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Diversity of canopy spiders in north-temperate hardwood forests

Maxim Larrivee

Department of Natural Resource Sciences

McGill University

Montreal, Quebec, Canada

April 2009

A thesis submitted to the Faculty of Graduate Studies and Research in

partial fulfillment of the requirements for the degree of Doctor of Philosophy

© M. Larrivee

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1+1 Canada Abstract

The objective of this thesis was to understand the spatial patterns and processes responsible for canopy and understorey spider (Arachnida: Araneae) diversity at multiple spatial scales in north-temperate hardwood forests. I sampled tree trunks (sticky traps) and foliage (beating) of sugar maple and American beech tree canopies and their understorey saplings in old growth forests near Montreal, Quebec. Results show the composition of canopy and understorey assemblages differed significantly, and so did sugar maple and American beech canopy assemblages. Each stratum was also dominated by different species. The rank-abundance distribution of species from each habitat wsa also verticaly stratified because it fit different distribution models. Different factors likely structure assemblages in both habitats, particularly since the canopy is a less stable environment. Spiders from canopy and understorey foliage were tested in a laboratory for their propensity to balloon. General linear models indicated that small sized web-building spiders of the RTA and Orbicularia clades have the highest propensity to balloon. Small bodied species initiated ballooning regardless of the habitat they were collected in or their developmental stage. My results support the mixed evolutionary stable strategy theory and indicate the absence of risk-spreading in the dispersal strategy of canopy spiders. My last chapter focused on dispersal capacity and diversity patterns of spiders at multiple spatial scales. Analyses of the species diversity of limited and high dispersal capacity species subsets through nested-multivariate ANOVA, additive diversity partitioning, and species-abundance distribution curves all point towards species-sorting processes as the main driver of local community spider diversity at the tree and stand spatial scales. Mass- effects and patch-dynamic processes drive site and regional scale diversity patterns. This

I thesis demonstrates that spiders provide good models to test many biological hypotheses.

The research chapters of this thesis test hypotheses on the vertical stratification of forest spider diversity, the evolution of local dispersal adaptations, and the importance of dispersal capacity on species diversity patterns through a metacommunity framework.

II Resume

L'objectif de cette these etait de comprendre les patrons spatiaux de diversite des araignees (Arachnida: Araneae) et les processus les creant a echelles spatiales multiples en forets decidues temperees nordiques. J'ai echantillonne les troncs d'arbres (pieges collants) et le feuillage (battage) dans la canopee d'erable a sucre et d'hetre a grandes feuilles ainsi que dans la haute regeneration de chaque espece dans des forets surannees dans la region de Montreal, Quebec. Les resultats indiquent que la composition des assemblages de la canopee et de la strate arbustive different significativement de meme que ceux des canopees d'erable a sucre et de hetre a grandes feuilles. Des especes differentes sont significativement plus abondantes dans chaque strate d'elevation. La distribution de rangs d'abondance des especes indique que des mecanismes differents regissent la structure des assemblages de chaque habitat. La propension au ballonnement des araignees du feuillage de la canopee et de la haute regeneration a ensuite ete testee en laboratoire. Des modeles lineaires generaux indiquent que les petites araignees tisseuses de toile des clades RTA et Orbicularia ont une forte propension au ballonnement et que cette derniere est peu affectee par la stabilite de l'habitat. Les araignees de petite taille ballonnent peu importe leur niveau de developpement. Mes resultats supportent la theorie de la strategic evolutive mixte stable et l'absence d'une repartition du risque dans la strategie de dispersion des araignees de la canopee. Mon dernier chapitre traite de

P influence de la capacite de dispersion sur les patrons de diversite des araignees a echelles spatiales multiples. Des analyses multi variees et nidifiees de sous-ensembles d'especes d'araignees a capacite de dispersion reduite ou forte indiquent que des processus de tri des especes produisent les patrons de diversite des araignees aux echelles

III spatiales de l'arbre et du peuplement alors que des processus d'effets de masse et des dynamiques de peuplement regissent les patrons de diversite aux echelles du site et de la region. Cette these demontre que les araignees sont excellentes pour tester plusieurs hypotheses ecologiques liees a la distribution de la diversite verticale et horizontale, et ce sur plusieurs echelles spatiales.

IV Contribution of authors

This thesis consists of 3 original papers co-authored by my supervisor, Dr. Christopher

Buddie. Chapter 3 of this thesis is accepted for publication in the journal Agricultural and

Forest Entomology. I intend to submit Chapter 4 to the journal Ecological Entomology as an original paper, and the original paper version of Chapter 5 is in preparation for the

Journal of Animal Ecology. For each of the papers presented within, I planned the experimental designs with valuable input from my supervisor and my committee members Drs. A.Gonzalez and T. Wheeler. I was responsible for fieldwork, identification, and I performed all analyses presented with feedback from my supervisor and committee members. I wrote the first drafts of all manuscripts. Final drafts contained useful comments and at times direct contributions of my supervisor. All others who contributed to the production of these papers through field or laboratory work, or through an input of ideas or financial support are acknowledged within each original paper.

V Contributions to knowledge

Chapter 3:

This original paper characterized and compared foliage spider diversity in the canopy and

understorey of sugar maple and American beech in old-growth north-temperate hardwood

forests. Several aspects of this original paper are novel contributions to canopy ecology and spider ecology: 1) Use of an aerial platform allowed a regional scale canopy

arthropod diversity study with many replicates using a direct sampling technique; 2) the results demonstrated differences between canopy and understorey spider diversity and the complementary nature of the fauna in these two habitats; 3) results also showed that spider assemblage composition differs between sugar maple and American beech canopies, and that different processes drive spatial patterns of diversity in the canopy and the understorey. This original paper should inspire further canopy athropod studies in temperate forests because of the possibilities offered by this new canopy access method and the demonstration that the canopy spider fauna is relevant to the biological diversity of north-temperate hardwood forests.

Chapter 4

This original paper is the first investigation of the ballooning propensity of spider species across many families in a forest and in the canopy. The adaptive links among ballooning propensity, life history traits and habitat conditions make ballooning an important research area. The knowledge gained in this study can be applied to other areas of ecology like understanding the processes that account for spatial patterns of diversity. My

VI results showed that the propensity to balloon is similar among spiders in the canopy and the understorey habitat. The highest propensity to balloon in a forested habitat belonged to small-bodied web-building spiders from the RTA and Orbicularia clades. The dispersal strategy of canopy spiders does not seem to be based on risk-spreading but instead maintenance of cursorial and aerial dispersal (in similar proportions) in canopy and understorey spider populations suggest mixed evolutionarily stable strategies. The results presented in this paper on the influence of body size and feeding strategy on ballooning propensity in a forest habitat have implications in the fields of spider and evolutionnary ecology.

Chapter 5

This original paper demonstrated that ecologists can test ecological hypotheses about regional diversity patterns and processes with work in temperate forest canopies. The use of a mobile aerial platform allowed replication of a hierarchical sampling design nested in space and this is new to canopy ecology. The originality of this paper resides in its hierarchical design of four nested spatial scales and its use of subset of species that vary in dispersal capacity to investigate spider diversity patterns and to test hypotheses about metacommunities. It also provided the first combined assessment of canopy foliage and trunk spider diversity in north-temperate hardwood forests. The results showed species- sorting processes such as niche and resource availability influence north-temperate hardwood forest spider diversity more than dispersal capacity at small spatial scales (tree and stand scales). Species diversity at the site and regional spatial scales was mainly

VII ^^ influenced by mass-effects and patch-dynamic processes with dispersal capacity and

habitat availability significantly influencing spider diversity patterns.

#>

VIII Acknowledgements

I am most grateful to my wife Michelle for her love, patience, never ending support and motivation. I love you. Also, over the last two and half years, thank you to my daughter

Xoe for making us realize what life is all about; simple pleasures and unconditional love.

This thesis would have never been possible without my thesis director's belief and faith in my ability to manage such an ambitious project, thank you Chris. Thank you also Chris for all the latitude and support you gave me to develop my project, and your guidance as well. Chris, I learned a lot from your passion for life, your ability to separate work from friendship in due times, and also from your parenting advices! To my parents, thank you for your emotional support and all your encouragements. To Joey Bowden, Briana

Schroeder, Zach Sylvain, Annie Hibbert, Kathleen Aikens, Katleen Robert, Kristen

Brochu, and Jean-Francois Aublet; thank you so much for the countless hours and dedicated help you provided me during my field work, you guys were more than I could have ever asked for. You allowed me to abide by my moto: "sample the heck out of everything; once you're done you can't go back". Carol Frost, thank you so much for your help with my spider hotel. Thank you to all the other members of the Buddie lab:

Alida Mercado, Michel Saint-Germain, Tara Sackett, Annie Webb, Hirondelle Varady-

Szabo, Elise Bolduc, Andrea Dechene, Tonia Motchula, and Charles Stephen, for your valuable input during our Thursday meetings, your patience around all my stuff in the lab, and most importantly for making me feel part of the lab even with my diminished physical presence over the last two years. A special thank you to my great friends Joey

Bowden and Michel Saint-Germain for their stimulating discussions about science and their camaraderie in and outside the lab. Also, thank you to my best friend Frederic

IX Lavoie for providing me everything I needed every time I stayed in Montreal. You are truly my brother from another mother. I am very grateful to the Canadian National

Collection of Insects, Arachnids and Nematodes (CNC), and to Dr. Peter Mason who provided me access to the collection, an office, and everything I needed to be productive.

I also thank le Centre d'Etude de la Foret for their support and particularly Marc

Mazerolle for all his help. To my great friend Dr. Charles Dondale, my mentor in spider taxonomy, thank you for all your help (and chocolate) throughout the years. I also thank everyone else at the CNC for their support and help. Thank you also, to the conservation officers from Oka provincial Park, to Donald Rodrigue and his staff from Mont Saint-

Bruno provincial Park, Benoit Hamel from the Mont Saint-Hilaire Gault Nature Reserve, and to Christina Idziak curator of the Morgan Arboretum. Finally, thank you to my advisory committee members Drs. Andy Gonzalez and Terry Wheeler for your valuable comments, they greatly improved my project. Finally, I thank the following funding agencies for making my thesis a reality: Le Fonds Quebecois de la Recherche sur la

Nature et les Technologies (doctoral research scholarship); the Natural Sciences and

Engineering Research Council of Canada, the Canada Foundation for Innovation, and the department of Natural Resource Sciences at McGill University all provided various types of financial support to my project.

X Table of contents

Abstract I Resume Ill Contribution of authors V Contributions to knowledge VI Acknowledgements IX Table of contents XI 1. Introduction 1 1.1 Summary of objectives 5 2. Literature review 9 2.1 Temperate canopy spider ecology 9 2.2 Spider dispersal 13 2.3 Diversity patterns in space 17 2.4 Metacommunity ecology 23 Original papers 28 3. Diversity of canopy and understorey spiders in north-temperate hardwood forests 29 3.1 Preface .30 3.2 Abstract 31 3.3 Introduction 32 3.4 Material and methods 34 3.5 Results 40 3.6 Discussion 43 3.7 Acknowledgements , 50 3.8 Literature cited 51 3.9 Tables 58 3.10 List of figures captions 62 3.11 Appendices 66 3.12 Connecting statement.. 69 4. Ballooning propensity of canopy and understorey spiders in a north-temperate hardwood forest 70 4.1 Preface 71 4.2 Abstract 72 4.3 Introduction 74 4.4 Materials and methods 77 4.5 Results 82 4.6 Discussion 84 4.7 Acknowledgements 89 4.8 Literature cited.... 91 4.9 Tables 95 4.10 List of figure captions 102 4.11 Connecting statement 105 5. Multiple spatial scale metacommunity dynamics of north-temperate hardwood forest spiders 106 5.1 Preface 107

XI 5.2 Abstract 108 5.3 Introduction 109 5.4 Materials and methods 114 5.5 Results 120 5.6 Discussion 122 5.7 Acknowledgements 129 5.8 Literature cited 130 5.9 Tables 136 5.10 List of figure captions 142 6. Summary 146 6.1 Synthesis 147 6.2 Conclusions and Suggested Future Directions 151 7. Literature cited 154 8. Appendices 164 8.1 Species collected on foliage and trunk of sugar maple and American beech canopy and understorey 164 8.2 List of generalized linear dispersal models (Chapter 4) 167

XII 1. Introduction

Canopy ecology is a relatively recent field. Interest in the fauna of tree crowns, its diversity and the ecological processes that drive it spiked after a seminal paper in which

Erwin (1982) estimated the diversity of arthropod life on earth to 30 million species. He went on to say that forest canopies represent the "Last Biotic Frontier" (Erwin 1983). In little time studies of canopy arthropods entered the ecological mainstream with the advent of new access methods (e.g., single rope climbing, cranes) and sampling techniques (e.g., fogging) (Moran and Southwood 1982; Kennedy and Southwood 1984; Stork 1987).

Standardized samples and increased replication provided by these new access and sampling techniques provided more thorough inventories of canopy diversity. Canopy studies involving solid tests of ecological hypotheses quickly followed (Ozanne etal.

2000; Basset et al. 2003).

Over the last 30 years, temperate canopy ecology has brought to light many ecological patterns. Arthropod species diversity varies significantly among tree species in temperate forest canopies (Moran and Southwood 1982), and between the understorey and the crown of mature trees in a forest (Turnbull 1960; Preisser et al. 1999; Vance et al. 2003;

2007; Ulyshen and Hanula 2007). The diversity of arthropods is generally higher in the understorey than in tree crowns of temperate forests, but this pattern can be reversed in particular insect families (Schowalter and Zhang 2005; Ulyshen and Hanula 2007). These differences are attributed to contrasting abiotic conditions in both habitats; temperature, humidity, wind, and light conditions fluctuate more and are harsher in the canopy

1 (Bohlman et al. 1995; Fagan et al. 2006; Lowman & Wittman 1996; Basset et al. 2003).

Strong seasonality and loss of leaves in the tree crowns reduce the quality of overwintering habitats available. Hence, there are probably limited possibilities for particular species to complete their full life cycle in the canopy and thus become specialized to temperate canopy habitats.

Arboreal spiders have been investigated in North American temperate forests, although many studies have focused on branches lower in the canopy or those accessible from the ground. Halaj et al. (1998; 2000) showed that arboreal spider richness was positively correlated with habitat structure and prey density. Other studies showed that arboreal diversity of spiders in coniferous trees did not differ between tree species (Stratton et al.

1979; Jennings and Collins 1986; Jennings and Dimond 1988). With two exceptions

(Mason 1992; Halaj et al. 1996), most of these studies were conducted at small spatial scales and did not compare canopy and understorey diversity. There are few comparative studies of canopy and understorey diversity and none have been conducted in mature north-temperate hardwood forests. Also, no study has attempted to define the contribution of tree canopies to diversity in mature temperate hardwood forests across multiple spatial scales within a region. More realistic estimates of species diversity in these forests depend on the inclusion of canopy-based studies.

