t: W = 705.5, p
= 2.20e-5; 2014_1t x 2015_2t: W = 1378.5, p = 4.99e-6). There were also statistically significant
differences regarding specimen density (Kruskal-Wallis chi2 = 47.16, df = 2, p = 5.74e-11), and once
more, samples from 2014 had considerably lower densities than those from 2015 (2014_1t x
2015_1t: W = 628.5, p = 2.46e-6; 2014_1t x 2015_2t: W = 929.5, p = 1.51e-10).

Regarding the colonisation status, in terms of species richness there were no statistically
significant differences between years and fogging episodes for the relative proportions of endemic,

82
native and introduced species (Kruskal-Wallis chi2 = 0.158, df = 2, p = 0.924), even if in 2014 the
community had a higher proportion on introduced species and a lower proportion of endemic species
that those found in both the control and the recolonised trees of 2015 (Fig. 5–1).

Considering the abundance, a decrease in the proportion of specimens of introduced species

was clear in the trees that were fogged for a second time in 2015 (the recolonised community). They
comprised only 1% of the collected specimens, which was even smaller than the proportions of
introduced specimens in the sample from 2014 (4%), or in the control trees fogged in 2015 for the
first time (3%) (Fig. 5–1). The large majority of collected specimens were endemics, accounting for
roughly 80% of all collected specimens. These differences were statistically not significant (Kruskal-
Wallis chi2 = 2.667, df = 2, p = 0.875).

Figure 5-1 Relative species richness (left) and abundance (right) of endemic (End), native (Nat) and introduced (Intr)
arthropods, for each year and fogging episode combination. 2014_1t – trees fogged in 2014; 2015_1t – control trees
fogged for the first time in 2015; 2015_2t – trees initially fogged in 2014 and fogged for a second time in 2015.

Concerning the trophic status, despite a slight increase in the proportion of herbivore species,
and a reciprocal decrease in the proportion of predator species in the recolonised trees, the general
patterns is preserved on both years and fogging episodes, with predators accounting for almost half
of the species collected (Fig. 5–2). Regarding the abundance, despite a decrease in the relative
abundance of specimens from predator species in the recolonised trees, relative abundances remained
fairly constant in both years and between fogging episodes (Fig. 5–2). Relative abundances of
herbivores remained virtually unchanged through the experiment. Also conspicuous was the
extremely high proportion of predators.

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 None of these differences were statistically significant, both in terms of species richness
(Kruskal-Wallis chi-squared = 0.009, df = 2, p = 0.995), or of abundance (Kruskal-Wallis chi-squared
= 1.077, df = 2, p = 0.584).

Figure 5-2 Relative species richness (left) and abundance (right) of fungivore (F), herbivore (H), predator (P) and
saprophyte (S) arthropods, for each year and fogging episode combination. 2014_1t – trees fogged in 2014; 2015_1t –
control trees fogged for the first time in 2015; 2015_2t – trees initially fogged in 2014 and fogged for a second time in
2015.

In relation to species abundance distribution (SAD) for arthropod community collected in

2014 and for the community in the following year (Fig. 5–3), it is clear that despite having the same
overall shape, some differences were noticeable, namely a decrease in the number of rare species and
an increase in the number of intermediately and highly abundant species in the recolonised trees.
Also, for introduced species, in 2014 these were fairly well represented in the canopies by
intermediately abundant species, but in the recolonised trees, all introduced species could be
considered locally rare, with the exception of the mimetid spider Ero furcata and of the leafroller
moth Rhopobota naevana (Hübner).

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Figure 5-3. Modified Preston's octaves histograms for the for the community present in the trees fogged for the first time
in 2014 (2014_1t) and for the community present in those same trees fogged for the second time in 2015 (2015_2t), with
discerning between the endemic (green), native (blue) and introduced (red) species components. Both graphs are scaled
equally for the Y-axis.

When ranking the species by abundance, with one single exception, the ten most abundant
species remained the same along both years and in the different fogging episodes, despite some
alterations in their rank position (Table 5–2). The following species were among the five most
abundant species: the endemic linyphid Savigniorrhipis acoreensis (the single most abundant
species), the endemic spiders Rugathodes acoreensis Wunderlich and Acorigone acoreensis, and the
native spider Lathys dentichelis. The endemic psocid Elipsocus brincki Badonnel had a sharp
increase in abundance on trees that were fogged for the second time in 2015, an increase that was not
followed in the control trees that were fogged for the first time in the same year.

85
Table 5-2 Rank abundance of the ten most abundant species, ordered by abundance values for the initial community of
2014. 2014_1t – trees fogged in 2014; 2015_1t – control trees fogged for the first time in 2015; 2015_2t – trees initially
fogged in 2014 and fogged for a second time in 2015. E – Endemic; N – Native.
Species 2014_1t 2015_1t 2015_2t

Savigniorrhipis acoreensis (E) 1 1 1

Rugathodes acoreensis (E) 2 3 5

Lathys dentichelis (N) 3 5 4

Acorigone acoreensis (E) 4 2 3

Trigoniophthalmus borgesi (E) 5 4 6

Elipsocus brincki (E) 6 12 2

Gibbaranea occidentalis (E) 7 7 9

Atheta dryochares (E) 8 6 7

Sancus acoreensis (E) 9 8 10
Cinara juniperi (N) 10 9 8

Among these ten most abundant species, eight were endemic and the remaining two were
native species. Equally, six of these ten species were spiders.

Regarding β diversity and the partition into its components of β Replacement and β
Richness, it was found that there were less differences in terms of β diversity between both
communities fogged in 2015 than between the initial community of 2014 and the control trees of
2015. In both cases higher values of β Replacement indicate that species turnover was the main
factor of variation in species composition between years and fogging events. When considering only
endemic species, dissimilarities between the communities were rather less evident, and once again
the major differences in the communities were between years. Species turnover was quite low
between the communities of 2015 and the initial community of 2014, and virtually inexistent
between the control trees and the recolonised community (emphasised in boldface, Table 5–3). On
the other hand, for the introduced species it is quite conspicuous that the three communities were
highly dissimilar, particularly between the initial 2014 community and both communities from 2015.
High rates of species turnover were the main cause for this differences, more so between the initial
community and the recovered community Table 5–3).

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Table 5-3 Rarefied values of Total β diversity, β Replacement and β Richness between the different years and fogging
episodes, for the entire community, for endemics and for introduced species. 2014_1t – trees fogged in 2014; 2015_1t –
control trees fogged for the first time in 2015; 2015_2t – trees initially fogged in 2014 and fogged for a second time in
2015
All Endemic Native Introduced

β-total 2014_ 2015_ β-total 2014_1t 2015_1t β-total 2014_1t 2015_1t β-total 2014_1t 2015_1t
1t 1t

2015_1t 0.42 - 2015_1t 0.26 - 2015_1t 0.36 - 2015_1t 0.71 -

2015_2t 0.42 0.28 2015_2t 0.24 0.12 2015_2t 0.38 0.29 2015_2t 0.71 0.50

β-Repl 2014_ 2015_ β-Repl 2014_1t 2015_1t β-Repl 2014_1t 2015_1t β-Repl 2014_1t 2015_1t
1t 1t

2015_1t 0.38 - 2015_1t 0.15 - 2015_1t 0.36 - 2015_1t 0.53 -

2015_2t 0.30 0.17 2015_2t 0.17 0.00 2015_2t 0.30 0.20 2015_2t 0.63 0.43

β-Rich 2014_ 2015_ β-Rich 2014_1t 2015_1t β-Rich 2014_1t 2015_1t β-Rich 2014_1t 2015_1t
1t 1t

2015_1t 0.03 - 2015_1t 0.11 - 2015_1t 0.0 - 2015_1t 0.19 -

2015_2t 0.13 0.10 2015_2t 0.04 0.08 2016_2t 0.05 0.1 2016_2t 0.06 0.14

In terms of the relation between Taxonomic and Functional diversity, in all instances and
combinations, and for both the full set of data and for the rarefied data, the FD increased
proportionally with the increase in TD, showing no signs of saturation (Fig. 5–4).

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Figure 5-4 Relationship between taxonomic richness (TD) and functional richness (FD) for the entire community and for
several subsets. For each subset, the graphic on the left (black dots) uses the real values for each subset, and the one on
the right (blue dots), the rarefied values of TD and TD. td – taxonomic diversity; tdr – rarefied taxonomic diversity; fd –
functional diversity; fdr - rarefied functional diversity. Summary of regression results in Appendix III.

88
 Regarding the taxonomic and functional diversity of all communities (the initial 2014
community, the community of the recolonised trees and that of the control trees from 2015), it is
possible to observe that overall tendencies are maintained through the different subsets of data [a)
colonisation status, b) adults and juveniles, c) predators and non predators, d) spiders only, e) with
the exclusion of singletons and doubletons, and f) with no rare species (Fig. 5–5). Only introduced
species, and spiders to a lesser extent, seem to display a decline in both TD and FD in the
recolonised community.

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Figure 5-5 Rarefied taxonomic diversity (TDr) and functional diversity (FDr) values for the distinct fogging episodes.
Values are calculated for the entire community and for its several subsets. For each subset, the graphic on the left refers
to the TD, and the one on the right (coloured green) to the FD. Significant differences are indicated with a red star
symbol. 2014_1t – trees fogged in 2014; 2015_1t – control trees fogged for the first time in 2015; 2015_2t – trees
initially fogged in 2014 and fogged for a second time in 2015.

90
 The most conspicuous pattern was that TD and FD values were rather similar for the initial
community, for the recolonised trees and for the community of the control trees. Kruskal-Wallis rank
sum tests showing no significant difference between these factors, either for the whole community or
for any other subsets of data (p-value > 0.05). This was in general mirrored by the other subsets of
the community.

Considering now the extent to which the communities I studied would differ from others in
case they were randomly assembled (a “null community”), it is quite clear that, in general, TD and
FD was significantly lower than what would be expected from a randomly assembled null
community, either for the initial 2014 community, for the community of the recolonised trees and for
that of the control trees from 2015. Significant differences are indicated in Figure 6 and the results of
the significance tests are summarized on Table 5–4.

General trends for the subsets were not so conspicuous, but TD and FD were in general
comparatively lower in the recolonised community that in the other fogging episodes when
considering only predators or spiders, or when removing all the singletons and doubletons.

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Figure 5-6 Comparison between the TD and FD of the sampled communities and that of a null community. Values are
calculated for the entire community and for its several subsets. For each subset, the graphic on the left refers to the TD,
and the one on the right (colored green) to the FD. Significant differences are indicated with a red star symbol. 2014_1t –
trees fogged in 2014; 2015_1t – control trees fogged for the first time in 2015; 2015_2t – trees initially fogged in 2014
and fogged for a second time in 2015.