In this thesis, I set out to identify the major patterns and processes governing the diversity of canopy and understorey spiders of sugar maple {Acer saccharum Marsh.) and

American beech (Fagus grandifolia Ehrh.) trees across multiple spatial scales in north-

2 temperate hardwood forests of southern Quebec, Canada. I chose sugar maple and

American beech as the focal tree species of the study because they are the most abundant species in these forests. The saplings of both species also dominate the understorey typical to sugar maple forests. Focus on abundant forest trees accessible with an aerial lift platform maximized the replication possible in the study. The aerial lift platform (the

DINO 260xt, distributed by Specialty Equipment®, USA) has a maximum elevation of 26 meters and can be towed from site to site with a 4WD vehicle. It rotates completely on itself thus can sample with a 360 degree radius. In towing position, the DINO is only 2 m wide, 7 m long and 3 m high. Use of this aerial platform is the corner stone of my sampling design and provides unprecedented rapid and direct access to the canopies of dominant temperate hardwood trees on well maintained park trails inside pristine old growth forests. The aerial platform's capacity to be transported over long distances provides the potential for any study to be well replicated across a whole region.

In Chapter 3, the first original paper of this thesis, I focus on characterizing and comparing the canopy and understorey spider diversity in north-temperate forests of southern Quebec. I direct my attention to the patterns of diversity through multivariate analyses of diversity, and focus on one spatial scale (i.e., the tree). I use rank-abundance distributions (RAD) and changes in species composition to explore differences between tree species sampled and also between the canopy and understorey. I fit RADs of spiders in both habitats and trees against statistical and biological models to detect potential processes influencing the structure of the observed RADs (Wilson 1991). Changes in spider assemblage composition are evaluated with multivariate permutational ANOVAs.

3 Species significantly associated with a tree species or stratum are identified with two-way

ANOVAs. Results of this work provide the baseline data for testing ecological hypotheses in Chapters 4 and 5.

Along with mites (Acaria) and moths (Lepidoptera), spiders are one of the major lineages of arthropods that can disperse passively in the air column (Bell et al. 2005). The apparent randomness of aerial dispersal behaviour and its related risk-reward outcomes inspire studies of adaptations to environmental conditions and the prevalence of life history traits associated with the frequency of this behaviour. In Chapter 4,1 quantify the pre-ballooning behaviours (i.e., strongly correlated to ballooning propensity) of north- temperate hardwood spiders in a laboratory setting. I test the hypothesis that canopy and understorey habitats provide contrasting environmental conditions influencing the ballooning propensity of the spiders living in each habitat. I also test ballooning propensity against various other spider life history traits to identify the suites of traits that most strongly affect this dispersal behaviour. The results of this chapter are used to group species into classes of "limited" and "high" dispersers. Two subsets become the backbone of Chapter 5, in which I determine the influence of dispersal capacity on spider diversity across multiple spatial scales.

In Chapter 5,1 use a spatially hierarchical nested design to compare the diversity patterns of canopy and understorey spiders across four spatial scales; the tree, stand, site and region. I contrast diversity patterns among the "limited dispersal" and "high dispersal" capacity datasets (i.e., from Chapter 4) to investigate processes that may account for

4 observed diversity patterns. The dataset is divided in this way because it is known that dispersal is one of the most important processes linking diversity patterns across spatial scales (Cadotte 2006). Diversity patterns from all spatial scales of the canopy, understorey, and dispersal datasets are contrasted with Species-Abundance Distributions

(SADs), diversity partitioning, and nested multivariate permutational ANOVAs. I use the dispersal subsets of species to test predictions about the influence of dispersal capacity on a and p-diversity patterns across spatial scales (Hubbell 2001, Mouquet and Loreau

2003). I use a metacommunity framework (Wilson 1992; Holyoak et al. 2005) as a model for the interpretation of the diversity patterns produced in Chapter 5. A metacommunity is defined as a set of local communities linked by dispersal (Leibold et al. 2004). As such, any changes in the diversity patterns observed in the dispersal subsets can be linked to processes influenced by dispersal such as species aggregation and habitat heterogeneity. Similar diversity patterns in both dispersal subsets will indicate that processes other than those influenced by immigration and emigration regulate spider diversity patterns.

1.1 Summary of objectives

The main goal of my thesis is to identify the regional spatial patterns and processes dictating canopy spider diversity within a nested subset of spatial scales in the sugar maple dominated north-temperate hardwood forests of southern Quebec. These spatial diversity patterns are then contrasted with spider diversity patterns in the understorey.

Through a laboratory dispersal experiment, ballooning propensity of north-temperate

5 hardwood spiders is quantified to test the influence of the habitat and life history traits on ballooning propensity to identify parameters that promote ballooning. The final objective of the thesis is to contrast the diversity patterns of "limited dispersal" or "high dispersal" capacity species subsets across multiple.spatial scales to measure the influence of dispersal on regional spider diversity patterns. Each chapter is formatted as an original paper with detailed objectives and hypotheses to be tested.

In Chapter 3 I characterize and compare the diversity and community composition of canopy and understorey spider assemblages associated with sugar maple and American beech trees. More specifically, I ask whether spider diversity is randomly distributed in the canopy and the understorey, and assess if the spider composition differs between the canopy of sugar maple and American beech and their understorey saplings. I make the following predictions:

Pi: The diversity and species composition of canopy and understory spiders will be different.

P2: The diversity and species composition of the spider assemblages in sugar maple and

American beech canopies will be different.

P3: The diversity and species composition of the spider assemblages in sugar maple and

American beech understorey saplings will be different.

6 In Chapter 4 I measure the ballooning propensity of north-temperate hardwood forest spiders and identify important habitat and life history traits responsible for the initiation of ballooning. My specific objectives are to: 1) compare the ballooning propensity of canopy and understorey spiders sampled in a north-temperate hardwood forest and, 2) test the influence of biotic and abiotic factors on ballooning propensity. I make the following predictions:

Pi: Ballooning propensity is higher for individuals sampled in the canopy due to greater instability in various environmental factors.

P2: Small sized individuals from abundant species will balloon more frequently, a finding previously documented (Humphrey 1987; Roff 1991).

P3: Web-building species will show a higher propensity to balloon; increased silk production is correlated with higher ballooning propensity (Bonte et al. 2003).

Chapter 5 investigates changes in community composition and richness of spider assemblages in north-temperate hardwood forest as a function of spatial scales. My primary objective is to identify potential biological processes affecting spider diversity at each spatial scale, using a metacommunity framework. In my analyses I consider local community species-abundance distribution, composition, and richness at four spatial scales: tree, stand, site, and regional. I also use subsets from the complete species pool to investigate the influence of dispersal capacity and habitat type on local community structure across space. I make the following predictions:

7 Pi: The species-abundance relationship will become increasingly lognormal.

P2: Canopy and understorey assemblages will not follow similar SAD models due to increased mass and rescue effects in the canopy habitat.

P3: Spatial scales will not contribute equally to the regional richness pool.

P4: Subsets of highly dispersering species will increase a-diversity and decrease |3- diversity, homogenizing local diversity across spatial scales.

P5: Subsets of species with limited dispersal ability will decrease a-diversity and increase

P-diversity across spatial scales. 2. Literature review

2.1 Temperate canopy spider ecology

Forest canopies are thought to contain 50% of all species (Didham and Fagan 2004), and canopies perform or regulate essential ecosystem functions including photosynthesis, energy flow, biogeochemical cycles, and carbon sequestration (Ozanne et al. 2003).

Tropical forest canopies have been studied more extensively than their temperate counterparts especially due to the fascination generated by their rich and unknown biodiversity. Temperate forests do, however, harbour an important component of North-

American biodiversity (Yahner 1995). The temperate forest canopy arthropod fauna has been studied (e.g., Moran and Southwood 1982; Halaj et al. 1998; 2000; Gering et al.

2003) but seldom has the canopy fauna been compared directly to the fauna living directly below in the understorey. The drastic seasonal changes in temperate forests limit the potential for animals to develop specialized niches in the canopy as many animals return to the ground to overwinter. Nevertheless, temperate canopy studies demonstrate that the canopy fauna is generally less rich and differs in composition and dominance structure with the understorey fauna (Preisser et al. 1999). These differences are attributed to contrasting abiotic and biotic conditions in the habitats (Le Corff and

Marquis 1999).

In the canopy, the short term (daily) and long term fluctuations in light, temperature, moisture, are in contrast with the conditions found in the understorey (Bohlman et al.

9 1995; Fagan et al. 2006; Lowman & Wittman, 1996; Basset et al. 2003). Canopy habitats of mature forests experience higher fluctuations in solar radiation, temperature, and wind speed. Light transmission decreases gradually from the canopy to the understorey

(Canham et al. 1994). For example, only 1-2 % direct sunlight reaches the forest floor in sugar maple forests (Ellsworth and Reich 1992). These abiotic differences between the canopy and understorey are reflected in habitat structure: Canopies contain more leaves, and the leaves are thicker and narrower than their understorey counterparts (Parker 1995).

Leaf nutrient content differs between canopy and understorey and between tree species

(Le Corff and Marquis 1999; Fortin and Mauffette 2002). Leaf microhabitat is more abundant in the canopy but is potentially less varied than in the understorey (Uetz and

Dillery 1969). These habitat differences between the canopy and the understorey are reflected in patterns of arthropod diversity of temperate forests (Ulyshen and Hanula

2007). This is especially true in the case of general predators, such as spiders, the diversity of which is often linked to habitat complexity and local environmental conditions (Stratton et al. 1979; Greenstone 1984; Lawrence and Wise 2004).

In temperate forests, canopy arthropod diversity differs among tree species (Southwood et al. 1982; Schowalter and Ganio 1998; Schowalter and Zhang 2005) but generally not among individuals of the same tree species (Southwood et al. 2005; but see Ozanne et al.

2000). Species richness increases with tree abundance (Kennedy and Southwood 1984) and structural complexity of the habitat (Halaj et al. 2000). Temperate canopy arthropod communities exhibit vertical stratification (Schowalter and Ganio 1998; Le Corff and

Marquis 1999; Vance et al. 2003; 2007; Ulyshen and Hanula 2007). This stratification

10 maybe more distinct within lower taxonomic levels (e.g., family, genus) (Ulyshen and

Hanula 2007). Densities of hunting and web-building spiders are similar between low canopy distal and basal branch samples of mature sugar maples (Brierton etal. 2003) but differ between the lower and upper canopy. Turnbull (1960) and recently Aikens (2008) both found that the upper canopy spider assemblage of hardwood stands were subsets of the lower canopy assemblages and a decreasing similarity in species assemblages was found between the shrub layer, the lower canopy, and the upper canopy spider assemblage. Low similarity between arboreal and ground-dwelling spiders was also found in beech forests of Germany (Hovemeyer and Stippich, 2000). Comparative studies of canopy and understorey arthropod faunas demonstrate vertical stratification in community composition and, contrary to the tropics, the canopy fauna is generally less diverse and abundant than its understorey counterpart (Preisser et al. 1999; Vance et al.

2003; 2007; Ulyshen and Hanula 2007). Aside from foliage, tree bark and suspended litter represent other important reservoirs of canopy arthropod diversity (e.g., Proctor et al. 2002; Bealieu et al. 2006; Lindo and Winchester 2006).

In north-temperate hardwood forests, tree bark offers widely different potential habitat than foliage for spiders, and it offers an important overwintering habitat for bark, foliage, and ground living spiders (Bower and Snetsinger 1985). Bark can also act as a transitional and mating habitat for foliage and ground living spiders. In England, bark spider abundance was positively correlated with bark complexity of oak trees but was negatively correlated on pine trees (Curtis and Morton 1974). In dominant European deciduous trees, single spider species dominate smooth bark trees and a more diverse

11 fauna is found on fissured bark trees, and the complex fissured bark offers diverse microclimates producing more diverse bark assemblages (Nicolai 1986). Ecological studies on bark spider diversity patterns in North-American north-temperate hardwood forests are few and the canopy fauna has never been investigated (Pinzon and Spence

2008). Tree trunks represent excellent model communities to study spatial diversity patterns; they have been suggested to represent "islands in a sea of continuous litter" for the oribatid mite fauna (Proctor et al. 2002). As such, a particular attention to the tree trunk spider fauna of North-temperate hardwood forests will provide a complementary portrait to the foliage spider fauna also investigated in this thesis.

Spiders are a good model taxon for comparative canopy biodiversity studies; they are generally found in high abundance in forests (e.g., Buddie et al. 2000), their distributions and abundances are linked to structural attributes of the habitat (Pettersson 1996; Larrivee et al. 2005), they play key functional roles in ecosystems (e.g., Lawrence and Wise

2004), and their taxonomy is relatively stable and accessible (e.g., Coddington and Levi

1991). It is well documented, especially on coniferous trees, that predacious spiders play a significant role in structuring tree canopy food webs (Loughton et al. 1963; Halaj et al.

1997); spiders are also prey for the avifauna (Gunnarsson 1996; Gunnarsson and Hake

1999). Their abundance, richness and community structure in tree canopies are associated with vegetative structure complexity (Stratton et al. 1979; Jennings and Dimond 1988;

Jennings et al. 1990; Halaj et al. 1998). Spider density and composition varies between the understorey strata and the tree crown but also within mature hardwood tree crowns

(Aikens 2008). Prey availability and predator pressure can also limit spider abundance

12 and richness (Gunnarson 1996; Halaj et al. 1998; 2000). In summary, it is well established that environmental factors and habitat complexity strongly influence spider diversity, including assemblages occuring in forest canopies. However, biotic factors, including dispersal ability, are also important factors relating to spider diversity.

2.2 Spider dispersal

In my thesis, I adopt the definition of dispersal proposed by Bullock et al. (2001) who refer to dispersal as intergenerational movement excluding within generation movement pertaining to home range related foraging activities. Dispersal can result in reproduction, death or simply the occupation of an available niche. Its incentives and outcomes are of biotic (population density, life cycle, resources) and abiotic (seasonality, habitat, and climatic conditions) nature (Dieckmann etal. 1999). Consequently, dispersal strategies, rates, and capacities vary within and between species in local communities (Richter 1970;

Morse 1993; Bonte et al. 2003). Arthropods use active (controlled walk, flight, and swim) and passive (uncontrolled flight driven by air or water currents, or phoresy) dispersal strategies. Passive aerial dispersal rates in spiders are influenced by body size, habitat specialization, feeding habits, and it can reflect their phylogenetic history over longer time spans (Bonte et al. 2003). The capacity to disperse over long distances is linked to the strategy used. In arthropods, generally speaking, active flyers and passive aerial dispersers are more prone to long dispersal events than cursorial dispersers

(Driscoll 2008).

13 Spiders can disperse by both cursorial and aerial means. Aerial dispersal, often called ballooning, is produced by wind drag on a silk line(s) rendering the spider airborne once traction on the silk outweighs gravity (Weyman 1993). Passive aerial dispersal involving silk (i.e., ballooning) is performed by species in three orders of arthropods (Araneae,

Acari and Lepidoptera) (Bell et al. 2005). Ballooning is deeply rooted in spider phylogeny but it is not a trait found in all families (Bell et al. 2005). Some species disperse by cursorial means only, while other species disperse aerially and cursorily throughout their life. Generally large bodied spiders (> 5 mm body size) balloon mostly as first or second instars (i.e., when their body size is < 3mm) and tend to disperse cursorial means as they grow (Richter 1970; Roff 1991). Small bodied spiders (~ < 3 mm body size) balloon throughout their life span.

Ballooning individuals do not control where they land rendering the behaviour very risky.

Dispersal is not as risky for habitat generalist as compared to specialist species (Den Boer

1990). Generalist species can afford to have high dispersal rates as the likelihood of finding suitable habitat is high. Bet-hedging or risk-spreading theory supports the adaptive value of high dispersal rates for habitat generalist species. Species can spread risk by having large numbers of individuals, a trait generally successful in spatiotemporally unstable habitats (Hopper 1999; Kisdi 2002). Mixed Evolutionarily

Stable Strategy (ESS) also explains differences in intra-specific dispersal frequencies

(Maynard-Smith and Price 1973). In mixed ESS, individuals within a population use different but equally successful dispersal behaviors or rates to limit conflicts over space

14 and resources (Riechert 1978; Weyman et al. 2002). Under an ESS, each individual's dispersal behaviour follows a fixed probability distribution or one that responds to biotic and abiotic factors (Bell et al. 2005). Bet-hedging and ESS theories are supported by studies on spider ballooning frequencies that link increased fitness to variability in passive dispersal propensity (Weyman et al. 2002; Bonte et al. 2003b; Bell et al. 2005).

Thus, these adaptive features associated with dispersal capacity distribute populations unevenly across space and are reflected in community structure. Passive aerial dispersal is negatively associated with the degree of habitat specialization, large body size and hunting strategy (Bonte etal. 2003; 2006; Driscoll 2008).

From a metacommunity perspective (i.e., local communities linked by dispersal within a region (Wilson 1992; Leibold et al. 2004)), species with high dispersal capacity are less prone to local extinctions while those with low dispersal capacity can become locally extinct more frequently (Gonzalez et al. 1998; Gonzalez 2005; Leibold et al. 2004).

Consequently, species assemblages with low dispersal capacity should show low d- diversity and high P-diversity (Mouquet and Loreau 2003). In sand dune ecosystems in

Belgium, increasing habitat stability and connectivity reduced patch P-diversity and increased a-diversity by allowing more specialized spider species to co-exist with generalist spider species (Bonte et al. 2006). The factors influencing ballooning propensity can also help explain how ballooning contributes to the success of a species in different or patchy habitats. Understanding the influence of various biotic (e.g., body size, developmental stage, sex, phylogeny, feeding strategy, habitat specialization) and abiotic (e.g., habitat stability, connectivity, predictability, and seasonality) factors on the

15 ballooning propensity of spiders can help explain how dispersal capacity influences species distribution patterns at multiple spatial scales. For example, Bonte et al, (2003;

2006b) showed that habitat specialists have lower ballooning propensities than generalists, while habitat connectivity increased ballooning propensity. This was reflected in the local (3 and a-diversity of dune spider assemblages. Hence, dispersal capacity and related life history traits are associated with local and regional diversity patterns and help elucidate the processes governing species diversity patterns across space.

The importance of dispersal on the structure of communities is relatively well established but how dispersal influences community structure is not as clear. Dispersal can have opposing effects on local species coexistence: it can increase local diversity by re­ establishing extinct local populations (e.g. rescue-effect, Brown and Kodric-Brown 1977) and by maintaining populations through immigration of individuals from densely populated adjacent local communities (e.g. mass-effect (Shmida and Wilson 1985); source-sink dynamics (Pulliam 1988)). Dispersal also affects local diversity negatively by introducing better competitors, more predators, and limiting spatial refuges to inferior competitors or prey (Kneitel and Miller 2003; Cadotte and Fukami 2005). At the regional scale, dispersal capacity can also produce opposing effects; limited dispersal increases local P-diversity and reduces a-diversity, and high dispersal capacity diminishes local p- diversity and increases a-diversity (Hubbell 2001; Mouquet and Loreau 2003; Gonzalez

2005). Better comprehension of the influence of dispersal on diversity patterns resides in defining spatial scales within a region in a hierarchical manner (Gering and Crist 2002;

16 Cadotte and Fukami 2005). The hierarchical nature of space and its transposition onto diversity patterns has attracted much attention recently (e.g., Lande 1996; Gering and

Crist 2002; Crist et al. 2003; Lindo and Winchester 2008).

2.3 Diversity patterns in space

Understanding patterns of species diversity and processes that generate it through space and time is one of the goals of ecology (Wiens 1989; Tokeshi 1999). Species diversity research focuses on patterns of distribution, abundance and interactions among species

(Leibold et al. 2004). Studies of biodiversity typically start with searching for non- random patterns in species diversity through observational studies. Once non-random spatial patterns of diversity are established, systems can be investigated further to identify the processes underlying those patterns through hypothesis testing and a priori knowledge of the ecosystem. These patterns and processes are observed at various temporal and spatial scales and their importance can vary across scales (Rosenzweig

1995; Holyoak et al. 2005). Variations in diversity patterns in time range from diurnal- nocturnal patterns (Buddie & Rypstra 2003), seasonal and yearly patterns of species diversity (Stork et al. 2001), and over longer ecological or evolutionary time scales

(Rosenzweig 1995).

At very large scales (continental) species diversity is largely influenced by factors related to latitude (Simpson 1964; Peck et al. 2005), altitude and by available energy (Currie

1991). In general, higher species richness is found towards the equator, and at lower

17 elevations, respectively. Species geographic ranges are independent from one another, and their abundance across their range is mostly low (rare) with a few peaks (McGill and

Collins 2003). Local and regional spatial scales are herein implicitly defined as follows: local scale is a spatial scale small enough that individuals could encounter and interact with each other during their life cycle (Holyoak et al. 2005); regional scalerefers to the overall area containing the species pool that could colonize any location within the region through dispersal over one or more generations (Srivastava 1999).

Assessing the importance of local processes (competition, niche breath, predation) and regional processes (dispersal: e.g. immigration/emigration) that shape local community diversity has received much attention in the ecological literature (e.g., Ricklefs 1987;

Gonzalez et al. 1998; Bell 2001; Leibold et al. 2004). At the local spatial scale, without external influence considered, species diversity patterns are influenced by predation, resource availability, ecological and spatial niche availability, and competition (Ricklefs

1987; Cornell and Lawton 1992; Kneitel and Miller 2003; Cadotte et al. 2006). Local habitat complexity strongly influences local spider diversity (Greenstone 1984; Halaj et al. 2000; Larrivee et al. 2005). Predation by spiders can also affect local species diversity across trophic levels (Schmitz 2008). Local competition and co-existence within and between species also influences local diversity by narrowing ecological niches (Marshall and Rypstra 1999; Harwood and Obrycki 2005). In metacommunity studies, local diversity of inquilines increases in resource supplemented pitcher plants (Kneitel and

Miller 2002), while the presence of predators can reduce local diversity (Cadotte et al.

2006). Thus local processes influence local diversity but can not explain all of it. Larger

18 scale processes occurring regionally influence local species diversity. Regional species pools and the overall dispersal capacity of the species within the region along with local community assembly patterns strongly influence local community diversity (Hubbell

2001;Leiboldefa/. 2004).

At the regional scale, species diversity patterns are influenced by historical events (e.g.; disturbance regime: forest fire cycles, insect epidemics) and habitat heterogeneity

(Petraitis et al. 1989; Cornell 1999; Mackay and Currie 2001; Tews et al. 2004). Regions characterized by frequent disturbances support populations of species with high dispersal capacities and short generation times, and species tend to be more generalist in their habitat choices, hence are often good colonizers due to their high dispersal capacity

(Cadotte 2007). In the context of increasingly fragmented habitats regionally, more specialized species with diminished dispersal capacity are more sensitive to local extinctions (Bonte et al. 2003; 2006a). Regional processes are reflected in the diversity patterns found at a regional scale and can inform us on the processes shaping local community diversity (Holyoak et al. 2005).

Regional and local community diversity are related and interconnected (Ricklefs 1987).

Local-regional (LR) relationships are frequently used to study the relationship between local and regional processes and how it affects the structure of local community diversity

(Cornell and Lawton 1992). A linear relationship between local and regional diversity indicates that local diversity is unsaturated and strongly influenced by regional processes and a curvilinear relationship indicates local diversity saturation and points toward local

19 interactive processes independent of the regional species pool (Srivastava 1999).

Recently, the neutral theory of biodiversity and biogeography, and the metacommunity theory have emphasized the importance of dispersal (immigration/emigration) on regional and local diversity patterns (Hubbell 2001; Bell 2001; Leibold et al. 2004).

Holyoak et al. (2005) stressed the importance of considering multiple spatial scales to better understand at what scales metacommunity processes are most influential to local community diversity.

Scale, by definition, is hierarchical in nature such that smaller scales are nested within larger scales (Tokeshi 1999). Since Wiens' (1989) seminal paper, more attention has been paid to the hierarchical nature of spatial patterns and processes. Empirical studies show that species diversity patterns are hierarchically nested in space and driven by different processes depending on the spatial scale considered (Willis and Whittaker 2002; Cadotte and Fukami 2005; Lindo and Winchester 2008). For the reasons outlined above, studies investigating species diversity patterns now often consider multiple spatial scales. This helps to understand how diversity changes across spatial scales and how each spatial scale and its processes influence diversity patterns at other scales (Cushman and

McGarigal 2002; Holyoak et al. 2005; Gonzalez 2005; Bonte et al. 2006a; Lindo and

Winchester 2008). The concept of a, p, and y-diversity (Whittaker 1975) is often used to analyze diversity patterns within and between local communities and across spatial scales

(Veech et al. 2002; Larrivee et al. 2005; Bonte et al. 2006). Alpha and P-diversity correspond to the within and between habitat diversity while y-diversity corresponds to the regional diversity. Lande (1996) recognized that Whittaker's approach did not weigh

20 equally the components of diversity when partitioning them across spatial scales as it is a multiplicative approach. He proposed an additive relationship between the diversity components allowing the analysis of the contribution to the regional species pool of a and P-diversity components across spatial scales. As such, the metacommunity and its paradigms provide a novel conceptual framework to study the impact of local community interactions at the regional scale through multiple spatial scales within a spatially nested hierarchic design.

Most species are unevenly distributed in space which creates different species composition from one site to another (Bell 2005). This is easily observed by plotting histograms of the relation between abundance and the number of species having this abundance creating a Species Abundance Distribution (SAD). Relative Abundance

Distribution (RAD) plots are another means of visualizing and comparing statistical aspects of species composition; all species are ranked starting with the most common and ending with the rarest species (Whittaker 1975; McGill etal. 2007). Observed distributions are investigated through models that potentially account (fit) for the species abundance relationships. Many models have been proposed to match observed SAD's and serve as explanations of community structure: 1) statistical models anchored on probability distribution functions with no biological interpretation (Pielou 1975; Mcgill et al. 2007); 2) biological models based on classical ecological tenants like the spatial niche concept or resource partitioning (Tokeshi 1999); 3) dynamical models relying on stochastic demographics parameters like birth, death, immigration, number of species, community size, and speciation (Bell 2000, Hubbell 2001). The lognormal distribution

21 has proven a very good fit to empirical SADs at a variety of spatial scales even though it has no direct link to classic ecological tenants (McGill 2003; Connolly et al. 2005;

Dornelas et al. 2006; Dornelas and Connolly 2008). Dynamical models have occupied much of the SAD debate in recent years particularly because, unlike other types of models, they produce predictions that can be tested (McGill et al. 2007). Recently, models combining both niche concepts and neutral dynamics have been suggested advocating that niche and neutrality form a continuum in space (Gravel et al. 2006; Holt

2006).

Species-abundance distribution (SAD) models lend themselves very well to study the influence of habitat and dispersal on local communities nested in space. Changes in species-sorting and niche apportionment dynamics inside local communities at different spatial scales can be investigated by comparing SADs at different spatial scales within a metacommunity. Departure of the local community SAD from the metacommunity SAD reflects the influence of non-random processes on species composition. Changes in the shape of SADs at the local and regional scales can be related to spatial aggregation of conspecifics (Green & Plotkin, 2007). The metacommunity SAD tends to produce a log- series curve due to high dispersal rates while local communities tend to produce lognormal SADs with surpluses of rare species (Hubbell 2001; Bell 2001; McGill 2003).

Recently, lognormal and multimodal SAD's have been unveiled as the spatial scale or sampling effort increases (Connolly et al. 2005; Dornelas et al. 2006; Dornelas and

Connolly, 2008). The emergence of those lognormal distributions is thought to result from combinations of stochastic and environmental processes. Comparing dispersal

22 driven SADs from different spatial scales will help detect the spatial scale at which dispersal impacts SADs within a metacommunity.

2.4 Metacommunity ecology

As an extension of metapopulation ecology (Hanski and Gyllenberg 1993), metacommunity ecology provides a framework to study regional diversity patterns and associated processes at multiple spatial scales. In general, spatial dynamics within a metacommunity can be explicit or implicit. Studies considering space explicitly keep track of the location of all local communities within the metacommunity. Spatially explicit models require extensive data to be recorded and analyzed. While able to explore a variety of dynamic models, many spatially explicit models become mathematically intractable (Holyoak etal. 2005). Thus, most metacommunity studies are spatially implicit. Implicit studies provide a simplified representation of metacommunity dynamics; yet they can clarify emergent properties of local community dynamics that result from multivariate species interactions potentially lost in spatially explicit models.

There are explanations for the recent interest generated by metacommunity ecology: 1) It allows investigators to consider multiple spatiotemporal scales within a region and thus interpret local and regional diversity patterns as a two-way street, and 2) It provides competing, and at times, complementary models to describe metacommunity dynamics.

In their seminal paper on metacommunity ecology, Leibold et al. (2004) recognize four paradigms defining metacommunity dynamics in which they consider space implicitly:

23 1) Patch dynamics: Assumes that all patches are identical. Local community diversity is restricted by dispersal capacity and the spatial dynamics are driven by local extinctions and colonization.

2) Species-sorting: Stipulates that local community diversity is driven by resource gradients and niche space availability. Dispersal capacity does not limit local diversity.

3) Mass-effect: Focuses on the importance of immigration and emigration in maintaining local populations across the metacommunity in a context where patch quality varies creating source-sink population dynamics (Pulliam 1988).

4) Neutrality: Assumes all species are neutral in their competitive and dispersal ability, and have similar fitness (Hubbell 2001). Local community diversity dynamics arise from immigration, emigration, birth and death rates of individuals randomly moving through the metacommunity.

Local communities are not necessarily driven by a single paradigm at any given time; their dynamics can share attributes of more than one paradigm. All interacting species in a metacommunity will not conform to one model. Different metacommunity perspectives have interactive influences on local community dynamics the strength of their influence varies across local communities and perhaps across spatial scales within the metacommunity. Life history trait patterns of species subsets in local communities offer the potential to segregate the influence of each paradigm on local community diversity patterns. For example, species guilds sharing common life history traits related to dispersal capacity (e.g., wing length, body size, and dispersal mode) can be used to test the importance of species interactions (species-sorting dynamics) vs. mass-effects. The

24 strength of effect of each paradigm also varies with the spatial scale considered. Thus, the diversity patterns of the different guilds can then be compared at different spatial resolutions to detect changes in the influence of the different metacommunity models at particular spatial scales.