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Table 5-4 Summary of the T-test significance values for the differences between the communities of the distinct fogging
episodes in my study and that of the equivalent null community.
Subset Factor TD FD
All 2014_1t T-test p= 0.005 T-test p= 0.223
2015_1t T-test p= 0.010 T-test p= 0.003
-5
2015_2t T-test p= 3.294 e T-test p= 3.357 e-5
Indigenous 2014_1t T-test p= 0.0001 T-test p= 0.200
2015_1t T-test p= 0.054 T-test p= 0.012
2015_2t T-test p= 0.004 T-test p= 0.002
Endemic 2014_1t T-test p= 0.0001 T-test p= 0.001
2015_1t T-test p= 0.026 T-test p= 0.025
2015_2t T-test p= 0.046 T-test p= 0.005
Introduced 2014_1t T-test p= 0.003 T-test p= 0.001
2015_1t T-test p= 0.002 T-test p= 0.005
2015_2t T-test p= 0.0004 T-test p= 0.0003
No Singletons/Doubletons 2014_1t T-test p= 0.001 T-test p= 0.165
2015_1t T-test p= 0.008 T-test p= 0.002
2015_2t T-test p= 1.356 e-5 T-test p= 7.450 e-5
Adults 2014_1t T-test p= 0.007 T-test p= 0.269
2015_1t T-test p= 0.109 T-test p= 0.155
2015_2t T-test p= 0.008 T-test p= 0.153
Juveniles 2014_1t T-test p= 0.001 T-test p= 0.112
2015_1t T-test p= 0.002 T-test p= 0.019
2015_2t T-test p= 2.993 e-5 T-test p= 0.0001
No rares 2014_1t T-test p= 8.901 e-6 T-test p= 0.018
2015_1t T-test p= 0.009 T-test p= 0.004
2015_2t T-test p= 9.115 e-6 T-test p= 1.936 e-5
Predators 2014_1t T-test p= 0.784 T-test p= 0.764
2015_1t T-test p= 0.277 T-test p= 0.033
-5
2015_2t T-test p= 3.808 e T-test p= 0.001
Non-predators 2014_1t T-test p= 1.527 e-5 T-test p= 0.031
2015_1t T-test p= 0.006 T-test p= 0.0003
2015_2t T-test p= 0.0001 T-test p= 3.381 e-5
Spiders 2014_1t T-test p= 0.606 T-test p= 0.294
2015_1t T-test p= 0.626 T-test p= 0.382
2015_2t T-test p= 0.0004 T-test p= 0.003

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 5.4. Discussion

A period of roughly one year passed between the initial and the second fogging of the same
trees, and therefore for the recolonisation of the trees and recovery of the community. This time
interval did not allow for a more refined understanding of the recolonization processes, but logistical
constraints prevented any refogging experiment in a short interval after the initial fogging in 2014.
Refogging experiments after an intermediate interval (six months after the initial fogging, i.e.) would
also be unfeasible, as that would coincide with the harsher winter months, and besides the
methodological problems presented by the rain and wind, annual variations in the arthropod
communities mediated by the climate would interfere in the compatibility of the data (Rui Nunes,
unpublished data). Moreover, a recent publication by Borges et al. (2017) on seasonal trends in
Azorean arthropods shows clearly that the peak of activity coincides with my sampling campaigns,
which validates the taken options.

In general, the communities seem to have recovered well, both in terms of abundance and of
species composition, which confirms my first prediction. The differences between the initial
community of 2014 and that of the same trees fogged again in 2015 (either in number of collected
specimens, or in terms of average numbers of species or of specimens per sample/square meter or per
tree), are most likely due to weather constraints and logistical difficulties, experienced during the
2014 campaign, than to major differences between the initial arthropod community and that of the
recovered community, as shown by the similarities in values between the recovered community and
that of the control trees (Table 5–1) and corroborated by the low dissimilarity values in terms of β
diversity for endemic species, particularly those between the control and the recovered communities
(Table 3).

Equally, with one exception, the most abundant species remained the same, despite some
fluctuations in rank between the three communities (initial, recovered and control). As for the
endemic psocopteran Elipsocus brincki, little is known about the ecology of this species (P. Borges,
personal communication) and further studies would be necessary to ascertain if the sharp increase in
abundance was a consequence of the defaunation and subsequent recolonisation processes, or some
intrinsic population pattern.

My results also show some constancy regarding at the trophic groups, with the relative
proportions of species richness and abundance remaining more or less unaltered through the distinct
fogging episodes (Moran & Southwood 1982, Stork 1987), even if still dominated by predators (see
Chapters 2 and 3, Borges et al. 2008, Nunes et al. 2015).

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 There was a decline in abundance of specimens of introduced species in the recolonised
community. Despite suffering only a small decline in species richness, something that was also
mirrored in the control trees, the real and relative abundances of specimens from introduced species
took a sharp decline, with specimens from introduced species accounting for only 1% of the 10658
arthropods collected in the recolonised trees. This result favors prediction four, i.e. exotic arthropods
are possibly filtered by the architecture and biotic and abiotic conditions of the tree canopies and
cannot recolonize faster. In fact, in the recolonised community, with the exception of two species
[Ero furcata (Araneae) and Rhopobota naevana (Lepidoptera)], all introduced species could be
considered rare: This differs from the community of 2014, where there were present several
intermediately abundant introduced species and agrees with the observed decline in abundance.
Accordingly, most of the intermediately abundant and abundant species were endemic, as well as the
three most abundant ones. In fact, of the 11 introduced species present in the recolonised community,
five were singletons, two were doubletons and only the two aforementioned species had more than
ten specimens in total in my samples.

This points to a resilience by the indigenous canopy arthropod communities towards

disturbances and invasions. It was already established that the introduced species have some
difficulty in establishing themselves in the canopy habitat of the native forests (Gaspar et al. 2008,
Nunes et al. 2015, Florencio et al. 2016, Borges et al. 2017), with the introduced species present
being those that dispersed by stochastic processes into the canopies, with few being able to thrive at
low abundances. The harsh biotic and abiotic conditions presented by the canopies and the relative
isolation of the remaining forest patches (Florencio et al. 2016), as well as some form of interaction
with the highly abundant native and endemic species present might be some of the reasons for this
apparent inability by the introduced species in penetrating the canopy habitat. The role of the
architecture of the tree canopies as I mention in prediction three must have also a role.

After the defaunation event, it seems that the recovery by the indigenous community was
relatively fast, with the vacant niches being quickly recolonized by the mostly generalist and very
abundant native and endemic species present in the surrounding host plants, and facilitated by the
interconnectedness of the surrounding canopies, something that is corroborated by the very low or
almost inexistent species turnover. On the other hand, with some exceptions, the introduced species
will most likely reach the recently defaunated trees by stochastic dispersion and source-sink
processes with the nearby matrix of disturbed habitats, which will take more time to act, and it could
be argued that introduced species will not recover to a composition close to the original one, as most
of these species are likely vagrants, and not part of the community, which seems to be confirmed by

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the very high turnover rates observed for these species. This was also found in other works (Floren &
Linsenmair 1997, 1998, Azarbayjani et al. 1999, Mody et al. 2003), where in communities, or
subsets of the community, composed of rare or locally rare species subjected to stochastic processes,
the very high species turnover rates observed lead to recoveries in terms of abundance, but with
distinct and disharmonic species assemblages, which in the present work would be the case of the
introduced species, but not for the endemic or native species.

The fact that for the initial community, the control and the recovered communities the values
of TD and FD were statistically indistinguishable supports the evidence for a quick recovery of the
canopy communities, and therefore of its resilience towards disturbances. The significantly lower
values of TD and FD when compared with those expected from a community assembled randomly
seems to indicate a certain structure on the community, and that at least for some subsets of the
community, their recovery followed a deterministic pattern.

After the defaunation of the trees, subsequent recolonization processes began, with the main
input most logically coming from the available species pool, in this case, the communities present in
the surrounding, interdigitating trees, that are dominated by abundant and very abundant native and
endemic species. This would explain the very low abundance of introduced species present in the
recolonised trees, as well as the observed decrease in FD and TD in relation to the initial community,
with the loss of FD signaling the loss of the novel traits associated with the introduced species of
spiders (Rigal et al. 2018).

As previously stated, several of the combinations tested were not independent from each
other. For example, most of the introduced species present were considered rare species, as such, the
removal from the analysis of the singletons and doubletons, or the removal of the species with ten or
less representatives will also effectively remove almost all introduced species.

Regarding the relation between taxonomic and functional richness, there is a strong positive
relation between both, with FD increasing with the increase of TD and showing no evidence of
saturation. This indicates that the canopy fauna present in the native forests seems to remain
relatively unsaturated in terms of functional trait space. Similar results were found by Whittaker et
al. (2014) for the Azorean archipelago at a regional scale. However, the current results seem to imply
that this lack of trait saturation does not necessarily imply a vulnerability to invasion by introduced
species with distinct functional traits, as the community appears to remain rather resistant to
invasion, even with the generated disturbances and vacating of niches created by the fogging. In fact,

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TD and FD had in general only small fluctuations between years and fogging episodes, except for the
introduced species, where it suffered a decline.

This seems to refute my last prediction, that lack of trait saturation would leave the
arthropod communities vulnerable to invasion and that an increase in FD would be expected.

Of course one must not forget that the disturbances generated by the fogging, despite severe,
were punctual and located well inside the forest. If a larger contiguous area would have been
defaunated, or if this defaunation would have occurred in the forest edges, the community recovery
might have been different. The following chapter might provide some insights into this matter.

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Chapter 6
Isolated azorean cedar trees in a semi-natural pasture of Terceira
Human activities are altering and destroying the natural landscapes at an increasing rate
(Vitousek et al. 1997, Foley et al. 2005), changing the ecosystems structure and function (Vitousek et
al. 1997), endangering these ecosystems and putting biodiversity in general at risk of extinction
(Pimm et al. 1995, Tilman et al. 2001, Hanski et al. 2007). Extinctions can also occur as a delayed
effect of past or present alterations (Heywood et al. 1994, Tilman et al. 1994, Triantis et al. 2010a),
as in the case of the Azores (Triantis et al. 2010a).

There is ample evidence that Terceira island and the Azorean archipelago in general were
dominated by native forests before the initial contact with the Portuguese settlers (Drummond 1981,
Frutuoso 2005a, b, Connor et al. 2012, 2013). Starting with the clearings for the initial settlements
and their expansion, most of the native forest was destroyed by human action in the last 600 years
(Triantis et al. 2010a, Fernández-Palacios et al. 2011, Silveira, 2013). This was in part due to the
need of arable land and wood for the construction and growth of these initial settlements, but also
caused by the large scale use of the forest as firewood in the first centuries following the settlement,
something that was even noticed by contemporary chroniclers (Frutuoso 2005a, b). An additional
cause were the extensive agricultural production cycles experienced by the economy of the Azores,
which demanded an ever increasing allocation of land and forest destruction (Martins 1993). The
first of this cycles was that of woad (Isatis tinctoria L.) production, that started in the late 15th
century but saw its greatest expansion the 16th century (Frutuoso 2005a, Sequeira 2014), together
with the production of wheat and livestock (Frutuoso 2005a), being followed by other production
cycles, with great impacts in the native vegetation (Martins 1993).

Currently, livestock production is the main economic activity of the Azores (Cruz et al.
2007), having experienced a sharp increase since the eighties, following European Union financing
and incentives towards the growth of livestock and dairy production. This has translated in a great
expansion of the sown pastures and semi-natural pastures, in detriment of other land uses like
agriculture, production forests or native forest and vegetation (Cruz et al. 2007, Gil et al. 2018). In
fact, 89% of the used agricultural area in the Azores is occupied by permanent pastures (Gil et al.
2018).

In terms of land use in Terceira island, 41.5% of the soil is occupied by sown or semi-natural
pastures, 19% by diverse agricultural fields, 14.4% by production forest (mainly Cryptomeria
japonica (L.f.) D. Don or Eucalyptus spp) and 8.8% by urban and industrial areas (Cruz et al. 2007,

98
Borges et al. 2008). Only 14.2% are occupied by native vegetation (Cruz et al. 2007), with the extant
native forests restricted to a few dispersed high-altitude fragments, with areas between 4 and 1300 ha
(Borges et al. 2005, 2006, Gaspar et al. 2008) and still under threat due to habitat reduction,
fragmentation and invasive plant species like Pittosporum undulatum Vent and Hedychium
gardnerianum Sheppard ex Ker Gawl.

These past and present changes left their mark in the indigenous arthropod fauna of Terceira
island, as likely a sizable portion of the island’s fauna suffered from unrecorded extinctions (Cardoso
et al. 2010) and many species are possibly under an extinction debt (sensu Triantis et al. 2010a), and
so, there is some urgency in taking additional measures to protect the indigenous fauna.

Expansion of current protected areas might not be an option, particularly in a small oceanic
island where a large portion or the population is dependent of agriculture (Cruz et al. 2007) and
where land is a limited resource. As such, alternative conservation solutions should be investigated
and implemented, without damaging or antagonizing the local population, and allowing the
coexistence of existing land uses with conservation policies and a sustainable development of the
region.

Island biotas, like that of Terceira, are in general disharmonious, sensitive to habitat
destruction and prone to invasion by exotic species (Sax et al. 2002, Whittaker et al. 2014). These
communities are also characterized by low species richness (Triantis et al. 2012), showing no
saturation of functional trait-space occupancy (Whittaker et al. 2014), which also makes them
vulnerable to exotic species with new sets of functional characteristics. Several studies indicate that
these exotic species prefer the disturbed habitats of Terceira (Borges et al. 2008, Cardoso et al. 2009,
Florencio et al. 2016, Rigal et al. 2018), but nevertheless, these and other studies have also pointed
out that moderately disturbed habitats in Terceira island, like semi-natural pastures or production
forests can act as a refuge for native and endemic arthropod species (Borges & Wunderlich 2008,
Borges et al. 2008, Cardoso et al. 2009, Meijer et al. 2011, Florencio et al. 2016). This confirms, at a
local level, the importance of the quality of the surrounding matrix in the interconnectivity of habitat
patches in fragmented landscapes (Ricketts 2001, Cook et al. 2002, Baum et al. 2004, Debinski
2006).

Isolated trees or even small tree clusters are discrete units (Janzen 1968, Southwood &
Kennedy 1983) separated from source populations (Cook et al. 2002) by a matrix of variable
resistance and able to act like habitat islands. Schonberg et al. (2004) demonstrated that isolated
primary forest trees outside of their original forest matrix can preserve the original associated forest

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arthropod fauna. As such these “living dead” (Janzen 1986) can act as a repository of indigenous
fauna, and in the adequate conditions could even be sources of recolonisation (Schonberg et al.
2004).

I hypothesize that relict trees spread over the landscape, especially on semi-natural pastures
and other low disturbance habitats (many of them remnants from relatively recent deforestation), will
host at least a fraction of the original composition and structure of arthropod communities, while
simultaneously act as corridors, facilitating the interconnection of the extant forest patches of
Terceira.

Besides trying to answer this main question, some additional predictions can also be made:

a) Isolated trees in pastures, due to their architecture and biotic and abiotic conditions of
their canopies, can potentially act as an indigenous species repository, maintaining a community
similar to those of the extant native forests, despite the large scale disturbance suffered during the
clearing of the pasture;

b) High elevation semi-natural pastures, with low grazing pressure and insecticide use (cf.
Borges & Brown 2001) are still host to a high proportion of indigenous species (Borges et al. 2008,
Cardoso et al. 2009), with exotic species favoring more disturbed lowland habitats. Therefore, as
with the case of the forest communities (Chapter 5), recolonisation occurs quickly from the
surrounding species pool, favoring the highly abundant native and endemic species from the nearby
forests and heathland;

c) Even if isolated in a moderately disturbed matrix, the general biotic and abiotic conditions
inside the complex canopies of these high altitude J. brevifolia trees will still favor the native and
endemic species during the recolonisation process after the defaunation event, filtering out the
introduced species;

d) The lack of saturation in functional traits of indigenous species may imply lack of
resilience in the case of disturbance of the natural environment (Whittaker et al. 2014), leaving the
indigenous fauna of these isolated canopies vulnerable to further colonization and probable invasion
of exotic species with new traits during the recolonization process. Therefore, an increase in FD for
the introduced species would be expected in the recolonised trees.

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 6.1. Methods

6.1.1. Study site

Terceira Island, in the Azores Archipelago. The sampling took place in the Terra Brava
Nature Forest Reserve, on the semi-natural pasture described in Chapter 2.

6.1.2. Data collection

Fogging procedures followed the general protocol described in Chapter 2, with some
adaptations derived from the smaller stature, canopy volume, and wind swept nature of the J.
brevifolia specimens present (Fig. 6–1). The softer nature of the terrain also conditioned the protocol.
The soft, even soil allowed the use of steel rebar rods with a wire hook in one end to support the
collection funnels. These rods would be driven into the ground at regular intervals, close to the trunk.
The grommets of the funnels on the side closer to the trunk would be suspended from the wire hooks,
while the other side would be suspended from the branches, as per the standard protocol (see Fig. 6-
1). This allowed for a tighter and more regular placement of the funnels, which, in conjunction with
the smaller canopy area, enabled a higher percentage of coverage compared with the forest trees. In
the case of the tree overhanging the road, metal tent pegs were driven into the barrier, to support one
side of the funnels, while the other side was either supported by the steel rods or suspended from the
branches.

Also, the even ground allowed free movement around the trees during the fogging itself,
ensuring a thorough fogging of the canopies.

Three specimens of J. brevifolia were fogged in this semi-natural pasture, some days after
the completion of the fogging experiment in the forest (Chapters 4 and 5). In 2016, I started by
fogging the trees that had been previously fogged and defaunated in 2015, attempting then to sample
the three new control trees. Unfortunately, as mentioned in Chapter 2, only two of the three proposed
control trees were fogged, as a general deterioration of the weather conditions prevented further
fogging attempts during the season.

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Figure 6-1 Fogging of a J. brevifolia tree in the semi-natural pasture in 2016. Note the small and wind shaped
architecture of the canopy, and the arrangement of the collection funnels. Photo: Alejandra Ros Prieto.

Additionally, and as a way to glimpse what species were present in the vegetation of the
semi-natural pasture, and could potentially colonise the defaunated trees, three sweeping transects
were made on both years (2015 and 2016). A collapsible sweep net was used to collect the arthropods
from the vegetation. The specimens were then captured from the net with a pooter. The collection
vial of the pooter was a falcon tube, that at the end of the transect would be detached, filled with 96%
ethanol, labeled and sealed. Sweeping samples were stored in these tubes until sorting and
identification. Each transect was performed in different parts of the pasture and performed in an
“itinerant” way, following the contour of the terrain and trying to pass through different types of
vegetation, if some was conspicuous. Stops were done at intervals to collect the arthropods from the
net and to remove vegetation debris. Total effective sweeping time was of approximately five
minutes per transect.

6.1.3. Arthropod dataset

All the arthropods collected by pyrethrum knockdown in conjunction with branch beating
(as described in chapter 2) on 5 specimens of Azoren cedar (Juniperus brevifolia) growing in a semi-
natural pasture. As described above three specimens were fogged for the first time in 2015 and then
refogged in 2016, with the two remaining specimens being fogged for the first time in 2016 (see

102
Chapter 2 for further details). The arthropods collected by the sweeping protocol described in the
above section were also used for some basic comparisons.

Additionally, the arthropod samples from the three J. brevifolia trees in the forest that were
fogged for the first time in 2015 were also used, for some simple comparisons with those from the
pasture.

6.1.4. Data analysis

As with the previous chapters, all statistical analyses were implemented in R version 3.3.3
(R Core Team, 2017), with some basic calculations and graphics being performed using the
LibreOffice spreadsheet (The Document Foundation).

The data analysis followed the same procedures described in the previous chapter.

In the first section of this chapter I analyze the differences between three specimens of J.
brevifolia fogged in the semi-natural pasture in 2015 with those of the three control J. brevifolia
fogged in the native forest in the same year (cf. Chapters 4 and 5).

Basic metrics for both communities were calculated after Chapters 3 and 4. Also, as with the
previous chapters, the package gambin (Matthews et al. 2014) was used to assess the distribution of
the relative species abundances (SADs) for the arthropod community between the forest and semi-
natural pasture J. brevifolia trees, while Beta diversity calculations were performed using the R
package BAT (Cardoso et al. 2015), and total differentiation divided into its species replacement
(βrepl) and species richness differences (βrich) components (Carvalho et al. 2012).

For the second section, concerning the defaunation and recolonisation of J. brevifolia trees in
the semi-natural pasture, the parameters described above were also analyzed for the communities
present in the pasture trees, regarding the differences between years and fogging episodes (if it was
the first or the second time that a given tree was fogged).

The BAT package was used to calculate both Taxonomic Diversity (TD) and Functional
Diversity (FD) for the conjunction of year and fogging episode

As with the previous chapter, FD was calculated based on a functional tree based on a traits
matrix for the species present in the pasture trees, that consisted of the same categorical and
continuous morphological trait variables of ecological significance used in Chapter 5. Kruskal-Wallis
rank sum test was performed to identify potential differences between factors (year and fogging
episode), both in terms of taxonomic and functional diversities, using the rarefied datasets.

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 If differences were present, a Wilcoxon signed rank test was performed on pairs of factors, to
ascertain which were different. As they represent only two data points, the control trees were not
considered in these statistics, but were still graphically represented, as a visual aid.

This was done for the entire community, but also for subsets according to: a) colonisation
status (endemic, native and introduced), b) predators and non predators, c) with the exclusion of
singletons and doubletons, and d) with the exclusion of rare species (with less than five individuals).
In the case of the introduced species, due to the very low abundance present in the canopies of the
individual trees, rarefaction was not applied to this dataset, as this would entail a great loss in
information.

Once more, to evaluate if in any factor, or group of factors, in the community was a subset
with higher or lower taxonomic and/or functional diversity that what would be expected by chance, a
null model was created following the method described in the previous chapter (Chapter 5).

The same procedure was used to evaluate functional diversity, using the previously created
functional tree for the species present in the pasture trees.

Besides pooling the entire community, species were also pooled using other criteria and the
corresponding null assemblages created, repeating the procedure and analyses described. In the case
of the control trees, the same applies as described, being graphically represented as a visual aid.

For part of the analysis, an introduced species Ectopsocus briggsi McLachland (Insecta,
Psocoptera) that attained high abundance in 2016 was excluded from the calculations, as its presence
in the samples from 2016 was most likely due to some intrinsic or temporal process, independent
from the fogging experiment. This will be further expanded in the discussion.

6.2. Results

In this section I will first present the results from the comparison between the three J.
brefivolia trees from the forest that were fogged for the first time in 2015 as a control, and the three
semi-natural pasture specimens that were fogged also for the first time also in 2015. The second part
will consist of the study of the recolonisation processes in the J. brevifolia trees isolated in the semi-
natural pasture, akin to the recolonisation study presented in the previous chapter.