Metacommunity ecologists seek to explain patterns of species diversity linked to changes in composition related to environmental factor and their gradients, and across spatial scales (Holyoak et al. 2005). Single species local community dynamics are determined mainly by species interactions and dispersal. As the spatial scale increases, dispersal

(mass and rescue effects), and the historical context (priority effects-species assembly, disturbance regime) have a larger influence on species diversity patterns (Cadotte 2006).

Dispersal links diversity patterns across spatial scales through colonization ability (mass and priority effects) and local population persistence (rescue effect) (Brown and Kodric-

Brown 1977; Shmida and Wilson 1985). Different dispersal capacities are reflected in species interactions, local community richness and composition, and species turnover rates (P-diversity) within and between local communities. High dispersal capacities help maintain or increase species diversity across spatial scales, while limited dispersal capacities can result in local extinctions and high species turnovers as spatial scale increases (Hubbell 2001; Mouquet and Loreau 2003).

Empirical support for the importance of dispersal (mass effect and patch-dynamics) versus species-sorting and neutrality remains scarce in the literature (but see Kneitel and

Miller 2003; Cadotte and Fukami 2005; Vanschoenwinkel et al. 2007) and few empirical

25 metacommunity studies address local communities hierarchically nested in space but rather on a local to regional spatial scale basis (but see Cadotte and Fukami 2005; Miller and Kneitel 2005; Lindo and Winchester 2008). The number of spatial scales needed to best understand metacommunity dynamics is not clearly defined (Holyoak et al. 2005), and studies with hierarchically nested spatial scales can test metacommunity paradigms over more than two spatial scales.

Invertebrates, because of their small size, high richness and abundance at small spatial scales, and various dispersal modes (i.e., passive and direct flight, cursorial) represent excellent model taxa to test metacommunity paradigms. Their local communities occupy small spatial scales with areas of generally less then 30 metres (Digweed et al. 1995), allowing high number of replicates across several orders of magnitude in space. Spiders represent an ideal arthropod group to empirically test metacommunity paradigms because they are highly diverse, and occupy a similar functional/ecological niche (i.e., top arthropod predators). Since they are all predators, their diversity is strongly influenced by environmental conditions and habitat complexity (Uetz 1979; Greenstone 1984; Buddie et al. 2000; Larrivee et al. 2005). Also, their dispersal capacity varies within local communities and can be related to life history characteristics and/or habitat conditions.

As such, spiders from the canopy and understorey of north-temperate hardwood forests can be used as a model assemblage to investigate the influence of habitat and dispersal on local community diversity at multiple spatial scales within a metacommunity framework.

The canopy and understorey spider assemblages of north-temperate hardwood forests differ in composition and these assemblages can be separated in species subsets of

26 limited and high dispersal capacity based on their propensity to disperse passively through ballooning.

In summary, this literature review shows that north temperate hardwood forest canopies offer the possibility, by using spiders as a model taxon, to test modern ecological models in multiple ways. This review shows that through the characterization of species diversity patterns we can assess habitat and life history constraints on a dispersal mechanism. It also shows that we can determine, within a metacommunity framework, the main processes that structure spider diversity in north temperate hardwood forests by contrasting the diversity patterns at different spatial scales of spider species subsets with different dispersal capacity.

27 Original papers

28 3. Diversity of canopy and understorey spiders in north-temperate hardwood

forests

Maxim Larrivee' and Christopher M. Buddie'

'Department of Natural Resource Sciences, McGill University, 21,111 Lakeshore Road,

Saint-Anne-de-Bellevue, Quebec, Canada, H9X 3V9

Published in Agricultural and Forest Entomology (April 2009)

29 3.1 Preface

Studies of North-temperate hardwood canopy spider diversity have been mostly descriptive to this day. Dinstinctiveness of the canopy fauna and its contribution to the overall diversity of north-hardwood temperate forest spider assemblages should be characterized to assess the relevance of including canopy sampling to monitor hardwood forest spider diversity. This paper characterizes and compares canopy and understorey foliage spider diversity of sugar maple and American beech in old-growth north- temperate hardwood forests of southern Quebec. Several aspects of the sampling access and design of this paper are novel to canopy ecology and spider ecology. It demonstrates the usefulness of aerial platforms to perform regional scale arthropod diversity studies with large numbers of replicates using a direct sampling technique. Canopy spiders had previously been mostly investigated indirectly by clipping branches. The results in this paper demonstrate that canopy spider diversity differs in species composition and is complementary to the understorey fauna. They also show that canopy species composition differs between sugar maple and American beech and suggest that different processes are driving canopy and understorey spatial patterns of diversity. The information presented in this chapter should help stimulate ecological studies on spiders and overall arthropod diversity in temperate canopies because of the sampling methods used and the demonstration that forest canopies are important reservoirs for spider diversity in north-temperate forests.

30 3.2 Abstract

We characterize and compare diversity patterns of canopy and understorey spiders

(Arachnida: Araneae) on sugar maple (Acer saccharum Marsh.) and American beech

(Fagus grandifolia Ehrh.) in hardwood forests of southern Quebec, Canada. We sampled canopies of 45 sugar maple and 45 American beech trees and associated understorey saplings in mature protected forests near Montreal. Samples were obtained by beating the crown foliage at various heights and by beating saplings around each tree. Eighty-two species were identified from 13,669 individuals. Forty-eight species and 3,860 individuals and 72 species and 9,809 individuals were collected from the canopy and the understorey, respectively. Multivariate analyses (NMDS ordination and NPMANOVA) showed the composition of canopy and understorey assemblages differed significantly, and canopy assemblages differ between tree species. Rank-abundance distribution models fitted to the canopy and understorey data indicate that different mechanisms structure the assemblages in both habitats. Three abundant spider species were significantly more common in the canopy, ten species were collected significantly more often in the understorey. The forest canopy is an important reservoir for spider diversity in north- temperate forests.

Keywords Canopy, spiders, diversity, sugar maple, American beech, hardwood temperate forest, understorey, Araneae, Rank-Abundance Distribution (RAD)

31 3.3 Introduction

Forest canopies may harbour up to 50% of all living organisms (Didham and Fagan

2004), and key ecosystem functions occur in or are regulated by the forest canopy (e.g., photosynthesis, energy flow, biogeochemical cycles, carbon sequestration) (Ozanne et al.

2003). Better access, recent standardized and replicated studies are helping to understand understorey and forest canopy dynamics (Basset et al. 2003a; Fagan et al. 2006).

Differences between the canopy and the understorey are reflected by the uniqueness and diversity of the fauna associated with tree canopies, best exemplified by arthropods

(Erwin 1982; Basset et al. 2003a; Winchester 1997; Lindo and Winchester 2006).

Previous work shows that canopy arthropod abundance and community structure differ between tree species (Southwood et al. 1982; Schowalter and Ganio 1998; Schowalter and Zhang 2005) but generally not between individuals of the same tree species

(Southwood et al. 2005; but see Ozanne et al. 2000). Species richness tends to increase with tree abundance (Kennedy and Southwood 1984) and structural complexity of the habitat. Prey density increases species richness and abundance of predators (Halaj et al.

2000). Temperate canopy arthropod communities can exhibit vertical stratification

(Schowalter and Ganio 1998). Densities of hunting and web-building spiders are similar between low canopy distal and basal branch samples of mature sugar maples (Brierton et al. 2003). In England, the upper canopy spider assemblage of an oak stand (Quercus robur L.) was a marginal extension of the lower canopy assemblage and decreasing similarity was found between the shrub layer, the lower canopy, and the upper canopy

32 spider assemblage (Turnbull 1960). Low similarity between arboreal and ground- dwelling spiders was found in beech forests of Germany (Hovemeyer and Stippich 2000).

Spider abundance was positively correlated with bark complexity of oak trees but negatively correlated on pine trees in England (Curtis and Morton 1974).

Spiders are a good model taxon for biodiversity studies as they are generally found in high abundance in forests (e.g., Buddie et al. 2000), their distributions and abundances are linked to structural attributes of the habitat (Pettersson 1996; Larrivee et al. 2005), they play key functional roles in ecosystems (Lawrence and Wise 2004), and their taxonomy is relatively stable and accessible (e.g., Coddington and Levi 1991). It is well documented, especially on coniferous trees, that predacious spiders play a significant role in structuring tree canopy food webs (Loughton et al. 1963; Halaj et al. 1997); spiders are also prey for the avifauna (Gunnarsson 1983; 1996; Gunnarsson and Hake 1999). Their abundance, richness and community structure in tree canopies are associated with vegetative structure complexity (Stratton et al. 1979; Jennings and Dimond 1988;

Jennings et al. 1990; Halaj et al. 1998). Prey availability has been shown to limit spider abundance and richness (Halaj etal. 1998; 2000).

The size and composition of deciduous hardwood forests in eastern North America has changed dramatically over the last two centuries due to harvesting, agriculture, urbanization and introduced pests and pathogens (Hale et al. 1999; Brisson and Bouchard

2003). It is therefore important to characterize the diversity of canopy and understorey arthropods in north-temperate hardwood forests. Such data can help establish more

33 realistic estimates of species diversity in these forests, especially if canopy-based sampling is included. Research on canopy arthropods in mature hardwood forests of

Eastern North America has been mostly inventorial (Brierton et al. 2003) or focused on herbivorous insects (e.g., Krinsky and Godwin 1996; Fortin and Mauffette 2001; 2002;

Gering et al. 2003; Vance et al. 2003). Studies on generalist predators, such as spiders, are notably absent. Our general objective was to characterize and compare the diversity and community composition of canopy and understorey spider assemblages associated with sugar maple and American beech trees. More specifically, we asked whether spider diversity is randomly distributed in the canopy and the understorey, and assessed if the spider composition differs between the canopy of sugar maple and American beech and their understorey saplings.

3.4 Material and methods

3.4.1 Sampling design and study sites

Fifteen mature sugar maple and 15 American beech trees were sampled in each of three sites within the greater Montreal region (SW Quebec, Canada): (i) the Mont-St-Hilaire biosphere reserve (MSH) (45°32' N; 73°09' W), (ii) Oka National Park (OKA) (45°28'

N; 74°04' W), and (iii) Mont-St-Bruno National Park(MSB) (45°33' N; 73°19' W). The

90 trees sampled were chosen from the subset of healthy trees dominating the canopy.

The average height (± SE) of the trees was (24.7 m ± 0.3 m) whereas the average diameter at breast height was (44.4 cm ± 1.1 cm). The mean number (± SE) of mature

34 trees per 400 square metres was 7.7 ± 1.0 and 8.4 ± 1.7 for sugar maple and American beech whereas there were 2.5 ± 0.3 saplings of sugar maples per square metre and 1.0 ±

0.1 for American beech. Individuals of American beech were assessed for severity of beech bark disease to ensure that sampled trees were in a similar state of health. The following criteria were used in our American beech tree selection: no or minimal crown damage, no or minimal bark damage on the trunk, and no or minimal amount of dead or dying branches in the crown.

Canopies were accessed using a DINO 260xt® (distributed by Specialty Equipment,

Indianapolis, IN, USA) mobile aerial lift platform towed from site to site. The lift enabled us to reach heights of > 26 m in the canopy and it had a range of horizontal motion of

11.7 m with the ability to rotate 360 degrees around its base. Each tree (canopy and understorey) was sampled approximately every 21 days. In 2005, there were four sampling periods between June 10 and August 30. In 2006, there were six sampling periods, four between May 15 - July 19 and two between August 23 and September 18.

No samples were taken between July 19 and August 22 as data from the 2005 revealed that many (unidentifiable) juveniles were present during that period. Early and late season represent peak periods of adult spider catches in northern forests (Buddie and

Draney 2004; Niemela et al. 1994). Spiders were sampled in the canopy and the understorey using a beating sheet. In the canopy, every sample consisted of beating six branches five times each (in sequence) (three mid-canopy branches, three upper canopy branches) and six saplings (smaller than 3 m in height) in the understorey. A conscious

35 effort was made to beat branches of similar size in the canopy and the understorey to standardize beating samples as much as possible. We defined mid-canopy as the upper half of the crown up to the last two metres, and upper canopy is defined as the last two metres of the crown up to the interface with the atmosphere (Basset et al. 2003b).

Spiders were identified to species level whenever possible using the keys of Paquin and

Duperre (2003) and Ubick et al. (2005). Classification followed Platnick's World Spider

Catalog V8.5 (Platnick 2007). Voucher specimens are deposited at the Lyman

Entomological Museum (Ste-Anne-de-Bellevue, Quebec) and the Canadian National

Collection (Ottawa, Ontario). Juveniles were assigned to a species only in the case where the juvenile individuals had morphological traits that were unique to a species or when an extremely high percentage of the adults identified were of one species in a genus (for example: adults of Emblyna sublata (Hentz) represented 97.5% of all adult Emblyna identified), or the genus was represented by only one species in our geographical area. As such, we are confident that the dataset used to produce our species level analyses renders an adequate portrait of the spider assemblages found on the foliage of northern temperate hardwood forest.

3.4.2 Data analyses

The analyses are based on individuals that could be identified reliably to the species level, a procedure commonly used for arachnid biodiversity research (e.g., Buddie et al.

2000; Beaulieu et al. 2006). About 2,100 juveniles (13.5 % of the total collection) could

36 not be identified to species level and were therefore removed prior to analyses. The removal from the data matrix of these juveniles did not affect the quality of our interpretation or the power of our statistical analyses.

We fitted observed rank-abundance distribution (RAD) curves to assess the dominance structure of spider assemblages collected in the canopy compared them to those collected in the understorey. The observed RAD's were fitted to five species abundance distribution models: niche preemption, lognormal, veiled lognormal, Zipf, and Zipf-

Mandelbrot following Wilson's (1991) approach. The fitted curves were created using the radfit function from the Vegan Library in R (Oksanen et al. 2006). This function also calculates an Akaike Information Criterion (AIC) score for each model to identify the species abundance distribution model that best represents the observed data based on the principles of parsimony and simplicity (Mazerolle 2006). We used the delta AIC and

Akaike weights to assess the scores of all the models fitted. Models with a delta of 2 or less that had an Akaike weight < 0.9 were selected to best approximate the true model of the observed data (Mazerolle 2006). We also calculated the complementarity of the canopy and the understorey species richness and of the sugar maple and American beech species richness with the Marczewski-Steinhauss (M-S) complementarity index (Colwell and Coddington 1994). The index varies from 0 (identical species list) to 1 (full complementarity of the species list).

We used Coleman rarefaction curves (Estimates, Version 8.0 (Colwell 2006)) to provide a measure of expected species richness (mean ± SD) for spiders from canopy and

37 understorey foliage of sugar maple and American beech. We opted for this approach as it is generally less biased by sampling effort than other diversity indices (Gotelli and

Colwell 2001; Buddie etal 2005).