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 6.2.1. Forest vs. Pasture cedar trees
A total of 1795 specimens from 35 species were collected in the canopies of the forest
cedars. These belonged to 20 families and 10 orders. Araneae was the most diverse and abundant
order. Comparatively, a total of 2767 arthropod specimens, belonging to 38 species, 30 families and
11 orders were collected in the canopies of the pasture cedars. In similarity with the forest trees,
Araneae was the most species rich and abundant order in isolated pasture cedars.

For the herbaceous pasture vegetation, 48 specimens from 18 species, 13 families and 6
orders were collected. Most of the species were spiders, followed by Hemiptera. Of the six endemic
species present in the herbaceous pasture vegetation, five were common canopy species, being also
collected in the cedars, while the sixth was the Azorean endemic wolf spider (Pardosa acorensis
Simon). Native and introduced species were also represented by six species each in the vegetation,
but of these, only two native [Hoplothrips corticis (De Geer) and Macaroeris cata] and one
introduced (Tenuiphantes tenuis Wunderlich) species were found in both the pasture canopies and
herbaceous pasture vegetation. Diversity and abundance information regarding the specimens
collected in the canopies of the pasture and forest cedars, along with information for the specimens
collected in the herbaceous pasture vegetation is summarized in Table 6–1.

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Table 6-1Summary table with the arthropod species richness (S), abundance (N), number of singletons and doubletons,
number of trees and of samples, average number of species per tree, number of species and specimens per square meter,
for the J. brevifolia trees sampled for the first time in 2015, both for the forest and semi-natural pasture, together with
some information regarding the arthropods collected on the herbaceous vegetation of the semi-natural pasture (Pasture
Fog/Year J. brevifolia Forest 2015 J. brevifolia Pasture 2015 Pasture

Trees 3 3 -

Samples 14 15 3

S 35 38 18

N 1795 2767 48

Singletons 9 9 8

Doubletons 1 4 5

Average species per tree 26.3±4.0 24±2.7 -

Species per m2 16.3±4.8 14.9±2.7 -

Specimens per m2 128.2±65.0 184.5±77.7 -

In both habitats the number of species was similar, as was the number of singletons, but
considerably more arthropod specimens were collected in the canopies of the pasture trees.
Accordingly, the average number of species per trees and per square meter were rather close in both
habitats, but the semi-natural pasture trees were host to higher arthropod densities (specimens per
m2) (Table 6–1) but none were statistically distinct (Species density: Kruskal-Wallis chi-squared =
0.932, df = 1, p = 0.334; Specimen density: Kruskal-Wallis chi-squared = 3.281, df = 1, p = 0.070).

Forest and semi-natural pasture trees had similar proportions of endemic and native species,
with endemics accounting in both cases for 50% of the species present, but the proportion of
introduced species was slightly higher in the pasture trees (Fig. 6–2). In the herbaceous vegetation,
each colonisation status accounted for roughly one third of the species. There were no statistically
significant differences between the trees on both habitats in terms of species richness (Kruskal-Wallis
chi-squared = 0.048, df = 1, p = 0.827).

In terms of relative abundance (Fig. 6–2), the proportion of introduced specimens was quite
low in the tree canopies of both habitats, even if slightly lower in the pasture trees. Endemic

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specimens composed the majority of the arthropods collected in the forest trees, with 80% of the
specimens, while in the pasture trees the endemics had a decrease in the relative abundance regarding
the natives, with each accounting for roughly 50% and 40% of the specimens, respectively. In the
herbaceous vegetation specimens of introduced species accounted for some 22% of the population,
while natives and endemic accounted each for some 40%. In terms of abundance by colonisation
status, no statistically significant differences were also observed between the trees on both habitats
(Kruskal-Wallis chi-squared = 0.0.48, df = 1, p = 0.827).

Figure 6-2 Relative species richness and abundance of endemic (E), native (N) and introduced (I) arthropods for the J.
brevifolia trees fogged for the first time in the forest and in the semi-natural pasture in 2015, and for the herbaceous
vegetation of the pasture. Jun_For – J. brevifolia trees in the forest; Jun_Past – J. brevifolia trees in the pasture; Pasture –
herbaceous vegetation.

Concerning the trophic status (Fig. 6–3), forest trees had a higher percentage of herbivorous
species than the pasture trees, but these were still lower that the proportion of predators. Pasture trees
also showed a higher proportion of saprophytes that the forest ones. Predator species dominated in
the herbaceous vegetation, accounting for 70% of the species present, while saprophytes were totally
absent. Differences between trees in both habitats were not statistically significant (Kruskal-Wallis
chi-squared = 0.021, df = 1, p = 0.885).

In terms of relative abundances (Fig. 6–3), predators accounted for most of the individuals
present in the trees of both habitats, but in the pasture trees 30% of the specimens present were
saprophytes. In both instances, less than 16% of the specimens collected were herbivores. There were
no significant differences between trees in both habitats (Kruskal-Wallis chi-squared = 0.75, df = 1, p
= 0.383). In the herbaceous vegetation, 80% of the specimens present were predators.

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Figure 6-3. Relative species richness and abundance of fungivore (F), herbivore (H), predator (P) and saprophyte (S)
arthropods for the J. brevifolia trees fogged for the first time in the forest and in the semi-natural pasture in 2015, and for
the herbaceous vegetation of the pasture. Jun_For – J. brevifolia trees in the forest; Jun_Past – J. brevifolia trees in the
pasture; Pasture – herbaceous vegetation.

Looking at the species abundance distribution (SAD) for both the forest and the pasture
canopy communities (Fig. 6–4), some differences were apparent. The forest community seemed to
follow a multimodal distribution, with many rare species, but also with several intermediately
abundant and abundant species, while the pasture canopy community had only two modal classes,
with several rare species and some intermediately abundant and few abundant species, with the shape
of the SAD approaching a logseries.

Regarding colonisation status (Fig. 6–4), in the forest was noticeable that most of the
abundant species were endemic, while in the pasture there was some parity between endemic and
native species. It was also conspicuous the low number of introduced species present in both
communities.

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Figure 6-4 Modified Preston's octaves histograms for the for the community present in the J. brevifolia trees fogged for
the first time in the forest and in the semi-natural pasture in 2015, discerning between the endemic (green), native (blue)
and introduced (red) species components. The graphs are scaled equally for the Y axis.

Comparing rank abundances (Table 6–2), Elipsocus brincki and Lathys dentichelis, two
native species also present in the forest in lower numbers, were the dominant species in the pasture
canopies, while the three most abundant species in the forest conserved their relative positions with
each other in the pasture trees, despite the overall loss of rank.

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Table 6-2 Rank abundance of the five most abundant species in the forest and in the semi-natural pasture trees fogged for
the first time in 2015, ordered by abundance values for the initial community the forest J. brevifolia trees. E – Endemic;
N – Native
Species J. brevifolia Forest 2015 J. brevifolia Pasture 2015

Savigniorrhipis acoreensis (E) 1 3

Cinara juniperi (N) 2 4

Acorigone acoreensis (E) 3 5

Trigoniophthalmus borgesi (E) 4 11

Zetha vestita (N) 5 8

Elipsocus brincki (E) 8 1

Lathys dentichelis (N) 10 2

Considering now the β diversity of both canopy communities (Table 6–3), it was possible to
observe that species turnover was the main cause of dissimilarities between the forest and semi-
natural pasture trees, either when considering the entire community or only the endemic species,
although total dissimilarity values were lower between the habitats in the case of the endemics. For
the native species, both species turnover and differences in species richness were equally important
in explaining the dissimilarities between the communities, as was also the case of the introduced
species, where the high total dissimilarity between the forest and pasture trees also seemed to be
equally caused by species turnover and by differences in the number of species present (Table 6–3).

Table 6-3 Rarefied values of Total β diversity, β Replacement and β Richness between the forest and semi-natural pasture
J. brevifolia trees sampled for the first time in 2015. Results are presented for the entire community, and for endemic,
native and introduced species. J_For – J. brevifolia trees in the forest; J_Past – J. brevifolia trees in the pasture
All Endemic Native Introduced

β-total J_For β-total J_For β-total J_For β-total J_For

J_Past 0.42 J_Past 0.29 2015_1t 0.53 J_Past 0.67

β-Repl J_For β-Repl J_For β-Repl J_For β-Repl J_For

J_Past 0.37 J_Past 0.20 J_Past 0.24 J_Past 0.33

β-Rich J_For β-Rich J_For β-Rich J_For β-Rich J_For

J_Past 0.02 J_Past 0.05 J_Past 0.29 J_Past 0.33

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 6.2.2. Recolonization in pasture cedars
A total of 8056 specimens were collected by fogging in the canopies of J. brevifolia in semi-
natural pasture during the two years of the experiment. These specimens belonged to 38 species, 44
families and 13 orders (Acari, Collembola, Hymenoptera and Diptera are not factored in these
numbers). Araneae, Psocoptera and Hemiptera were the most abundant orders, with Araneae being
also the most species rich, being followed by Coleoptera and Hemiptera. The native spider Lathys
dentichelis was the single most abundant species, with 2376 specimens collected, or 29% of the
collected arthropods. This was followed by the introduced Psocoptera Ectopsocus briggsi, but this
seems to be a particular case, that will be discussed further on.

For the species present in the semi-natural pasture, a total of 91 specimens, belonging to 20
species, 13 families and six orders were collected by sweeping. Araneae, followed by Hemiptera
were simultaneously the most abundant and species rich orders. Of these 20 species, six were
endemic, seven native and the remaining seven, introduced. All the endemic species present in the
sweeping samples were also present in the trees, while only the same two native and one introduced
species reported in the previous section were also found in both habitats. All endemic species were
forest canopy species, with the exception of the Azorean endemic wolf spider Pardosa acorensis, a
ground dwelling species.

Table 6–4 summarizes the diversity and abundance information regarding the specimens
collected in the canopies, per year and fogging episode, along with some other relevant information.

Table 6-4. Summary table with the arthropod species richness (S), abundance (N), number of singletons and doubletons,
number of trees and of samples, average number of species per tree, number of species and specimens per square meter,
for the total extent of the fogging experiment, and for each year and fogging episode combination. Values in parenthesis
refer to these same metrics without the introduced Psocoptera Ectopsocus briggsi. 2015_1t – trees fogged in 2015;
2016_1t – control trees fogged for the first time in 2016; 2016_2t – trees initially fogged in 2015 and fogged for a second
time in 2016.
Fog/Year 2015_1t 2016_1t 2016_2t Total
Trees 3 2 3 8
Samples 15 9 14 38
S 38 (37) 29 (28) 43 (42) 58(57)
N 2767 (2758) 2952 (1823) 2337 (2046) 8056 (6627)
Singletons 9 7 16
Doubletons 4 3 4
Average species per tree 24±2.7 21±4.2 25.33±3.8 -
Species per m2 14.9±2.7 (14.5±2.5) 12.8±3.1 (11.8±3.1) 15±2.9 (14.2±2.8) -
Specimens per m2 184.5±77.7 (183.8±77.7) 338±164.5 (202.6±76.2) 166.3±97.7 (146.1±72.9) -

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 The most striking result was the very high density of specimens in the control trees. This was
caused by only one species, the introduced Psocoptera Ectopsocus briggsi. If this species was
removed from the calculations, the density of specimens in these trees dropped considerably, being
also accompanied by a less conspicuous decrease in density on the recolonised trees while being
negligible in the initial 2015 community (Table 6-4).

Considering the initial 2015 community and the recolonised one, it is conspicuous that
despite having fairly similar numbers of species, almost half of the species that appeared in the
recolonised community were singletons or doubletons. Accordingly, arthropod densities were lower
in the recolonised community than in the control trees or in the initial community, while species
density was higher in the recolonised community. However, none of these apparent differences were
statistically significant (Species per tree: Species density: Kruskal-Wallis chi-squared = 2.249, df = 2,
p = 0.325; Kruskal-Wallis chi-squared = 4.7862, df = 2, p = 0.091; Specimen density: Kruskal-Wallis
chi-squared = 3.35, df = 2, p = 0.187).

Regarding the colonisation status, endemic species accounted for 50% the species present in
the trees in 2015, while only 15% of the species were introduced. In the control community from
2016, 30% of the species were introduced and endemic species still accounted for roughly another
45%. In the case of the recolonised community, endemic, native and introduced species accounted
each for roughly one third of the species present (Fig. 5). This differences were, nevertheless, not
statistically significant (Kruskal-Wallis chi2 = 1.882, df = 2, p = 0.39).

Considering the abundance data, the impact caused by the presence of Ectopsocus briggsi is
quite apparent when comparing the relative abundances of introduced species for both communities
of 2016, with and without this species (Fig. 6–5). In the control trees almost 40% of the collected
specimens were introduced, while in the recolonised trees these accounted for 13% of the specimens.
E. briggsi is excluded (Fig. 6–5), introduced species represented less than 1% of the collected
specimens in the recolonised community, as was the case for the initial community of 2015, with
only 17 specimens collected. The proportion was similar for the control trees.

In 2015 the large majority of collected specimens were endemics, accounting for roughly
60% of all collected specimens, in 2016 (with E. briggsi removed) they represented only 30% and
36% of the specimens collected in the control trees and in the recolonised trees, respectively, these
proportions being lower if this species was maintained in the samples. Accordingly, natives had a
considerable increase in relative abundance, accounting for 63% of the specimens in the recolonised
community (Fig. 6–5, bottom chart). However, there were no statistically significant differences

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between the communities (with E.briggsi; Kruskal-Wallis chi2 = 0.089, df = 2, p = 0.957; without
E.briggsi: Kruskal-Wallis chi2 = 0.157, df = 2, p = 0.925).

Figure 6-5 Proportion of endemic (E), native (N) and introduced (I) arthropods for each year and fogging episode
combination. Results are presented in terms of relative species richness (a) and relative abundance (b) for the entire
dataset, and of relative species richness (c) and relative abundance (d) without the introduced species Ectopsocus briggsi.
2015_1t – trees fogged in 2015; 2016_1t – control trees fogged for the first time in 2016; 2016_2t – trees initially fogged
in 2015 and fogged for a second time in 2016

When considering the trophic status, both the initial 2015 community and the recolonised
trees had similar proportions of species richness in the distinct trophic groups, while the control trees
had, in comparison, a higher proportion of herbivore species and lower of saprophytes (Fig. 6–6).
Once more, the relative abundance of Ectopsocus briggsi, a saprophyte, in 2016 was quite
noticeable, particularly in the control trees (2016_1t). Saprophythes accounted for 20% of the
specimens in the recolonised community, but if E. briggsi was removed, this proportion was halved.
The proportion of herbivores was fairly constant along the years and fogging episodes. (Fig. 6). Also
noticeable was the extremely high proportion of predators, particularly in 2016. However, there were
no significant differences for both species richness (Kruskal-Wallis chi2 = 0.119, df = 2, p = 0.942),
or abundance (with E. briggsi; Kruskal-Wallis chi2 = 0.038, df = 2, p = 0.981; without E.briggsi;
Kruskal-Wallis chi2 = 0.5, df = 2, p = 0.779).

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Figure 6-6 Proportion of fungivore (F), herbivore (H), predator (P), ants (P/H) and saprophyte (S) arthropods, for each
year and fogging episode combination. Results are presented in terms of relative species richness (a) and relative
abundance (b) for the entire dataset, and of relative species richness (c) and relative abundance (d) without the introduced
species Ectopsocus briggsi. 2015_1t – trees fogged in 2015; 2016_1t – control trees fogged for the first time in 2016;
2016_2t – trees initially fogged in 2015 and fogged for a second time in 2016.

Observing now the species abundance distribution (SAD) for the whole canopy arthropod
community collected in 2015, for the community of the control trees and for the community that
recolonised the defaunated trees (2016_2t) (Fig. 6–7), two kinds of distribution were apparent: the
trees fogged for the first time in 2015 (2015_1t) seemed to have two modes, one of rare species and
another one of intermediate abundant species; the other two communities had an unimodal
distribution, with several rare species and few intermediately abundant and abundant ones. However,
there was an apparent increase in rare species in the recolonised trees fogged for the second time in
2016 (2016_2t).

If the colonisation status is also taken into consideration (Fig. 6–7), with the exception of the
introduced E. briggsi in 2016, basically all intermediately abundant and abundant species were either
native or endemic. It was also clear that the spike in singletons in the recolonised community was
mainly due to specimens from introduced species.

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Figure 6-7 Modified Preston's octaves histograms for the for the community present in the trees fogged for the first time
in 2015 (2015_1t), for that of the control trees fogged for the first time in 2016 (2016_1t) and for the community present
in the recolonised trees fogged for the second time in 2016 (2016_2t), discerning between the endemic (green), native
(blue) and introduced (red) species components. A red star indicates the psocoptera Ectopsocus briggsi. The graphs for
the initial community and for the control trees are scaled equally for the Y axis.

Ranking the species by abundance, it can be seen that the most abundant species in 2015,
Elipsocus brincki, disappeared completely in 2016, being replaced by the introduced E. briggsi
(Table 6–5). The native spider Lathys dentichelis was the second most abundant species in 2015 and
in the control trees, while being the most abundant in the recolonised community. The remaining
three species conserved their rank- abundances without fluctuations, in both years and all fogging
episodes.

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Table 6-5 Rank abundance of the five most abundant species, ordered by abundance values for the initial community of
2015. 2015_1t – trees fogged in 2015; 2016_1t – control trees fogged for the first time in 2016; 2016_2t – trees initially
fogged in 2015 and fogged for a second time in 2016. E – Endemic; N – Native, I – Introduced.
Species 2015_1t 2016_1t 2016_2t

Elipsocus brincki (E) 1 - -

Lathys dentichelis (N) 2 2 1

Savigniorrhipis acoreensis (E) 3 3 3

Cinara juniperi (N) 4 4 4

Acorigone acoreensis (E) 5 5 5

Ectopsocus briggsi (I) 18 1 2

Regarding β diversity and the partition into its components of β Replacement and β
Richness, it was possible to observe that species turnover was the main cause of dissimilarities
between the initial community and both communities from 2016. However, differences in the total
number of species present was as important as species turnover in the dissimilarities between the
community of the control trees and that of the recolonised trees (Table 6–6).

Table 6-6 Rarefied values of Total β diversity, β Replacement and β Richness between the different years and fogging
episodes, for the entire community, for endemic, for native and for introduced species (with E. briggsi removed). 2015_1t
– trees fogged in 2015; 2016_1t – control trees fogged for the first time in 2016; 2016_2t – trees initially fogged in 2015
and fogged for a second time in 2016.
All Endemic Native Introduced

β-total 2015_1t 2016_1t β-total 2015_1t 2016_1t β-total 2015_1t 2016_1t β-total 2015_1t 2016_1t

2016_1t 0.55 - 2016_1t 0.50 - 2016_1t 0.50 - 2016_1t 0.78 -

2016_2t 0.48 0.53 2016_2t 0.37 0.35 2016_2t 0.39 0.50 2016_2t 0.77 0.75

β-Repl 2015_1t 2016_1t β-Repl 2015_1t 2016_1t β-Repl 2015_1t 2016_1t β-Repl 2015_1t 2016_1t

2016_1t 0.42 - 2016_1t 0.35 - 2016_1t 0.00 - 2016_1t 0.44 -

2016_2t 0.35 0.26 2016_2t 0.32 0.25 2016_2t 0.35 0.00 2016_2t 0.15 0.40

β-Rich 2015_1t 2016_1t β-Rich 2015_1t 2016_1t β-Rich 2015_1t 2016_1t β-Rich 2015_1t 2016_1t

2016_1t 0.12 - 2016_1t 0.11 - 2016_1t 0.50 - 2016_1t 0.33 -

2016_2t 0.14 0.26 2016_2t 0.06 0.06 2016_2t 0.06 0.50 2016_2t 0.62 0.33

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 Considering now the different colonisation status, for endemic species dissimilarities
between the communities were rather evident for the initial community and that of the control trees,
the remaining differences being less severe. In all cases, species turnover seemed to be the main
cause (Table 6–6). Dissimilarities between the communities were also evident in the case of the
native species and while species turnover was the main cause for the dissimilarity between the initial
and the control communities, dissimilarities between the initial and the recolonised community, and
between both communities from 2016 seemed to be caused by differences in species richness. For
the introduced species, β-diversity was very high between all three communities. In the case of the
comparison between initial and recolonized trees these dissimilarities were mainly explained by
differences in the number of species, for the other cases, besides species turnover, differences in the
total number of species present were also an important factor (Table 6–6).

Looking now at the relation between Taxonomic and Functional diversity (Fig. 6–8), it is
possible to observe that for the entire community and for its subsets (and for both the full set of data
and for the rarefied data), the FD increased proportionally with the increase in TD, showing no signs
of saturation.

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Figure 6-8 Relationship between taxonomic richness (TD) and functional richness (FD) for the entire community and for
several subsets. For each subset, the graphic on the left (black dots) uses the real values for each subset, and the one on
the right (blue dots), the rarefied values of TD and TD. td – taxonomic diversity; tdr – rarefied taxonomic diversity; fd –
functional diversity; fdr - rarefied functional diversity. Summary of regression results in Appendix IV.

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 There were no statistically significant differences between the arthropod communities of the
different years and fogging episodes in terms of taxonomic or functional diversities, but some
general trends could be observed in the data when comparing the initial 2015 community (2015_1t)
with that from the recolonised trees of 2016 (2016_2t) (Fig. 6–9). As a whole, the community on the
recolonised trees showed an increase in taxonomic diversity that was not proportional to the large
increase in functional diversity. In the distinct subsets of the community, endemic species were the
only ones that registered a decrease for both TD and FD in the recolonised community, while for
natives the increase in TD and FD in the recolonised community was less conspicuous. On the other
hand, introduced species showed a sharp increase in both TD and FD in the recolonised community.
When removing singletons, doubletons or locally rare species, functional diversity increased in the
recolonised community, despite a decrease in taxonomic diversity for the case of the removal of rare
species. Both predators alone or non-predator species showed an increase in FD in the recolonised
community that was not proportional to the smaller increase in TD.

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Figure 6-9 Rarefied taxonomic diversity (TDr) and functional diversity (FDr) values for the distinct fogging episodes.
Values are calculated for the entire community and for its several subsets. For each subset, the graphic on the left refers
to the TDr, and the one on the right (colored green) to the FDr, except for introduced species, where TD and FD are used
instead. An asterisk in the header of the subset denotes the removal of the introduced Ectopsocus briggsi. 2015_1t – trees
fogged in 2015; 2016_1t – control trees fogged for the first time in 2016; 2016_2t – trees initially fogged in 2015 and
fogged for a second time in 2016.