A nonmetric multidimensional scaling ordination (NMDS) was performed in R (R

Development Core Team 2007) using the package labdsv (Roberts 2006) to visualize the ordination structure of the samples based on the community composition (Anderson

2001). The data table was submitted to a Hellinger transformation (Legendre and

Gallagher 2001) from the Vegan Library in R (Oksanen et al. 2006) and a distance matrix was created using the Hellinger distance (Vegan Library, dist. function). Confidence ellipses were overlaid on the graph representing one standard deviation from the centroid of each group. The first dimension accounted for 44.7 percent of the variation, and the second for 27.8 percent. A third axis accounted for 11.2 percent but is not shown in the graphical representation. The third dimension did not add value to the interpretation of the ordination and the reduction in stress value for a two dimension NMDS compared with a three dimension one was small. Stress values of the two dimension NMDS and the three dimension NMDS were below 20. A stress below twenty signifies that the ordination provides a useful description of the information in the distance matrix

(Legendre and Anderson 1999). We used the measure of stress for our NMDS provided in the output of the labdsv routine (Roberts 2006) using the function "bestnmds" for solutions ranging from two to five dimensions. Stress refers to the amount of information lost between values in the distance matrix and the inter-point distances plotted in the ordination. It is the equivalent to the sum of squared residuals of regression analysis. In

38 this case the stress formula is based on the sum of squared differences between the fitted distances and the expected distance values from the regression function (Legendre and

Legendre 1998).

As a complement to the NMDS ordination procedure we completed a three-way permutational multivariate ANOVA with the software PERMANOVA (Anderson 2005) with sampling height, tree type and year representing the three factors. This was done to statistically test the effect of those factors and their interaction on changes in species composition. The data were Hellinger transformed prior to the analysis (Legendre and

Gallagher 2001). This nonparametric multivariate analysis is highly appropriate for our data since we are considering multiple response variables (spider species) and multiple objects (180'sampling sites). It can handle large multiple species datasets that contain more species than replicates and have many rare species creating a matrix with numerous zeros (McArdle and Anderson 2001). It is also possible to partition the total variability between factors using distances other than the Euclidean distance (Legendre and

Anderson 1999). Nonparametric approaches need only to comply with the assumption that the data are independent and that replicates are exchangeable (Legendre and

Anderson 1999). The test of significance for the three factors was done through the permutation of the rows of the raw data matrix. A total of 9999 permutations were performed for every test of significance. Pairwise comparisons were performed to test the levels of each factor when a factor or interactions between the factors were significant using a Monte-Carlo randomization permutation (4999 permutations) procedure of the total number samples associated with each set of comparisons.

39 Two-factor ANOVAs were completed to test for changes in abundance of spiders between the canopy and the understorey (first factor) and between sugar maple and

American beech (second factor). Only the spider species with a minimal abundance of 90 individuals (i.e., half the sample size) were tested to detect any species specialized in one of those habitats. We were purposefully conservative with this threshold to ensure there were enough data for parametric statistics, and to ensure species were common enough to represent a functionally important part of the assemblage. The data were log transformed when necessary to meet the assumptions of normality and homogeneity of the residuals.

For all factorial tests an alpha level of 0.05 was used. Pairwise comparisons were performed for each factor using the Least Significant Difference (LSD) approach.

3.5 Results

Overall 15,806 spiders (87.3 % of which were juveniles) representing 14 families, 52 genera and 82 species were collected during the summers of 2005 and 2006. A total of

13,669 individuals (87.0 % of which were juveniles) was identified to species and used for subsequent analyses (Table 1, Appendix A). Seventy-two percent of the catch, and 61 species belonged to the web-builder ecological guild (Families: Araneidae, Agelenidae,

Dictynidae, Linyphiidae, Mimetidae, Tetragnathidae, Theridiidae, Uloboridae) and 28% of the catch and 21 species to the hunter guild (Families: Clubionidae, Lycosidae,

Philodromidae, Pisauridae, Salticidae, Thomisidae). E. sublata (Dictynidae) accounted

40 for 38.1 % of the collection and the 10 most commonly collected species accounted for

77.4 % of all collections.

3.5.1 Species richness

The veiled lognormal distribution provided the best fit to the RADs of the understorey spider assemblages (smallest delta AIC and Akaike weights) (Fig. 1). The canopy spider assemblages RADs were fitted best by the Zipf-Mandelbrot model (Fig. 1). When all the samples were pooled together the RAD model that best fit the observed data was the lognormal model (Fig. 1). The understorey assemblages showed a linear decay in abundance between the most dominant species (E. sublata) and the species represented by singletons while both canopy assemblages had a distribution that most resembles an exponential decay in abundance. The understorey and the canopy assemblages had a complementarity index (Marczewski-Steinhauss) of 0.53 indicating that both habitats were complementary while the spider assemblages sampled on sugar maple and

American beech foliage were very similar with a complementarity index of 0.2.

Rarefaction estimates from Coleman curves showed that sampling was sufficient to collect most spider species present in the understorey of our study trees, although the rate of accumulation of species in the canopy remained high (Fig. 2). There was no overlap in species richness estimate curves between the understorey and the canopy samples (Fig.

2); at a standardized number of 1838 individuals (the minimal number of individuals sampled in one habitat type), species richness estimates were higher in the understorey than the canopy. Species richness estimates were higher in the sugar maple understorey

41 as compared to that of American beech trees (Fig. 2, i.e., sample size of 4500 individuals).

3.5.2 Spider assemblage composition

The NMDS ordination depicts a clear separation between the samples collected in the canopy and the understorey (Fig. 3). However, the canopy samples of American beech and sugar maple samples were clustered together and the confidence ellipses overlap. A similar pattern was observed for the understorey, where the ellipses overlap. The marginally smaller confidence ellipses around the samples from the understorey indicate somewhat less variance between the samples than between canopy samples (Fig. 3). The nonparametric multivariate 3-way ANOVA indicated that the composition of the spider assemblages did not differ significantly between the two species of trees but differed significantly between the canopy and the understorey (Table 2); this confirmed results from the NMDS ordination (Fig. 3). There was a significant interaction between tree and height factors on spider composition (Table 2). A pairwise comparison indicated a significant difference between the spider assemblage composition associated with the canopies of sugar maple and American beech (t [i, 89] = 2.25, p-value = 0.002) but not between the understorey assemblages by tree species (t [i, 89] = 1.14, p-value = 0.1782).

Species composition of canopy spiders in both tree species did not vary significantly between years. Pairwise comparisons testing this effect found a significant difference between the spider assemblages in the canopy (t [i, 89] = 6.91, p-value = 0.0054) and the

= understorey (t [i; S9] 6.59, p-value = 0.0080) for both sampling years. Thus, spider

42 composition differed significantly between the canopy and understorey samples but not between American beech and sugar maple when understorey and canopy samples were pooled. A significant interaction between the factors height and tree indicated that canopy spider composition differed between tree species.

3.5.3 Species-specific responses

Ten of the most commonly collected spiders were significantly more abundant in the understorey (Table 3). Tetragnatha versicolor Walckenaer was significantly more abundant on sugar maple understorey saplings while Theridion lyricum Walckenaer was significantly more abundant on American beech saplings (Table 3). Three species were significantly more abundant in the canopy. Hentzia mitrata (Hentz) and Theridion murarium Emerton were more abundant in the canopies of both trees while Araniella displicata (Hentz) was significantly more abundant in sugar maple canopies. The crab spider Philodromus rufus vibrans Dondale was significantly more abundant on sugar maple trees (Table 3). Ten spider species were collected only in the canopy, seven of which were singletons.

3.6 Discussion

Spider assemblages inhabiting the forest canopy were distinct from understorey assemblages immediately beneath the same trees in north-temperate hardwood forests.

The major differences between spider assemblages in vertical space were highlighted by

43 lower species richness and evenness, and significantly fewer individuals and spider species in the canopy. In horizontal space, the species composition of sugar maple and

American beech canopy assemblages differed in composition while the composition of understorey saplings did not. Our sampling design for tree canopies allowed us to replicate our project over a large spatial scale and test ecological hypotheses about the spatial distribution of canopy spider assemblages. Our results support findings from other canopy studies stating that the canopy fauna is distinct from the understorey fauna (e.g., oribatid mites: Lindo and Winchester 2006; other arthropods: Schowalter and Zhang

2005).

The different shapes of the best fit models for the observed RADs exemplified the differences between the understorey and canopy spider assemblages. The Zipf-

Mandelbrot curves highlighted an exponential decay in abundance of the canopy assemblages. This illustrates the high dominance by a few species in the assemblage's abundance distribution. It fits assemblages with many rare species as does a logseries model. Zipf-Mandelbrot fits are generally associated with unstable habitats (Wilson

1991). This is an important prediction of this model in our context since the structure of canopy arthropod assemblages can be partially driven by tolerance to environmental conditions (Basset et al. 2003b).

The veiled lognormal model, in contrast, was the best fit for the understorey spider assemblages. It shows a linear decay in abundance: a more even abundance distribution of spider species in the understorey. A veiled lognormal model also indicates that only a

44 fraction of the common species from the assemblage was detected. A larger sample would collect the part of the assemblage behind the veil (Oksanen et al. 2006). This was confirmed when all the canopy and understorey samples were pooled together; here, the best fit model was the lognormal distribution. The veiled lognormal model fit is more representative of communities associated with stable habitats (Magurran 2004).

An interesting aspect of our data is that the lognormal becomes the best fit model when all samples are pooled. When all understorey samples were pooled the veiled lognormal remained the best fit model (result not shown) and so did the Zipf-Mandelbrot model

(result not shown) when all canopy samples were pooled. This also highlights the complementarity of both habitats, as also shown by the M-S complementarity index, in revealing a more complete spider assemblage associated with the foliage of both tree species.

Predictions arising from the RAD models relate to habitat stability and environmental conditions associated with tree canopies and understorey habitats. Short term (daily) and long term fluctuations in light, temperature, moisture, and wind in the canopy create a more unstable habitat then provided by the understorey (Bohlman et al. 1995; Fagan et al. 2006; Lowman and Wittman 1996; Basset et al. 2003a). Higher and more diverse resource availability and less severe habitat conditions in the understorey contribute to its higher evenness and richness as 10 species were significantly more abundant in this forest stratum compared to three species in the canopy.

45 The canopy foliage of deciduous trees in north-temperate forests has to be recolonized every spring rendering it available to pioneering species. The structure of our RADs from the canopy spider assemblages and their best fit models also demonstrate the typical shape of RAD curves for newly colonized habitats. They show high dominance in the species abundance distributions (Magurran 2004). With a small proportion of the individuals overwintering in bark crevices up in the canopy (M. Larrivee - personal observation), recolonization of the canopy habitat most likely occurs from the ground and through long distance aerial dispersal (ballooning). Aerial dispersal from spiders is thought to be random or part of a bet hedging life history strategy (Bonte et al. 2003). As such, ballooning is adaptively favored by species with broad habitat preferences (Kisdi

2002). The most abundant species of the canopy assemblages in our samples H. mitrata,

A. displicata, and T. murarium are known aerial dispersers (Bell et al. 2005) and are eurytopic (Drew 1967; Richman 1989; Jennings and Collins 1986), and we suggest they are pioneer species of hardwood canopies in eastern Canada. A. displicata and T. murarium make their web across a single leaf where they sit throughout the day (Dondale et al. 2003). This use of a single leaf for web-building could explain why they are significantly more abundant in the canopy as the overall quantity of leaves (potential habitat) surpasses that of the understorey saplings surrounding each tree.

Our results about vertical distribution of spiders on deciduous trees corroborate other findings. Arboreal spider composition decreases in similarity from the shrub layer, to the low canopy and the high canopy (Turnbull 1960; Hovemeyer and Stippich 2000). In

British-Columbia, structural features of the tree architecture of Abies amabilis Douglas ex

46 J. Forbes played an important role in determining mean spider population intensities and resulted in a significant difference in the composition of the spider guilds associated with the upper and lower crowns of A. amabilis (Winchester and Fagan 2000). Changes in the structural complexity of the vegetation have been linked to changes in spider diversity within and between coniferous tree species in many studies (Stratton et al. 1979; Jennings and Dimond 1988; Pettersson 1996; Schowalter 1995; Schowalter and Ganio 1998; Halaj et al. 2000; Thunes et al. 2003).

Spider assemblage composition differed significantly between sugar maple and American beech canopies. Compositional differences of the canopy assemblages may be related to ecological and physical differences between sugar maple and American beech (e.g., bark type, texture, architecture, overall tree health). Compositional differences could also result from different regional abundances in sugar maple and American beech within our sampling area. Regional tree abundance may affect arboreal arthropod diversity associated with a tree species (Kennedy and Southwood 1984; Southwood et al. 2005), and the diversity and composition of canopy arthropods can change significantly between deciduous tree species (e.g., Brierton et al. 2003; Moran and Southwood 1982; Kennedy and Southwood 1984; Southwood et al. 2005).

In contrast to our findings in the canopy, the composition of spider assemblages associated with understorey saplings of American beech and sugar maple were similar.

This may relate to the more stable climate found in the understorey and the absence of beech bark disease on saplings of American beech (Le Guerrier et al. 2003). Also,

47 saplings of both species have similar plasticity in their crown architecture (Takahashi and

Lechowicz 2008) minimizing potential structural differences that could influence spider composition.

Several spider species were more commonly sampled in the understorey, and their life histories can explain this distribution. The higher abundance of the Dolomedes tenebrosus Hentz (Pisauridae) can be explained by its association with ground-level wet habitats (Dondale and Redner 1990). Enoplognatha ovata (Clerck), an introduced species, was significantly more abundant in the understorey. It builds a web on a single leaf and the literature mentions that it is associated with understorey foliage (Brierton et al. 2003). The jumping spiders Eris militaris (Hentz) and Pelegrina proterva

(Walckenaer) are foliage dwellers, typically inhabiting shrubs and trees (Richman 1989;

Maddison 1986; 1996; Dondale 1961).

In this study we described the canopy spider assemblages associated with temperate hardwood forests and showed that this fauna is distinct compared to the understorey. We detected differences in the spider assemblages associated with the canopy of each tree species but not in the understorey saplings. Our work represents the first step towards unraveling the mechanisms governing canopy spider diversity in north-temperate forests.

A few studies (e.g., Gering et al. 2003; Progar and Schowalter 2002; Lindo and

Winchester 2006) have already addressed these issues in part and generate highly relevant and complementary information to ground level knowledge on regional species

48 dynamics. We reinforce the relevance of including canopy research when providing an accurate understanding of temperate hardwood forest biodiversity.

49 3.7 Acknowledgements

The authors would like to thank K. Robert, K. Brochu, K. Aikens, B. Schroeder, Z.

Sylvain, J. Bowden, and J.F. Aublet for their relentless effort and dedication over two summers of field and laboratory work. We also thank Dr. C. Dondale for assistance with spider identification and Dr. P. Mason from the Canadian National Collection for support. We thank the Centre d'etude de la foret for its support. The research was funded by the Fonds Quebecois de Recherche en Nature et Technologies (FQRNT) to ML, the

National Science and Engineering Research Council of Canada (NSERC) (discovery grant to CMB), the Canadian Foundation for Innovation New Opportunities Grant

(Project #9548, to CMB), and the Department of Natural Resource Sciences (McGill

University). Finally, we thank John Spence and anonymous reviewers who helped improve earlier drafts of the manuscript.

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Southwood, T. R. E., V. C. Moran, and C. E. J. Kennedy. 1982. The Richness, Abundance and Biomass of the Arthropod Communities on Trees. Journal of Animal Ecology 51:635-649.