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 Considering now the extent to which the communities studied would differ from a randomly
assembled community (a “null community”), it would appear that with a few exceptions when
considering their subsets, both the initial community and that of the recolonised trees are not
statistically different from communities assembled at random (Fig. 6–10). One of the exceptions
were the endemic species, which in the recolonised communities presented both TD and FD values
that were significantly lower than those expected in a randomly assembled community (TD endemic:
T-test p = 0.035; FD endemic: T-test p = 0.018). While for 2015 only the community without the
locally rare species showed a significant difference in TD from what would be expected at random
(TD no rares: T-test p = 0.013); the community without singletons and doubletons also showed
differences from a null community that were close to significance (T-test p = 0.056) in that year.
Differences in TD from a null community were also close to significance in the initial community for
the subset without locally rare species (T-test p = 0.051) in 2015. Introduced species in the
recolonised community were statistically indistinguishable from a community formed at random,
particularly in terms of TD (T-test p = 1).

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Figure 6-10 Comparison between the TD and FD of the sampled communities and that of a null community. Values are
calculated for the entire community and for its several subsets. For each subset, the graphic on the left refers to the TD,
and the one on the right (colored green) to the FD. An asterisk in the header of the subset denotes the removal of the
introduced Ectopsocus briggsi. 2015_1t – trees fogged in 2015; 2016_1t – control trees fogged for the first time in 2016;
2016_2t – trees initially fogged in 2015 and fogged for a second time in 2016.

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 6.3. Discussion

6.3.1. Forest vs. Pasture cedar trees

Considering first the communities present in the J. brevifolia trees from the semi-natural
pasture and from the forest, it was possible to see that general community metrics were rather similar
in terms of total number of species, species density or numbers of singletons or rare species for both
communities. On the other hand, the number of collected specimens was considerably higher in the
semi-natural pasture trees, meaning a considerable (if not significant) increase in arthropod density in
the canopies of these trees.

The proportions of endemic, native and introduced species were similar in both
communities, but some dissimilarities occurred between them. In the case of the endemic species,
these dissimilarities were relatively low, and species turnover seems to be the main cause of it.
Moreover, looking at the SAD of both communities some distinctions are apparent, as the forest
community had a higher number of abundant species and these are mainly endemic, while in the
pasture trees there were less abundant species present, and many of the abundant species present
were natives. Conversely, a considerable portion of the singletons in the forest were natives, while in
the pasture trees they were endemic. This might indicate that, at least for some endemic species,
these isolated trees might act as sinks.

Interestingly enough, the three most abundant species in the forest cedars, despite being
supplanted in rank by Elipsocus brincki and Lathys dentichelis in the semi-natural pasture canopies,
retained their relative ranks, which might indicate some structure in the assembly of Azorean canopy
arthropod communities in J. brevifolia. It should also be noted that three out of the five most
abundant species found in the pasture canopies can be considered J. brevifolia specialists (S.
acoreensis, C. juniperi and E. brincki) (Chapter 4).

Additionally, both canopy arthropod communities show considerable constancy regarding

the proportions of the trophic groups present, despite being in distinct habitats, reinforcing also some
possible influence of the intrinsic tree characteristics in the formation of these communities (Mody et
al 2003). Both communities were also dominated by predators, which was not totally unexpected for
J. brevifolia trees (Borges et al. 2008, Nunes et al. 2015, cf. Chapters 3, 4 and 5).

Contrary to what would be expected (Cook et al. 2002), overlap between the communities of
the semi-natural pasture matrix and that of the canopies of the trees in the pasture matrix was very
low, as only one out of the six introduced species present in the herbaceous vegetation was also

123
present in the canopies, and only two out of the six native species present in the herbaceous
vegetation were also present in the canopies. One of these species, the salticid Macaroeris cata is
also common in the native forests (Chapter 4, Nunes et al. 2015). The case of the endemic species is
also curious, as five out of the six species present in the herbaceous vegetation were also present in
the canopies, but all of them are also common forest species (Appendix I), having most likely
dispersed from the trees or from the nearby endemic vegetation.

These results seem to confirm my first prediction that isolated native trees maintain
communities similar to the original forest communities and can act as repositories of indigenous
species (Janzen 1986, Schonberg et al. 2004), despite the drastic changes in the surrounding matrix
generated by the clearing of the native vegetation to create the current pasture.

As already mentioned, a possibility for these similarities between the communities of the
forest and pasture trees, might be the architecture of the trees themselves and in conditions in their
canopies, as this seems to be an important factor in structuring the communities, including the
presence of epiphyte mats, a characteristic of the native Azorean forests (Gabriel & Bates 2005) that
has been considered important for several groups in other parts of the world (Yanoviak et al. 2003)
and that was also present in the sampled trees in the pasture.

Regarding the endemic and native forest arthropod species present in the herbaceous
vegetation of the pasture, it is likely that, as mentioned above, these are specimens that dispersed
from the nearby Erica azorica heathland, an important host plant species in the Azores (Ribeiro et al.
2005), from the surrounding patches of native forest, or even from the canopies of the isolated J.
brevifolia trees, as it seems that these isolated native trees still maintain arthropod communities that
are at least partly similar to those from the forest, potentially acting as repositories of indigenous
species. This would confirm the importance of high quality semi-natural pastures in the Azores as
refuge (Borges & Wunderlich 2008, Borges et al. 2008, Cardoso et al. 2009, Meijer et al. 2011,
Florencio et al. 2016), but also, in conjunction with the isolated trees, as corridors and stepping-
stones (Gilpin 1980, Simberloff et al. 1992, Tewksbury et al. 2002, Schonberg et al. 2004) between
the patches of native forest, thus answering my main question.

Also, for less mobile species like the endemic Trigoniophthalmus borgesi, it would also be
interesting to ascertain if the specimens found on the tree canopies were individuals that were able to
disperse from the nearby native vegetation, or if they are relics (Janzen 1986, Schonberg 2004),
descendants of specimens that were in the trees or rock outcrops when the forest was cleared and
transformed into a semi-natural pasture in the eighties.

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 6.3.2. Canopy arthropod recolonization in isolated pasture trees
I should start this section by justifying my decision regarding the the removal of one species
from most of the analysis. I removed the introduced psocopteran Ectopsocus briggsi from most of
my analysis because I am convinced that the observed pattern was not caused by the fogging
experiment, but most likely it was due to some intrinsic mechanism/behavior or to some external
factor that caused this great fluctuation between years. In 2015 there were six psocopteran species
present in my samples, all native and endemic, except for nine specimens of E. briggsi. In the
following year E. briggsi was present in high abundance, with only one more species present, in very
low numbers. If this was a consequence of an open niche space created by the fogging, it would be
expected that the highest densities would be found in the previously defaunated trees, but the
opposite was found, in fact, only one of these previously defaunated trees had a relatively high
abundance of this species, and still lower than that of the control trees. These groups are
understudied in the archipelago, with many knowledge gaps existing regarding their biology and
ecology (P. Borges, personal communication). Therefore, I maintain my conviction that what was
observed was part of some unknown cyclic process with a peak of density in 2016. Therefore, this
species will not be considered in the following discussion.

Several differences can be observed between the initial community, that of the control trees
and the community from the recolonised trees. There were more species present in the recolonised
community than the initial one, but almost half were present as singletons and doubletons. The
recolonised trees also had fewer specimens present that in 2015, which also translates into a lower
arthropod density. On the other hand, the average number of species per tree and per square meter
were not as different between the initial and recolonised communities. This higher number of species
and singletons present, with similar values of species density (species per sampling unit) might
indicate the presence of some turnover between the individual trees.

The relative proportions of endemic, natives and introduced species also changed in the
recolonised community, with the three colonisation classes having now roughly the same number of
species present. This increase in the number of introduced species was not followed by any
noticeable increase in the abundance of these species. On the other hand, abundances of endemic
species were depressed in the recolonised community, while native species seem to have fared better
in the new community. This shift in the abundances of natives and endemics was in part due to an
increase in the abundance of one native spider species (Lathys dentichelis), although the rank
abundance results (Table 6–5) show a great degree of orthodoxy between the communities. Lathys
dentichelis seems to operate as an opportunist species.

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 Binning the population into octaves gave a clearer picture of the changes that occurred in the
structure of the community after the recolonization. The SAD of the new community has a clear
unimodal distribution, with an increase in the number of rare species (as mentioned above) and slight
reduction in the number of intermediately abundant and abundant species in relation to the initial
community. The spike in rare species is even more conspicuous as it was mainly caused by a large
influx of introduced species. This is also reflected in the very high dissimilarity between introduced
species for both communities in terms of beta diversity. Contrary to the recolonisation data from the
forest (Chapter 5), in the pasture most of this dissimilarity was explained by differences in the
number of species present and not by species turnover. Back to the SAD (Fig. 6–7) it can also be
seen that whereas the initial community had a higher component of endemics as abundant species, in
the recolonised community there seems to occur more parity between native and endemic species.
The community of the control trees seems to be somewhat intermediate between the other two.

Recolonisation by the indigenous species seems to have been slower than in the forest, as the
community has not fully recovered. Unlike the forest, these trees are not part of an interconnected
unit (Erwin 1990), and consequently, the arrival to the empty niches created by defaunation will
occur by dispersal and by continued or periodic immigration from the nearby matrix of natural
vegetation (Cardoso et al. 2009), and probably more importantly in this particular case, of heathland
(Ribeiro et al. 2005). This pattern partially negates my second prediction, that the community would
recover quickly. In fact, with the exception of endemic species that seem to have recolonised the
trees in a more deterministic way, the whole community and its remaining subsets appear to have
recolonised the tree in a way not distinguishable from a random assemblage, giving support to the
hypothesis of a colonization by dispersal and periodic immigration. Nevertheless, even if at a slower
pace, recolonisation still seems to favor the very abundant indigenous species from the nearby forests
and heathland, while recolonization by introduced species occurred by random dispersal processes,
with the more disturbed anthropogenic habitats (Cardoso et al. 2009, Meijer et al. 2011, Florencio et
al. 2016) acting as a likely source, even if some specimens might have dispersed from the nearby
trees or heathland.

Another factor that might influence the way that the trees are recolonised by a majority of
endemic and native arthropod species would be the presence of plant volatiles acting as attractants
(Metcalf 1987, Takabayashi & Dicke 1996). This effect would be of higher importance for the
recolonisation of the isolated pastures trees, than for the forest trees, as in this last case, the high
level of canopy interconnectedness (see Chapter 5) would overshadow the effect of the attractants.
Hypothetical co-evolutionary plant-insect processes (Cornell & Hawkins 2003) would also help

126
accounting for the high proportion of indigenous species in the recolonised isolated trees. This was
however outside of the scope of my work, and the sampling protocol does not allow the test of this
additional possibility. Nevertheless, this question should also be addressed in a future work.

As seen in the previous chapter, introduced species have some difficulty in establishing
themselves in the canopy habitat of the native forests (Gaspar et al. 2008, Nunes et al. 2015,
Florencio et al. 2016, Borges et al. 2017). The same still seems to be true for the pasture trees,
although it would also seem that in these trees, resilience by the indigenous canopy arthropod
communities towards disturbances and invasions was somewhat depressed and a relatively large
number of introduced species was collected in the canopies. Nevertheless, the still relatively low
number of specimens from introduced species found in the recolonised trees, despite the slower
recovery by the indigenous species, might indicate that introduced arthropods still suffer some sort of
filtering effect by the architecture of the tree canopies (Southwood & Kennedy 1983, Mody et al.
2003), confirming my third prediction.