Southwood, T. R. E., G. R. W. Wint, C. E. J. Kennedy, and S. R. Greenwood. 2005. The composition of the arthropod fauna of the canopies of some species of oak (Quercus). European Journal of Entomology 102:65-72.

Stratton, G. E., G. W. Uetz, and D. G. Dillery. 1979. Comparison of the Spiders of 3 Coniferous Tree Species. Journal of Arachnology 6:219-226.

56 Takahashi, K. and M. J. Lechowicz. 2008. Do interspecific differences in sapling growth traits contribute to the co-dominance of Acer saccharum and Fagus grandifolia? Annals of Botany 101:103-109.

Thunes, K. H., J. Skarveit, and I. Gjerde. 2003. The canopy arthropods of old and mature pine Pinus sylvestris in Norway. Ecography 26:490-502.

Turnbull, A.L. 1960. The spider population of a stand of oak in Wytham Wood, Berks, England. The Canadian Entomologist 92:110-124.

Ubick, D., P., Paquin, P.E., Cushing, and V. Roth. 2005. Spiders of North America: An identification manual. American Arachnological Society, Keene, NH.

Vance, C. C, K. R. Kirby, J. R. Malcolm, and S. M. Smith. 2003. Community composition of longhorned beetles (Coleoptera : Cerambycidae) in the canopy and understorey of sugar maple and white pine stands in south-central Ontario. Environmental Entomology 32:1066-1074.

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57 3.9 Tables

Table 3.1: Number of individuals and species sampled during the 2005 and 2006 sampling seasons in the canopy and understorey of American beech and sugar maple trees in sugar maple forests of southern Quebec, Canada. Numbers in brackets represent the percentages of juveniles while numbers in parentheses represent the number of singleton species.

Individuals Species

Canopy Understorey Total Canopy Understorey Total

Maple 2005 1215 [90] 2987 [92.4] 4202 [91.7] 27(12) 43(12) 51 (15)

Maple 2006 807 [81.5] 2078 [78.2] 2885 [79.2] 31 (14) 50(16) 55(18)

Maple Total 2022 [86.5] 5065 [86.6] 7087 [86.6] 40 (18) 62(21) 65 (19)

Beech 2005 1157 [92.6] 3107 [92.1] 4264 [92.2] 26(6) 39(12) 45(15)

Beech 2006 681 [79.7] 1637 [77.6] 2318 [78.2] 29(13) 44(7) 55(15)

Beech Total 1838 [87.8] 4744 [87.1] 6582 [87.3] 37 (14) 53 (12) 69 (17)

Total 3860 [87.2] 9809 [86.8] 13669 [87.0] 48(17) 72(24) 82(23)

58 Table 3.2: Results from a three way non-parametric permutational multivariate ANOVA with sampling height, tree type and year representing the 3 factors being tested against spider species composition found at each sampling location in southern Quebec sugar maple forests. Each unit of replication represents the pooled sampling effort within each year. (MC) = Monte-Carlo randomization.

Source df F P(MC)

Tree 1.8289 0.1947

Height 70.3618 0.0001

Year NA NA

Tree x Height 2.4592 0.0253

Tree x Year 1.4299 0.3067

Height x Year 24.4362 0.0001

Tree x Height x

Year 1 0.4368 0.9251

Residual 352

Total 359

59 Table 3.3: Results from 2-factor ANOVAs on the effect of sampling height and tree species on the most collected spiders from sugar maple and American beech canopy and understorey in three study sites in SW Quebec, (df = 1,1, 356). Letters "a" and "b" indicate

significant differences between canopy and understorey. Letters "c" and "d" indicate significant differences between tree species.

Family Species Beech Maple Height Tree Height x Tree

Understorey Canopy understorey Canopy F-ratio P F-ratio P F-ratio P

Araneidae Araneus marmoreus Clerck 1.1 ± 1.18 a 0.04 ±0.21 0.98 ±1.01 a 0.07 ±0.25 75.48 0 0.009 0.92 0.08 0.78

Araniella displicata (Hentz) 1.27± 1.99 a 1.16*1.35 2.13±3.19ac 4.53 ± 4.89 bd 9.12 0.003 30.64 0 10.88 0.001

Cyclosa conica (Pallas) 1.24± 1.68a 0.71 ±1.29 1.71 ±2.6a 0.6 ±0.94 14.41 0 0.67 0.41 1.78 0.18

Dictynidae Emblyna sublata (Hentz) 59.24 ±46.02 a 9.38 ± 16.89 59.2±51.16a 5.4 ±7.07 137.84 0 0.14 0.71 0.27 0.61

Linyphiidae Ceraticelus fissiceps (O.P-C.) 1.58 ±2.44 a 0.02 ±0.15 1.33 ±3.4 a 0.07 ±0.25 30.81 0 0.091 0.76 0,22 0.64

Pityohyphantes costatus (Hentz) 5.69 ±4.19 a 0.13±0.5 6.47 ±5.72 a 0.09 ±0.29 139.63 0 0.72 0.4 0.88 0,35

Philodromidae Philodromns rufas vibrans Dondale 7.8 ±6.61 6.82 ±4.56 9.27 ± 7.76 c 9.71 ± 5.72 c 0.01 0,92 8.06 0.005 1.05 0.31

Pisauridae Dolomedes tenebrosiis Hentz 0.96 ±2.34 a 0.07 ± 0.45 2 ±3.95 a 0.02 ±0.15 18.69 0 2.28 0.13 2,7 0.1

Salticidae Eris militaris (Hentz) 4.56 ±8.02 a 0.8 ±1.36 3.91 ±6.86 a 0.58 ±1.18 34.68 0 0.52 0.47 0.12 0.73

Hentzia mitrata (Hentz) 0.44 ± 1.12 10.49 ± 6.39 b 0.93 ± 1.34 11.24 ± 6.99 b 196.28 0 0.1 0.32 0.11 0,74

Pelegrina proterva (Walckenaer) 3.56 ±4.24 a 1.84 ± 1.74 3.91 ±4.66 a 1.38 ± 1.75 24.77 0 0.003 0.96 0.89 0,35

Tetragnathidae Tetragnatha versicolor Walckenaer 2.02 ±3.69 2.18 ± 3 35 3.27 ± 5.8 c 4.16±5.58c 0.99 0.32 8.66 0.003 0.52 0.47

Theridiidae Enoplognatha ovata (Clerck) 4.64 ±5.47 a 0.11 ±0.32 4.58 ±5.03 a 0.02 ±0.15 79.54 0 0.02 0,88 0 0,98

Theridion lyricum Walckenaer 1.33 ± 1.82 ac 0.02 ±0.15 bd 0.73 ±1.03 a 0.04 ±0.21 39.3 0 3.28 0.071 3.8 0.05

Theridion murarium Emerton 3.44 ±3.33 5.8 ± 6.84 b 4.13 ±4.52 4.8 ± 5.29 b 4.72 0.03 0.02 0.9 1.36 0.25

Thomisidae Xysticus elegans Keyserling 1.18 ± 1.03 0.09 ±0.36 0.91 ± 1.08 c 0.02 ±0.15 1.84 0.18 64.78 0 0.66 0.42

60 >o 3.10 List of figures captions

Fig. 3.1: Rank-abundance curves for spiders collected in the understorey and canopy of sugar maple and American beech trees in sugar maple forests of southern Quebec,

Canada during the 2005 and 2006 sampling seasons. O = observed species counts; — = fitted values of the best fit model.

Fig. 3.2: Rarefaction estimates (Coleman curves) of expected species richness (mean ±

SD) for spiders collected in the canopy and understorey of sugar maple and American beech trees in sugar maple forests of southern Quebec, Canada during the 2005 and 2006 sampling seasons. For clarity, every fourth point from every curve is displayed on the graph.

Fig. 3.3: Two-factor nonmetric multidimensional scaling (NMDS) scatterplot of spider assemblages sampled in the canopy and the understorey of sugar maple and American beech trees in sugar maple forests of southern Quebec. Each sample is coded according to the tree type and the height (B=A.beech; M= S.maple; U=Understorey, C=Canopy).

Ordination stress = 18.05

62 Fig. 3.1

Beech canopy Maple canopy

63 Fig. 3.2

1000 2000 3000 4000 5000 Number of Individuals

64 Fig. 3.3

10r

oo h-'

CM 0 c/) X < • Beech Canopy ° Beech Understory A Stress = 18.05 Maple Canopy A Maple Understory -10L -10 -5 0 5 10 AXIS1 (44.7 %)

65 3.11 Appendices

Appendix 3.1

Pooled number of individuals and species sampled during the 2005 and 2006 sampling seasons in the canopy and understorey of American beech and sugar maple trees in sugar maple forests of southern Quebec, Canada. Species in bold were tested in a two-way

ANOVA with height (canopy vs. understorey) and tree species (s.maple vs. A.beech) as the two factors.

American beech Sugar Maple Total

Family Species Understorey Canopy Understorey Canopy

Agelenidae Agelenopsis potteri (Blackwall) 16 0 23 0 39

Agelenopsis utahana (Chamb. & Iv.) 5 0 11 1 17

Araneidae Araneus corticarius (Emerton) 0 0 1 0 1

Araneus diadematus Clerck 6 5 15 2 28

Araneus guttulatus (Walckenaer) 0 1 1 3 5

Araneus marmoreus Clerck 49 2 48 4 103

Araneus saevus (L. Koch) 42 3 39. 5 89

Araniella dispticata (Hentz) 57 52 97 210 416

Cyclosa conica (Pallas) 56 32 77 27 192

Eustala anastera (Walckenaer) 8 12 8 14 42

Larinioides cornutus (Clerck) 0 0 1 0 1

Larinioides patagiatus (Clerck) 0 1 0 1 2

Larinioides sclopetarius (Clerck) 0 0 1 1 2

Mangora placida (Hentz) 3 0 7 0 10

Neoscona arabesca (Walckenaer) 7 6 2 2 17

Clubionidae Clubiona canadensis Emerton 4 0 1 0 5

Clubiona obesa Hentz 0 3 1 1 5

Clubiona pygmaea Banks 0 0 0 1 1

Clubiona spiralis Emerton 16 0 9 0 25

Dictynidae Emblyna maxima (Banks) 6 0 6 0 12

66 Emblyna sp 1

Emblyna sublata (Hentz)

Linyphiidae Agynela serrata (Emerton)

Agyneta sp. 1

Agyneta unimaculata (Banks)

Aphileta misera (O.P.-C.)

Bathyphantes sp. I

Ceraticelus fissiceps (O.P-C.)

Drapestica aheranda Chamber! in

Erigone atra Blackwall

Glyphesis scopulifer (Emerton)

Gonatium crassipalpum Bryant

Halorates plumosus (Emerton)

Helophora insignis (Blackwall)

Hypselistes florens (O.P.-C.)

Kaestnariapullata (O.P.-C.)

Kaestnaria rufula (Hackman)

Linyphiidae sp. 1

Linyphiidae sp. 2

Linyphiidae sp. 3

Linyphiidae sp. 4

Mastophora hutchinsoni Gertsch

Neriene radiata (Walckenaer)

Pityohyphantes costatus (Hentz)

Lycosidae Hogna sp. 1 (Juv)

Pirata minutus Emerton

Trochosa sp. 1 (juv.)

Mimetidae Mimetus notius Chamberlin

Philodromidae Philodromus praelustris Keyserlin

Philodromus rufus vibrans Dond

Philodromus vulgaris (Hentz)

Pisauridae Dolomedes tenebrosus Hentz

Salticidae Eris militaris (Walckenaer)

Hentzia mitrata (Hentz)

Maevia inclemens (Walckenaer) Pelegrina proterva (Walckenaer) 160 83 177 64 484

Tutelina sp. 1 (juv.) 0 1 0 0 1

Tetragnathidae Tetragnatha laboriosa Hentz 3 1 1 2 7

Tetragnalha sp. 1 0 0 0 1 1

Tetragnatha slraminea Emerton 1 0 0 0 1

Tetragnatha versicolor Walckenaer 91 98 148 192 529

Theridiidae Achaearanea tabulata Levi 1 1 2 0 4

Argyrodes trigonum (Hentz) 1 0 14 0 15

Crustulina sticta (O.P.-C.) 0 0 . 1 0 1

Dipoena nigra (Emerton) 20 1 31 0 52

Enoplognatha ovata (Clerck) 209 5 206 1 421

Steatoda borealis (Hentz) 1 0 0 0 1

Theridiidae sp. \ 1 0 0 0 1

Theridiidae sp. 2 1 0 0 0 1

Theridion alabamense Gert. & Ar. 0 0 3 0 3

Theridion albidium Banks I 0 0 0 1

Theridion differens Emerton 0 0 1 0 1

Theridion glaucescens Becker 0 0 1 1 2

Theridion lyricum Walckenaer 60 1 33 2 96

Theridion murarium Emerton 155 261 188 220 824

Theridula emertoni Levi 0 0 1 0 1

Theridiosomatidae Theridiosoma gemmosum (L. Koch) 3 0 0 0 3

Thomisidae Misumena vatia (Clerck) 0 2 2 0 4

Misumenops asperatus (Hentz) 0 0 0 1 1

Tmarus angulatus (Walckenaer) 7 0 4 0 11

Xysticus elegans Keyserling 53 4 41 1 99

Uloboridae Uloborus g/omosus (Walckenaer) 4 0 6 0 10

Total 4744 1838 5065 2022 13669

68 3.12 Connecting statement

Chapter 3 demonstrate that spider assemblages from the canopy and understorey of sugar maple and American beech trees are different in north-temperate hardwood forests.

Different distribution models best fit RADs from both habitat and indicate a less stable habitat in the canopy. Both habitats contain dominant species that are significantly associated with them. I use the results from Chapter 3 that suggest differences in habitat conditions between the canopy and understorey habitats, and the results that identify spider species significantly associated with each habitat to build the hypotheses and predictions I test in Chapter 4. Chapter 4 investigates the importance of habitat conditions and life history traits on the propensity to balloon of north-temperate hardwood forests.

69 4. Ballooning propensity of canopy and understorey spiders in a north-

temperate hardwood forest

Maxim Larrivee and Christopher M. Buddie

Department of Natural Resource Sciences, McGill University, 21,111 Lakeshore Road,

Saint-Anne-de-Bellevue, Quebec, Canada, H9X 3V9

Original paper to be submitted to Ecological Entomology (Winter 2009)

70 4.1 Preface

Spider ballooning propensity has been investigated only for species of open and disturbed habitats and never with forest or canopy spiders. Ballooning propensity is a fascinating behavioural trait of spiders and the adaptive links it has with life history traits and habitat conditions make it an important research area. Knowledge of the drivers of ballooning propensity leads to a better understanding of spider dispersal capacity and potentially of spider diversity patterns. The originality of this paper resides in being the first test of the ballooning propensity of multiple spider species across many families in mature forest and old-growth forest canopy habitat. The results show that the unstable canopy habitat does not affect spider ballooning propensity differently than in the understorey habitat.

Small size web-building spiders from the RTA and Orbicularia clades have the highest propensity to balloon in a forested habitat, regardless of the vertical habitat stratification.