Still regarding the influence in the arthropod communities of the architecture of the trees and
of the biotic and abiotic conditions in the canopies (as already discussed above for the pasture trees
in 2015), the few species that were present in both the canopies and the herbaceous vegetation of the
pasture were mainly endemic species, also present in the native forest canopies, which leads to
deduct that even with new potential niches opened by the fogging, the species from the lower strata
do not take opportunity from these niches.

In addition, overall dissimilarities between the initial community and the recolonised one
were lower than between the initial community and the control trees, or between the control trees and
the recolonised community, which might hint at some effect of the characteristics of individual trees
(Mody et al. 2003), or also to temporal patterns in the structuring of the community (Azarbayjani et
al. 1999).

Regarding the relation between taxonomic and functional richness, as seen in the forest
communities (Chapter 5), and at a regional scale by Whittaker et al. (2014) for the islands of the
Azorean archipelago, the samples from the semi-natural pasture trees show that there is a strong
positive relation between TD and FD. Consequently, FD shows no evidence of saturation increasing
linearly with TD. This indicates that even in these isolated trees, the canopy fauna present seems to
remain relatively unsaturated in terms of functional trait space. The current results seem to imply
that, contrary to the situation in the native forest (Chapter 5) this lack of trait saturation seems to

127
cause a certain degree of vulnerability to invasion by introduced species with distinct functional
traits, taking advantage of the generated disturbances and vacating of niches created by the fogging.
Even so, the community appears to maintain some degree of resistance to invasion.

Moreover, the defaunation and the input of new introduced species in the community had a
generally positive effect in the functional diversity of the community, adding new, distinct traits,
something also observed by Rigal et al. (2018) and at a regional scale by Whittaker et al. (2014).
Only endemic species suffered a decrease in both taxonomic and functional diversity with the
recolonisation, possibly due to the loss of some locally rare or less mobile species,

These results seem to validate my fourth prediction, that FD would increase in the
recolonised community, particularly for the introduced species.

Importantly, one must not forget that these disturbances occurred in trees that were located in
a high quality, altitude semi-natural pasture, surrounded by a relatively undisturbed matrix of mostly
native vegetation, conditions favorable to a high proportion of indigenous species (Borges et al.
2008, Cardoso et al. 2009). However, the comparatively high number of introduced species found in
the recolonised community leads one to conjecture that if these trees would have been closer to more
heavily anthropic habitats, it is possible that an even higher proportion of introduced would have
been collected in the recolonised community.

Future studies including other isolated indigenous trees, in more disturbed habitats
(agricultural and urbanized), would help understand better their hypothetical role as relics, with
mostly self-sustaining populations, or if most of the species present in the trees sampled in my study
were the result of dispersal and constant immigration from the forest and heathland matrix, the trees
acting mostly as stepping-stones.

128
Chapter 7
General conclusions
From the present analysis of preexisting data pertaining to the canopy arthropods of the
Azores and of Terceira island in particular, as well as from previous results it is possible to assume
that despite the high proportion of introduced species in the Azores archipelago, the remnants of the
native forests, and more specifically its canopies, still maintain a high proportion of what would be
the original Azorean arthropod fauna. This pattern seems to be a characteristic of the native Azorean
canopies in general, but more markedly so on those of J. brevifolia. As such, it can be said that the
canopies in the extant patches of native forest act as a small window to what was the original pristine
Azorean arthropod fauna, at least above the 500 m altitude.

The fogging experiment allowed for a new approach to the study of the canopy arthropods in
Terceira island, and the advantages of this technique are apparent when considering the number of
species and of specimens collected in a relatively small number of trees inside a native forest
fragment, particularly when compared with previous island-wide studies.

From the fogging experiment, it was possible to see that the arthropod communities of the
native forest canopies seem to be relatively homogeneous, dominated by a few very abundant
endemic generalist species, with several intermediately abundant native and endemic species and
many rare species, a structure akin to that of temperate forests elsewhere (Basset 1991). Also, the
relatively low taxonomic diversity and overall abundance when compared with temperate forest
communities might be a consequence of not only biogeographical constraints, but also of the last 600
years of anthropic disturbance, that saw the destruction of more than 90% of the original habitats.

Contrary to what was previously observed for the archipelago and for Terceira, it would
seem that in my plot the individual host tree species would be of secondary importance in structuring
the communities, given the similarities between the communities of the three distinct tree species,
probably due to the generalist status of most of the collected species.

Another, possible explanation would be that the complex architecture of the canopies, its
closed nature and high degree of interdigitation might be responsible for a certain homogenization of
the arthropod community, as it turns the canopies into something akin to a single continuous habitat
inside the forest fragment (Erwin 1990), and given the dominance of J. brevifolia in my plot, the
communities present in each tree will most likely be a reflection of the communities usually present

129
in J. brevifolia, with its high spider load and high proportion of endemic species. This would also
account for other patterns like the high density of predators, mainly spiders, found in my samples.

One point that should also be stressed is the extremely low abundance of introduced species,
despite their relative species richness, and the abundance of endemics which seems to indicate that
despite being somewhat impoverished, the canopy arthropod communities of Terceira retain a high
degree of resilience towards disturbance and invasions.

Regarding the recolonisation processes of the canopy arthropods, the very dense nature of
the native Azorean forests, as well as the high amount of interdigitation between neighboring trees
has to be taken into consideration as a major factor when considering the structure of the canopy
arthropod communities, or the recovery of these communities after a severe disturbance like a
defaunation event, as this most likely turns the canopies into something akin to a single continuous
habitat, not unlike the “horizontal highways” alluded by Erwin (1990).

As previously said, the arthropod communities of native forest canopies are dominated by
some very abundant, generalist, endemic species and, to a certain extent, also by native species.
Thus, it would be safe to suppose that recolonisation and recovery processes would also follow
somewhat deterministic patterns, being driven by intrinsic characteristics of the Azorean forest
canopies, and to a certain degree by the particular characteristics of the individual trees (Mody et al.
2003), as well as by the structure of the source community. Rare species will most likely recolonise
the defaunated trees in a more random way, driven by stochastic dispersion processes. The same
should be the case of the introduced species that, with the exception of some intermediately abundant
species, most likely dispersed at random from within the forest patch, but most importantly from the
surrounding mosaic of production forests, pastures and other anthropogenic habitats, that act as a
source for dispersal for the introduced species that thrive in these. The fact that species turnover for
introduced species was higher between years that between the recolonised and control trees also
supports this assumption.

The native forest, or at least its canopies, seem to maintain a high degree of resilience
towards disturbance and invasion, even if the lack of functional traits would lead to suppose
otherwise. This might be a direct consequence of filtering by the particular biotic and abiotic
conditions present in the canopies.

Regarding the communities of the isolated azorean cedars in a semi-natural pasture, two
main conclusions would be that the structural and biotic and abiotic characteristics of the Azorean
cedar canopies, and even the characteristics of the individual trees (Mody et al. 2003) seem to play

130
an important role in the structuring of the arthropod canopy; the other is that, given the importance of
corridors and stepping-stones in increasing the connectivity of fragmented populations (Gilpin 1980,
Simberloff et al. 1992, Tewksbury et al. 2002), particularly in a low-resistance matrix (Ricketts
2001, Cook et al. 2002, Baum et al. 2004, Debinski 2006), this study stresses the role of the semi-
natural pastures of the Azores as a low-resistance matrix for endemic and native species (Borges et
al. 2008, Cardoso et al. 2009), which also enhances the role of isolated native trees as repositories of
indigenous fauna and as stepping-stones between the extant patches of native vegetation (see also
Florencio et al. 2016).

Nevertheless, the fogging experiment also revealed that the arthropod communities of these
isolated pasture trees are more vulnerable to disturbances and to invasion by exotic species.

I hope that the present study, despite its flaws, will help in increasing our current knowledge
regarding the indigenous arthropod communities of the Azores and consequently assist in the present
and future conservation measures, as well in the sustainable development of the region.

Equally, I also hope that this work will spur new studies in the Azores, or even in the other
islands of Macaronesia, taking advantage of the singular characteristics of the fogging technique to
produce a new body of comparable information regarding the canopy arthropod communities of
these islands and further increase our general understanding about the world around us.

131
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 Appendix I
List of arthropod species collected by canopy fogging in the native forest in the years of 2014 and
2015.

The classification system follows the general guidelines presented in Borges et al. (2010), with the higher taxa listed in a phylogenetic
sequence, from the less derived to more derived groups. The families, genera and species are listed by alphabetical order. Exceptions to this are
the Arachnidae, who follow the classification of the “World Spider Catalogue” by Platnick (2014); Coleoptera, that follow Bouchard et al.
(2011) and Lepidoptera, that follow Aguiar & Karsholt (2006). The genera and species are nevertheless also listed by alphabetical order.

The colonisation status of each species is presented in the 6th column of the list as follows: E – endemic; N – native; I – introduced. The trophic status is given the 7th
column as follows: P – predator; H – herbivore; S – saprophyte; F – fungivore. Collumns 8, 9 and 10 give the total number of speciemens collected for each tree species.
Total Colonisation Trophic
Order Family Species Ilex Juniperus Laurus
Abundance Status Status
Pseudoscorpiones
Chthoniidae Chthonius ischnocheles (Hermann) 7 I P - 7 -
Chthonius tetrachelatus (Preyssler) 1 I P - - 1
Neobisiidae Neobisium maroccanum Beier 9 I P 1 7 1
Opiliones Phalangiidae Leiobunum blackwalli Meade 62 N P 41 14 7
Araneae Dysderidae Dysdera crocata C. L. Koch 1 I P 1 - -
Mimetidae Ero furcata (Villers) 164 I P 59 83 22
Theridiidae Lasaeola oceanica Simon 10 E P 2 6 2
Rugathodes acoreensis Wunderlich 2043 E P 1034 830 179
Linyphiidae Acorigone acoreensis (Wunderlich) 2110 E P 1077 775 258
Canariphantes acoreensis (Wunderlich) 1 E P - 1 -
Erigone atra Blackwall 2 I P 1 1 -
Erigone autumnalis Emerton 3 I P 3 - -
Erigone dentipalpis (Wider) 5 I P 1 2 2
Microlinyphia johnsoni (Blackwall) 3 N P 1 2 -
Minicia floresensis Wunderlich 2 E P 1 1 -
Savigniorrhipis acoreensis Wunderlich 6218 E P 2227 3581 410

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(cont.)
Total Colonisation Trophic
Order Family Species Ilex Juniperus Laurus
Abundance Status Status
Araneae Linyphiidae Tenuiphantes miguelensis Wunderlich 4 N P 1 3 -
Tenuiphantes tenuis (Blackwall) 2 I P - 2 -
Walckenaeria grandis (Wunderlich) 3 E P 1 1 1
TetragnathidaeSancus acoreensis (Wunderlich) 640 E P 342 187 111
Araneidae Gibbaranea occidentalis Wunderlich 780 E P 379 287 114
Pisauridae Pisaura acoreensis Wunderlich 10 E P 5 5 -
Dictynidae Emblyna acoreensis Wunderlich 1 E P 1 - -
Lathys dentichelis (Simon) 1929 N P 736 1111 82
Clubionidae Cheiracanthium erraticum (Walckenaer) 10 I P 9 1 -
Clubiona decora Blackwall 7 N P 5 1 1
Thomisidae Xysticus cor Canestrini 9 N P 1 8 -
Salticidae Macaroeris cata (Blackwall) 118 N P 76 26 16
Diplopoda ChordeumatidaHaplobainosomatidae
Haplobainosoma lusitanum Verhoeff 27 I S 7 9 11
Diplopoda Julida Julidae Ommatoiulus moreletii (Lucas) 2 I H - 2 -
Chilopoda LithobiomorphaLithobiidae Lithobius pilicornis pilicornis Newport 14 N P 9 2 3
Insecta MicrocoryphiaMachilidae Trigoniophthalmus borgesi Mendes et al. 1192 E S 517 454 221
Blattodea Polyphagidae Zetha vestita (Brullé) 404 N S 242 135 27
Psocoptera Caeciliusidae Valenzuela flavidus (Stephens) 54 N S 42 3 9
Ectopsocidae Ectopsocus briggsi McLachlan 41 I S 31 4 6
Elipsocidae Elipsocus azoricus Meinander 7 E S 2 5 -
Elipsocus brincki Badonnel 1937 E S 300 1581 56
Epipsocidae Bertkauia lucifuga (Rambur) 2 N S - 2 -
TrichopsocidaeTrichopsocus clarus (Banks) 142 N S 97 20 25
Hemiptera Aleyroridae Gen. sp.1 19 E H 11 2 6
Aphididae Rhopalosiphum oxyacanthae (Schrank) 1 I H - 1 -
Cixiidae Cixius azoterceirae Remane & Asche 48 E H 22 16 10
Flatidae Cyphopterum adcendens (Herr.-Schaff.) 21 N H 7 11 3
Lachnidae Cinara juniperi (De Geer) 705 N H 143 551 11

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(cont.)
Total Colonisation Trophic
Class Order Family Species Ilex Juniperus Laurus
Abundance Status Status
Insecta Hemiptera Lygaeidae Beosus maritimus (Scopoli) 1 N H - - 1
Kleidocerys ericae (Horváth) 8 N H 3 4 1
Scolopostethus decoratus (Hahn) 1 N H - 1 -
Miridae Campyloneura virgula (Herrich-Schaeffer) 3 N P 1 1 1
Pinalitus oromii J. Ribes 257 E H 64 170 23
Nabidae Nabis pseudoferus ibericus Remane 1 N P 1 1 1
Psyllidae Strophingia harteni Hodkinson 5 E H 1 3 1
Tingidae Acalypta parvula (Fallén) 1 N H 1 - -
Triozidae Trioza (Lauritrioza) laurisilvae Hodkinson 148 N H 91 17 40
Thysanoptera PhlaeothripidaeHoplothrips corticis (De Geer) 8 N F 3 2 3
Neuroptera Hemerobiidae Hemerobius azoricus Tjeder 53 E P 24 20 9
Coleoptera Hydrophilidae Cercyon haemorrhoidalis (Fabricius) I S - 1 -
Staphylinidae Aleochara bipustulata (Linnaeus) 5 I P 3 2 -
Atheta aeneicollis (Sharp) 1 I P - 1 -
Atheta dryochares Israelson 949 E P 396 480 73
Tachyporus chrysomelinus (Linnaeus) 2 I P 2 - -
Xantholinus longiventris Heer 5 I P 4 1 -
Phalacridae Gen. sp.2 1 I? S - 1 -
Stilbus testaceus (Panzer) 1 N S 1 - -
ChrysomelidaeGen. sp.1 1 I? H - 1 -
Curculionidae Calacalles subcarinatus (Israelson) 338 E H 298 16 24
Drouetius borgesi borgesi Machado 2 E H 2 - -
Pseudophloeophagus tenax (Wollaston) 97 N H 2 93 2
Lepidoptera YponomeutidaeArgyresthia atlanticella Rebel 138 E H 65 68 5
Tortricidae Gen. sp.2 95 I H 36 47 12
Rhopobota naevana (Hübner) 90 I H 54 22 14
Crambidae Scoparia coecimaculalis Warren ? 9 E H 2 7 -
Geometridae Ascotis fortunata azorica Pinker 6 E H 3 3 -
Cyclophora azorensis (Prout) 158 E H 33 104 21
Nycterosea obstipata (Fabricius) 2 N H 1 1 -
Xanthorhoe inaequata (Warren) 118 E H 53 59 6
Totals 21274 8579 10866 1832

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 Appendix II
IndVal summary table from BALA
Summary table of IndVal results from the BALA database for Terceira island, with Indicator
species and corresponding host tree, indicator value, statistical significance of the associations and
the frequency. E - Endemic; N - Native; I - Introduced.

Indicator Species Host tree IndVal p-value Frequency

Rhopobota naevana (I) I. perado 0.53379536 0.001 15
Cixius azoterceirae (E) I. perado 0.39202023 0.001 9
Gibbaranea occidentalis (E) I. perado 0.24773077 0.007 1
Calacalles subcarinatus (E) I. perado 0.18901334 0.001 32
Macaroeris cata (N) I. perado 0.17841679 0.001 213
Cheiracanthium erraticum (I) I. perado 0.14294590 0.006 2
Anaspis proteus (N) I. perado 0.03130830 0.045 3
Eudonia luteusalis (E) I. perado 0.03024223 0.025 26
Savigniorrhipis acoreensis (E) J. brevifolia 0.62313572 0.001 298
Lathys dentichelis (N) J. brevifolia 0.58322549 0.001 10
Cinara juniperi (N) J. brevifolia 0.57219247 0.001 65
Argyresthia atlanticella (E) J. brevifolia 0.54746555 0.001 8
Rugathodes acoreensis (E) J. brevifolia 0.31546411 0.001 75
Zetha vestita (N) J. brevifolia 0.29540323 0.001 1
Pinalitus oromii (E) J. brevifolia 0.23930696 0.001 393
Sancus acoreensis (E) J. brevifolia 0.18243736 0.026 225
Elipsocus brincki (E) J. brevifolia 0.16318864 0.001 2
Xysticus cor (N) J. brevifolia 0.15816223 0.001 5
Tortricidae Gen. sp.3 (I) J. brevifolia 0.12185457 0.001 78
Tortricidae Gen. sp.6 (I) J. brevifolia 0.06675720 0.001 1
Trigoniophthalmus borgesi (E) J. brevifolia 0.05597994 0.014 55
Margarodidae Gen. sp.2 (N) J. brevifolia 0.04117647 0.001 1
Oedothorax fuscus (I) J. brevifolia 0.04033486 0.012 2
Dilta saxicola (N) J. brevifolia 0.03685287 0.013 1
Tortricidae Gen. sp.7 (I) J. brevifolia 0.03534059 0.006 4
Lasaeola oceanica (E) J. brevifolia 0.03090104 0.035 1
Erigone atra (I) J. brevifolia 0.02819726 0.009 33
Psocoptera Gen. sp.5 (N) J. brevifolia 0.02647059 0.017 1
Pardosa acorensis (E) J. brevifolia 0.01599204 0.044 6

156
Trioza laurisilvae (N) L. azorica 0.51307241 0.001 1
Cyclophora azorensis (E) L. azorica 0.15688248 0.006 32
Strophingia harteni (E) L. azorica 0.09783340 0.001 1
Nycterosea obstipata (N) L. azorica 0.08744996 0.001 1
Valenzuela flavidus (N) L. azorica 0.08371533 0.001 24
Kleidocerys ericae (N) L. azorica 0.07148200 0.001 53
Clubiona decora (N) L. azorica 0.05702788 0.001 3
Trichopsocus clarus (N) L. azorica 0.05212182 0.005 7
Heterotoma planicornis (N) L. azorica 0.02222222 0.003 1
Atlantopsocus adustus (N) L. azorica 0.01481481 0.030 1

157
 Appendix III

Summary table of the regression results for the relation between TD and FD without
rarefaction and with rarefaction (TDr and Fdr), for the entire forest canopy community and for its
several subsets.

Subset Relation R2 Adjusted R2 df F-statistic p - value

All TD/FD 0.775 0.769 37 127.5 << 0.05
TDr / Fdr 0.866 0.862 37 238.9 << 0.05
Indigenous TD/FD 0.676 0.667 37 77.1 << 0.05
TDr / Fdr 0.843 0.834 37 198.1 << 0.05
Endemic TD/FD 0.774 0.768 37 126.6 << 0.05
TDr / Fdr 0.820 0.815 37 168.7 << 0.05
Native TD/FD 0.812 0.807 37 159.9 << 0.05
TDr / Fdr 0.914 0.912 37 393.1 << 0.05
Introduced TD/FD 0.776 0.770 37 128.1 << 0.05
TDr / Fdr 0.734 0.727 37 102.1 << 0.05
Arareae TD/FD 0.655 0.645 37 70.1 << 0.05
TDr / Fdr 0.592 0.581 37 53.8 << 0.05
no SgDb TD/FD 0.764 0.758 37 119.9 << 0.05
TDr / Fdr 0.854 0.850 37 216.1 << 0.05
No Rares TD/FD 0.775 0.769 37 127.3 << 0.05
TDr / Fdr 0.833 0.828 37 183.9 << 0.05
Adults TD/FD 0.809 0.804 37 156.6 << 0.05
TDr / Fdr 0.847 0.843 37 205 << 0.05
Juveniles TD/FD 0.707 0.697 37 89.1 << 0.05
TDr / Fdr 0.798 0.793 37 146.2 << 0.05
Predators TD/FD 0.705 0.697 37 88.42 << 0.05
TDr / Fdr 0.865 0.862 37 238.5 << 0.05
Non Predators TD/FD 0.642 0.632 37 66.2 << 0.05
TDr / Fdr 0.749 0.742 37 110.2 << 0.05

158
 Appendix IV

Summary table of the regression results for the relation between TD and FD without
rarefaction and with rarefaction (TDr and Fdr), for the entire community present in the canopy of the
azorean cedar trees isolaten in a semi-natural pasture, and for its several subsets.

Subset Relation R2 Adjusted R2 df F-statistic p - value

All TD/FD 0.675 0.621 6 12.5 0.012
TDr / Fdr 0.781 0.745 6 21.5 0.004
Endemic TD/FD 0.721 0.674 6 15.5 0.008
TDr / Fdr 0.853 0.828 6 34.7 0.001
Native TD/FD 0.901 0.885 6 54.6 << 0.05
TDr / Fdr 0.862 0.839 6 37.4 << 0.05
Introduced TD/FD 0.900 0.883 6 53.8 << 0.05
TDr / Fdr - - - - -
no SgDb TD/FD 0.599 0.532 6 8.9 0.024
TDr / Fdr 0.669 0.614 6 12.2 0.013
No Rares TD/FD 0.900 0.883 6 53.8 << 0.05
TDr / Fdr 0.934 0.923 6 84.4 << 0.05
Predators TD/FD 0.798 0.64 6 23.7 0.003
TDr / Fdr 0.729 0.684 6 16.1 0.007
Non Predators TD/FD 0.256 0.132 6 2.1 0.201
TDr / Fdr 0.647 0.589 6 11.2 0.016

159
UNIVERSIDADE DOS AÇORES
Faculdade de Ciências e Tecnologia

Rua da Mãe de Deus

9500-321 Ponta Delgada
Açores, Portugal
 Whole Azorean arthropod diversity

2017
[TD]
diversity
Rui Miguel Ricardo Nunes