The results support the mixed evolutionarily stable strategy theory and reject the possibility of risk-spreading as an explanation for the dispersal strategy of canopy spiders. The information gathered in this paper will be of interests to spider ecologists and evolutionary ecologists. The influence of life history traits on the propensity of spiders to express a dispersal strategy will be of particular interest.

71 4.2 Abstract

Species found at high densities usually have high dispersal rates and increased fitness in unstable habitats. Theories about bet-hedging (risk spreading) strategy and mixed evolutionarily stable strategies are often used to explain high dispersal rates in organisms.

Spiders frequently disperse and colonize habitats through ballooning, a passive aerial dispersal process. Our main objective was to identify life history traits and environmental factors that influence ballooning propensity in spiders, using spiders from the foliage of the canopy and understorey of a north-temperate hardwood forest as a model system.

Individual spiders were brought into a laboratory to test their propensity to balloon, and we assessed the influence of body size, sex, development stage, hunting strategy, and phylogenetic background on this dispersal trait. A generalized mixed linear model indicated that small-sized web-building spiders from the RTA and Orbicularia clades had the highest propensity to balloon, whereas habitat stability (i.e., canopy compared to understorey) did not relate strongly to ballooning propensity. Species level models showed that small body size of juveniles had a strong effect on ballooning for species with large-bodied adults while individuals of small-bodied species initiated ballooning regardless of size, habitat or development stage. We found a negative correlation between the relative abundance of spiders and the ballooning frequency of foliage spiders from the understorey and the canopy. Our results support use of the mixed evolutionarily stable strategy as an explanation for ballooning propensities in canopy and understorey spiders but do not support bet-hedging as relevant to the dispersal strategy of canopy spiders.

72 Keywords Dispersal • Araneae • Habitat stability • AIC • Evolutionarily Stable Strategy

Risk-spreading

73 4.3 Introduction

Bet-hedging theory validates the adaptive value of spreading risk through dispersal for habitat generalist species (Denboer 1990). Under this view, species living in unstable habitats can spread risk by producing large numbers of individuals over space and time

(Hopper 1999; Kisdi 2002). In contrast, the concept of Evolutionarily Stable Strategies

(ESS) follows the game theory concept (Smith and Price 1973), and can also explain differences in intra-specific dispersal frequencies. Individuals within a population have different but equally successful dispersal behaviors (potentially ranging from none to full dispersal) to resolve contests over use of habitat based resources such as space or food

(Weyman et al. 2002). In a mixed ESS the dispersal behaviors adopted by each individual can be viewed as a fixed probability distribution or one that changes in time and is influenced by biotic and abiotic factors (Bell et al. 2005). Studies of spider ballooning frequencies have lent support to both ESS and bet-hedging theories linking variability in the propensity for passive dispersal with increased fitness (Weyman et al. 2002; Bonte et al. 2003b; Belled/. 2005).

Evaluating the influence of various biotic (body size, developmental stage, sex, phylogeny, feeding strategy, habitat specialization) and abiotic (habitat stability, connectivity, predictability, and seasonality) factors on the ballooning propensity of spiders can help explain how dispersal ability influences species distribution patterns at multiple spatial scales within a metacommunity framework. It is predicted that species with high dispersal capacity are less prone to local extinctions while populations of those with low dispersal power go locally extinct more frequently across the metacommunity

74 (Gonzalez etal. 1998; Leibold etal. 2004). Consequently, species assemblages with low dispersal capacity show low a-diversity and high P-diversity (Mouquet and Loreau 2003).

Members of three orders of arthropods (Araneae, Acari and Lepidoptera) can disperse using a passive aerial dispersal method involving silk (i.e., ballooning) (Bell et al. 2005).

Ballooning is risky behavior, as the individuals can not control where they land. Many frequent ballooners are good colonizers and pioneer species (Si.mberloff 1981; Edwards

1988). Ballooning happens over short (Meijer 1977; Heidger and Nentwig 1989; Toft

1995) and long distances (Glick 1939; Bishop and Riechert 1990). The factors influencing ballooning propensity can also help explain how ballooning contributes to a species' success in different or patchy habitats. For example, Bonte et al. (2003b; 2006) showed that habitat specialists have lower ballooning propensities than generalists, while habitat connectivity increased ballooning propensity. Some species can also be good colonizers because of their ability to establish themselves in a habitat and maintain persisting populations. Non-dunal xerothermic species increase species richness in sand dunes through short distance dispersal from adjacent source populations (Bonte et al.

2003a).

The dispersal ability and certain life history traits of a species can be modulated by the habitat they live in, its size, and connectivity (Bonte et al. 2006; 2007; Bonte and Lens

2007). In certain cases, life history traits can have more influence than the habitat on dispersal ability (Richter 1970; Bonte et al. 2003b). Ballooning can be a response to overcrowding or low resources (Legel and van Wingerden 1980; Morse 1993; Weyman and Jepson 1994). Higher ballooning frequency within a population is linked to

75 phenology in large spider species where body size limits ballooning as adults (Roff

1991). High ballooning frequencies are favorable to individuals living in unstable or ephemeral habitats (Southwood 1962; Greenstone 1982; Weyman etal. 1995; Samu,

Sunderland & Szinetar 1999), and to individuals that are habitat generalists (Richter

1970; Bonte et al. 2003b). The predictable temporal variability of a habitat (seasonality, periodical flooding) can also trigger increases in ballooning (Greenstone 1982).

Ecosystems with well known spider faunas associated with different habitat types are excellent templates for study of environmental variables and life history traits leading to ballooning.

Although some work has been done on ballooning within a family or genus of spiders

(e.g., Richter 1970; Weyman et al. 1995), little has been done, especially with Nearctic spiders, to examine the effects of habitat and life history traits on ballooning propensity of multiple spider species across many families (see Bonte et al. 2003b for a treatment of

European fauna). Most importantly the ballooning propensity of forest spiders has never been documented. The canopy and understorey of north-temperate hardwood forests in eastern North America is a suitable model system to investigate effects of habitat and life history traits on the ballooning propensity of spiders. These forests are climatically contrasting habitats due to the short term (daily) and long term (seasonal) fluctuations in light, temperature, moisture, and wind that characterize the canopy in contrast to a more stable understorey (Lowman and Wittman 1996; Fagan et al. 2006). Variations in wind conditions influence ballooning propensity (Bonte et al. 2007). The foliage spider fauna

76 is well known In this system, and previous work has illustrated strong stratification in spider assemblages between the canopy and the understorey (Larrivee and Buddie 2009).

Patterns in diversity show a differing dominance structure between the canopy and the understorey, likely echoing differences in habitat stability and colonization patterns between these habitats (Larrivee and Buddie 2009). The objectives of our research were to 1) compare the ballooning propensity of canopy and understorey spiders sampled from a north temperate hardwood forest; and 2) assess the influence of biotic and abiotic factors on ballooning propensity. We predicted that ballooning propensity will be higher for individuals from the canopy due to instability in various environmental factors; and that small sized individuals from abundant species would balloon more frequently, as previously documented (Humphrey 1987; Roff 1991). We predicted that web-builders would also show a higher propensity to balloon than hunters because increased silk production is correlated with higher ballooning propensity (Bonte et al. 2003b).

4.4 Materials and methods

4.4.1 Field sampling

Between May 10 and September 24, 2007, foliage spiders were sampled in the canopy of mature trees and understorey saplings (six on average) of both sugar maple {Acer saccharum Marsh.) and American beech (Fagus grandifolia Ehrh.) in three hardwood stands of the Morgan Arboretum, Sainte-Anne-de-Bellevue, Quebec, Canada (45°25'55"

77 N; -73°56'58" W). Canopy spiders were sampled in 12 dominant healthy trees in F. grandifolia and in A saccharum and understorey spiders were sampled on saplings of 3 m or less in height directly below the tree crowns sampled (see Larrivee and Buddie

(2009) for additional details about tree selection and canopy sampling). Spiders were sampled with a beating sheet and brought back to the laboratory immediately.

4.4.2 Laboratory experiment

In the laboratory the spiders were housed individually in 30 ml plastic containers with a piece of moist cotton to maintain humidity and prevent desiccation. They were fed live fruit flies {Drosophila melanogaster) and then left unfed for 7 days to control for hunger prior to experimentation. During this period the cotton was kept moist.

We tested ballooning propensity by placing each spider on a platform containing two climbing apparati (an entomological needle, 3.8 cm height, and an artificial plastic "tree",

5 cm height with a 5 cm long branch). The platform was surrounded by water to ensure the individual stayed on the platform (analogous design to that described by Bonte et al.

2003b). Pre-ballooning behaviors (tip-toe, suspended ballooning, and rafting; for detailed behavior description, see Bell et al. 2005) directly correlated with ballooning propensity

(Legel and van Wingerden 1980; Greenstone 1982; Bonte et al. 2003b) were recorded for three minutes without wind and three minutes with a wind speed of 0.85 meter per second. Wind speed, room temperature and humidity were recorded for the duration of each test with a portable air velocity meter (TSI® Model 8360) calibrated previously in a

78 wind tunnel. All spiders were tested under wind speed, humidity and temperature conditions that were conducive to ballooning to ensure that these environmental factors did not have a negative effect on the pre-ballooning behaviors of the individuals.

All individuals were identified to the lowest taxonomic level possible. For each individual, we measured its body size (mm) from the tip of the prosoma to the end of the abdomen (excluding the spinnerets), determined the sex for sub-adults and adults, recorded the sampling time (spring, summer, and fall), the habitat type (canopy or understorey), the feeding guild (hunter or web-builder), the developmental stage

(juvenile; includes all instars possible 1st to 5l instars, or adult) and its phylogenetic background (RTA or Orbicularia clade, taken from Bell et al. 2005)vBy controlling for hunger, wind speed, temperature, and humidity, we ensured the pre-ballooning behaviors observed in our laboratory experiment were linked to life history traits of the individuals and the habitat they were sampled in.

4.4.3 Data analyses

Data on the propensity to balloon were treated as a binomial response variable in a generalized linear mixed model (GLMM) with a Negative Binomial distribution. The

GLMM procedure was performed in R (R Development Core Team, 2008) with the package lme4 (Bates et al. 2008). We used the following parameters in our models to test for ballooning propensity: phylogenetic clade (RTA or Orbicularia), body size (mm), feeding guild (hunter or web-builder), habitat type (canopy or understorey), time of year

79 (spring, summer, fall), sex (male or female), and development stage (juvenile or adult).

Prior to analyses, we combined the clade and feeding guild parameters into one (RTA- hunter, RTA-web-builder, Orbicularia-web-builder) since no Orbiculate spider belonged to the hunter feeding guild. Bonte et al. (2003b) found that significant differences in ballooning propensity between species were due to phylogenetic background (RTA vs.

Orbicularia) and habitat specialization. As such, species identity (n = 29) is included as a random factor in the GLMM analysis. We also performed a generalized linear model analysis of our complete dataset excluding the variable species as a random factor to see how it affected the fixed factors in the GLMM analysis. Prior to the analyses, we standardized body size measurements by centering the values to their mean. We did not include wind speed, temperature and humidity parameters in the models since these parameters were controlled in the laboratory. We also analyzed a subset containing the

160 individuals for which we could determine sex.

We tested sets of GLM models with AICc for the most abundant foliage spiders of north temperate hardwood forests: Emblyna sublata (Hentz), Tetragnatha versicolor

Walckenaer, Philodromus rufus vibrans Dondale, and Theridion murarium Emerton.

GLM models were also tested for individuals of the families Salticidae and the genus

Clubiona (family Clubionidae) to maximize the number of replicates in the case of

Salticidae and because species determination in juveniles of the genus Clubiona was not possible. AIC is based on the principle of simplicity and parsimony, it allows multiple working hypotheses, and is based on strength of evidence (Anderson and Burnham 2002).

The relevant models and the parameters included in these models were based on previous

80 results from published literature and reviews in the field of spider ballooning (e.g.,

Weyman et al. 2002; Bell et al. 2005), and on our knowledge and experience with foliage spiders in north-temperate hardwood forests (Larrivee and Buddie 2009). Our models include all potential trait interactions as not all life history traits influence ballooning propensity independently (Appendix 1). For example, there is most likely a strong interaction between developmental stage and body size that affects ballooning propensity.

A complete list of the GLM models tested for the species-specific models is provided in

Appendix 1.

We used a multimodel inference (or model averaging) approach (Burnham and Anderson

2002; Mazerolle 2006) to test the parameters included in the models that had A/ < 2 when we could not select one model as the best representation of our observations. We determined which parameters had a strong influence on ballooning propensity by including model uncertainty (unconditional standard error (SE)) to the weighted averages of the estimate of each parameter (Mazerolle 2006). The weighted average of the estimates and the unconditional SE were used to determine the magnitude of the effect of the parameter on the propensity to balloon through 95% confidence intervals (CI). A parameter had a strong effect on the response variable if 0 was not included in the CI and the weighted regression coefficient fell inside the CI.

Because longterm intraspecific overcrowding positively influences ballooning propensity

(Legel and van Wingerden, 1980; Morse 1993; Weyman and Jepson 1994), we tested the presence of an overcrowding effect on ballooning propensity of the most abundant

81 spiders. We did so through pair-wise Pearson correlations of their ballooning frequency and the relative abundance of each species in north-temperate hardwood forests. The relative abundance values were obtained from a dataset of foliage spiders sampled from three hardwood forests of southern Quebec (Larrivee and Buddie 2009). These sites were within a 60 kilometre radius of the Morgan Arboretum. Species-abundance distributions

(SADs) of north-temperate hardwood spiders do not change significantly at small spatial scales in southern Quebec (see Chapter 5). Also preliminary analyses of the spiders sampled at the Morgan Arboretum indicate SADs similar to those from the dataset used to derive each species' relative abundances.

4.5 Results

In total, 455 spiders (207 from the canopy; 248 from the understorey) were tested for tip­ toe, suspended ballooning, and rafting. Forty percent of the individuals tested (45 % in the canopy; 36 % in the understorey) exhibited pre-ballooning behaviors (Table 4.1).

Eight species represented by one individual were removed from our statistical analyses.

Our generalized mixed linear model indicated that the ballooning frequency did not differ between spiders sampled in the canopy and the understorey (Table 4.2). Increasing body size, however negatively affected ballooning propensity (Table 4.2). The mean body size

(±SE) of spiders that tiptoed was 2.3 ± 0.08 mm; spiders that did not tiptoe had a mean body size (±SE) of 3.1 ± 0.08 mm (Fig. 4.1). Web-builders from the Orbicularia and RTA phylogenetic clades showed a significantly positive tendency to balloon but not hunters

82 from RTA phylogenetic clade (Table 4.2). The variance added to the model by the random variable "species" was small but removed a significant positive effect of season and a negative interaction between body size and summer dispersing individuals (Table

4.2). Earlier analyses (results not showed) testing ballooning propensity multiple models using AICc and model averaging also identified body size and the interaction between phylogenetic background and feeding guild, and tests on generalized mixed linear model of a subset of the individuals for which we could determine sex indicated that males did not differ from females in ballooning propensity. Effects of the other parameters were very similar to those found with the full dataset analysis with body size having a marginally negative influence on ballooning propensity.

In species-specific GLM models, AICc and model averaging showed that habitat type did not have a strong effect on any of the species (Table 4.3). Emblyna sublata, T. versicolor, and T. murarium had high pre-ballooning behavior frequencies regardless of body size, development stage, habitat type and sampling period (Table 4.3). These three species had a high tiptoe frequency and a small body size (Table 4.1). Increasing body size had a negative effect on ballooning propensity for P. rufus vibrans and members of the genus

Clubiona (Table 4.3). Salticid spiders sampled during the summer tiptoed less frequently

(Table 4.3).

The most abundant foliage spider in north-temperate forests, E. sublata, had a high tiptoe frequency in both habitats. When it was removed from the Pearson correlation analysis, we found weak negative correlations between the relative abundance of spiders and their

83 propensity to balloon in the understorey (-0.23 without E. sublata in the analysis; 0.70 with E. sublata in the analysis) and the canopy (-0.35 without E. sublata in the analysis; -

0.15 with E. sublata in the analysis) (Fig. 4.2). A T-test comparing the canopy and understorey pre-ballooning behavior frequencies of the most abundant spiders was not significant (t-stat =-0.021, df 2,i6 ;p = 0.98).

4.6 Discussion

Our laboratory experiment on pre-ballooning behavior demonstrates that forest spiders can have high ballooning propensities and that spiders from the canopy and understorey of a north temperate hardwood forest have similar ballooning propensities. Thus, we reject the hypothesis that differences in habitat stability between the canopy and understorey significantly affect ballooning behaviors given our geographic and ecological context. Similar ballooning propensities of canopy and understorey spiders indicate that dispersal behaviors are distributed similarly among individuals along the ballooning propensity probability distribution in each habitat (Bell et al. 2005). This result is somewhat surprising since the canopy habitat represents a less stable environment than the understorey: larger short term (daily) and long term (seasonal) fluctuations in light, temperature, moisture, and wind characterize the canopy compared to the understorey

(Lowman and Wittman 1996; Fagan et al. 2006). These environmental differences are also supported by a strong stratification in spider assemblages between the canopy and the understorey of north-temperate hardwood forests (Larrivee and Buddie 2009). The diversity patterns and the dominance structure of the canopy assemblages are also

84 characteristic of an unstable habitat, while the diversity and the higher evenness of the understorey assemblages is more typical of stable habitats (Larrivee and Buddie 2009).

The similar ballooning propensities in canopy and understorey spiders, despite the different environmental conditions in each habitat, suggest the presence of a mixed evolutionary stable strategy (i.e. with respect to dispersal, in this case is maintained at similar frequencies in both habitats) in the dispersal mode of the populations in each habitat for the following three reasons: 1) the habitat types had a similar effect on ballooning propensity in all our single species models and our full model; 2) there were no differences between the ballooning frequencies of the canopy and understorey populations of the most abundant species; 3) the negative correlation between relative abundance and ballooning frequency of the most abundant spiders was similar in the canopy and the understorey. Similar variability in ballooning propensity was observed between food deprived and satiated spiders leading (Weyman and Jepson 1994; Weyman et al. 1995) to suggest mixed ESS as the explanation for this similar variability in both treatments. These three elements of our results also allow us to conclude that there is no evidence of increased risk spreading (Hopper 1999) in canopy spider populations compared to the understorey populations. Evidence of risk-spreading would be represented by higher ballooning frequencies in canopy spiders to compensate for the less predictable nature of their habitat.

Regular movement of individuals between both habitats could explain the similar ballooning propensities in populations living in the canopy and understorey. The canopy

85 foliage habitat of temperate forests is thought to be recolonized every spring mostly by local dispersal from the understorey (Larrivee and Buddie 2009), creating a flux of individuals between the two habitats. Hence, similar ballooning propensities in both habitats even though these habitats differ in the short term predictability of their environmental conditions suggest that other factors are at play.

In our study, spiders with a body size less than 2.4 mm were more likely to balloon compared to larger-bodied spiders. Our species-specific models also detected a strong negative influence of increasing body size on ballooning propensity. This supports our initial prediction that small sized individuals have higher ballooning frequencies. Our results also support findings from other studies about the negative effect of increasing body size on ballooning (Humphrey 1987; Greenstone et al. 1987; Roff 1991). With few exceptions (see Greenstone et al. 1987; Schneider et al. 2001), it is well demonstrated that there are biomechanical constraints limiting ballooning by large spiders (> 3 mm)

(Humphrey 1987; Roff 1991). Roff (1991) points out that the mean size of ballooning

British spiders is 2.07 mm for species that balloon as adults and 2 mm for species where only juveniles balloon. The mean body size (2.31 mm ± 0.08 mm) of ballooning individuals in our dataset strongly supports Roff s (1991) findings and is in agreement with the theoretical values of Humphrey (1987). We also show that species maintaining small body sizes as adults (e.g., T. murarium, and E. sublata) have similar ballooning propensity as immatures and adults. In contrast, increasing body size had a strong negative effect on individuals of P. rufus vibrans and of the genus Clubiona; individuals of these species have larger body size as adults. An exception is T. versicolor; the

86 ballooning frequency of this species was not affected by increasing size but perhaps more by its web-building feeding strategy.

We show that the feeding strategy of web-building has a positive effect on ballooning propensity for spiders. This indicates that ballooning, while deeply rooted in spider phylogeny (Bonte et al. 2003b), is a highly plastic behavioral trait strongly influenced by feeding strategies such as hunting and web-building; these life history traits are common within both the Orbicularia and RTA phylogenetic clades. Ballooning propensity can be influenced predominantly by factors other than habitat stability such as habitat rarity

(Richter 1970) and the degree of habitat specialization of a species (Bonte et al. 2003b).

Habitat size and connectivity can also affect the propensity to balloon (Bonte et al. 2006).

Thus, factors such as feeding strategy and body size can have a stronger influence on ballooning propensity of canopy and understorey spiders than habitat effects.

Ballooning is thought to play an important role in the annual recolonization of the canopy of north temperate hardwood forests (Larrivee and Buddie 2009). However, only T. murarium and E. sublata (pioneer species in the canopy) have a high ballooning propensity. In contrast, the hunting spiders Hentzia mitrata (Hentz) (the most abundant spider in north-temperate hardwood canopies) and P. rufus vibrans Dondale another abundant species have lower ballooning propensity. This suggests that these hunting species, in the short term, colonize the canopy by cursorial means, a finding documented for the hunting spider Pardosa monticola (Clerck) (Lycosidae) in European coastal dune grasslands (Bonte et al. 2003a). They may also overwinter in the canopy beneath the bark

87 as they were both found, along with T. murarium, in high abundance on trunks in the canopy (Chapter 5). Furthermore, P. rufus vibrans and H. mitrata have larger bodied adults, thus generally ballooning as early instar juveniles. Younger instars of spiders mostly balloon in overcrowded conditions near the egg sac and rather than for colonizing

(Miller 1984; Morse 1993). Ballooning in young instars also diminishes the likelihood of cannibalism (Morse 1993). However, ballooning can still be a successful colonization strategy over longer periods of time (Bonte et al. 2003a).

Overcrowding has been suggested to influence ballooning propensity (Weyman et al.

1995; Legel and Van Wingerden 1980). In our study, we found a small negative correlation between ballooning propensity and regional relative abundance of all abundant spiders found in the canopy and the understorey of north temperate hardwood forests with the exception of E. sublata. This suggests that, aside from E. sublata populations, the populations of these common foliage spiders of north-temperate hardwood forests are not saturated or overcrowded. E. sublata's high ballooning propensity probably uses a habitat foraging technique similar to the one documented for

Dictyna arundinacea (Linnaeus) in agricultural lands (Heidger and Nentwig 1989).

Individuals of D. arundinacea were observed routinely performing small ballooning events (10cm to several meters) inside their local environment before settling in one spot.

In conclusion, ballooning propensity is influenced by a combination of factors that may not be primarily driven by habitat stability or deeply anchored in phylogeny. There is evidence that dispersal behaviour in foliage spiders of north-temperate hardwood forests results from a mixed ESS and that canopy spider populations are not likely spreading risk with increased ballooning frequencies compared to understorey populations. Life history traits such as feeding strategy and body size can have stronger effects on ballooning propensity than habitat stability. This new information on the various factors influencing ballooning propensity of foliage spiders of north-temperate hardwood forest could contribute to predict the ecological outcomes of spider ballooning events. With regards to

ESS, our results on body size and feeding guild could help future work to estimate the shape of the probability distributions for ballooning propensity. Bell et al. (2005) define ballooning propensity as a behavior shaped by internal and external stimuli linked to a fixed internal probability distribution or one that changes in time. Our results with regards to body size and feeding guild can also be used to predict diversity patterns across space. For example, species sharing similar body size and feeding attributes favoring high dispersal rates can maintain populations over large spatial scales within a particular habitat. On the other hand, species sharing attributes reflecting low dispersal power such as large bodied hunting spiders are more vulnerable to habitat fragmentation and local population extinctions (Den Boer 1990; Bonte et al. 2004).

4.7 Acknowledgements

We thank J.F. Aublet, C. Frost, and K.R. Aikens for their help in the field and in the laboratory. We thank the Morgan Arboretum staff for granting access to their forest, M.

Mazerolle from the Centre d'Etude de la Foret, and Ian Strachan for kindly providing laboratory equipment. The research was funded by the Fonds Quebecois de Recherche en

Nature et Technologies (FQRNT) to ML, the National Science and Engineering Research

89 Council of Canada (NSERC) (discovery grant to CMB), the Canadian Foundation for

Innovation New Opportunities Grant (Project #9548, to CMB), and the Department of

Natural Resource Sciences (McGill University). The research and experiments performed in this study comply with current Canadian laws.

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94 4.9 Tables

Table 4.1

Species tested for ballooning propensity. All individuals tested were collected at the

Morgan Arboretum, Quebec, Canada. Clade: RTA = Retro Tibial Apophysis, ORB =

Orbicularia; Feeding guild: Web = Web-builder, Hunter = Hunter.

Feeding Ballooning Mean body size Clade Family Species name n guild frequency (cm ± SE)

RTA Web Agelenidae Agelenopsis sp. 3 0.57 ±0.10

Web Agelenopsis potteri (Blackwall) 2 0.73 ± 0

ORB Web Araneidae Araneidae undet. 0.67 6 0.39 ±0.03

Web Araneus marmoreus Clerck 0.29 7 0.26 ±0.03

Web Araneus saevus (L. Koch) 0 1 0.14±0

Web Araniella displicata (Hentz) 0.50 6 0.34 ±0.09

Web Cyclosa conica (Pallas) 0.41 17 0.29 ± 0.04

Web Eustala sp. 0 2 0.25 ± 0.01

Web Larinioides cornutus (Clerck) 0 3 0.48 ± 0.20

RTA Hunter Clubionidae Clubionasp. 0.41 36 0.39 ±0.04

Hunter Clubiona spiralis Emerton 0 1 0.72 ± 0

RTA Web Dictynidae Dictynidae undet. 0.75 4 0.14 ±0.05

Web Emblyna sublata (Hentz) 0.85 57 0.21 ±0.01

95 ORB Web Linyphiidae Linyphiidae 0 1 0.11 ± 0

Web Erigone atra Blackwall 1 1 0.2 ±0

Web Neriene radiata (Walckenaer) 1 1 0.22 ± 0

Web Pityohyphantes costatus (Hentz) 0.33 9 0.36 ± 0.02

RTA Hunter Philodromidae Philodromus sp. 0.26 23 0.21 ±0.03

Hunter Philodromus rufus vibrans Dondale 0.29 49 0.19 ±0.01

RTA Hunter Pisauridae Dolomedes tenebrosus Hentz 0.26 ±0

RTA Hunter Salticidae Eris militaris (Hentz) 0.07 44 0.38 ± 0.02

Hunter Hentzia mitrata (Hentz) 0.13 39 0.35 ± 0.03

Hunter Maevia inclemens (Walckenaer) 0 5 0.88 ± 0.40

Hunter Pelegrina proterva (Walckenaer) 0.23 26 0.38 ±0.01

Hunter Synageles venator (Lucas) 0 1 0.23 ±0

ORB Web Tetragnathidae Tetragnatha sp. 7 0.29 ± 0.05

Web Tetragnatha versicolor Walckenaer 0.76 34 0.26 ± 0.03

ORB Web Theridiidae Argyrodes trigonum (Hentz) 1 5 0.22 ± 0.05

Web Dipoena nigra (Emerton) 0.67 3 0.14 ±0.01

Web Enoplognatha ovata (Clerck) 0.33 3 0.11 ±0

Web Theridion sp. 0.78 9 0.11 ±0

Web Theridion lyricum Walckenaer 0 1 0.14±0

Web Theridion murarium Emerton 0.54 37 0.17 ±0.01

Web Wamba crispulus (Simon) 0 1 0.38 ±0

RTA Hunter Thomisidae Misumenops sp. 0.21 ±0

96 Hunter Xysticus sp. 0.20 5 0.47 ± 0.05

Hunter. Xysticus elegans Keyserling 0 2 0.81 ±0.06

97 Table 4.2

Generalized linear mixed model (Negative Binomial) fit by the Laplace approximation of ballooning behavior according to habitat type, body size, sampling time, and the phylogenetic clade and feeding guild interaction*. Species identity** is included as a random factor. Clade*Guild: Phylogenetic clade (RTA or Orbicularia) interaction with

Feeding guild (Hunter or Web-builder): RTA*Hunter, RTA*Web-building,

Orbicularia* Web-building; Size: spider body size; Hab. type: habitat where spider sampled, understorey or canopy; TOY: time of year of sample, spring, summer, or fall.

Est. = estimate; SE = Standard error; SD = Standard deviation.

Fixed effects Est. SE P value Est. SE P value Intercept -0.677 0.520 0.193 Intercept -0.718 0.3738 0.055 Body size -2.942 1.219 0.016 Body size -2.2663 1.0532 0.031 Understorey 0.300 0.270 0.266 Understorey 0.2456 0.2445 0.315 Spring -1.029 0.729 0.158 Spring -1.0315 0.6712 0.124 Summer 0.866 0.614 0.158 Summer 1.1361 0.5364 0.034 RTA.WEB 2.291 0.841 0.006 RTA:WEB 2.877 0.4109 0.000 ORB WEB 1.655 0.458 0.000 ORB:WEB 1.6348 0.2451 0.000 size:spring 2.602 1.846 0.159 size:spring 1.756 1.7209 0.308 size:summer -2.879 2.188 0.188 size:summer -4.2502 1.9732 0.031

Random effects Variance SD Variance SD Species 0.657 0.811 - - * Species represented by at least 2 individuals were included in the model.

** Genus identity was used for immatures that could not be determined to species but were determined to belong to the same species for the following genera: Clubiona, Philodromus, Araneus, Theridion, and

Tetragnatha.

98 Table 4.3

Species specific AICc tests of the multiple linear regression models of ballooning behavior according to habitat type, body size, sampling time, and feeding guild following a binomial distribution model (negative binomial distribution model). K: number of parameters in the model; LL: log-likelihood; wi: AICc weight. Size: spider body size;

Weighted Reg. Coef.: Weighted regression coefficient; CI: Confidence Interval; Hab. type: habitat where spider sampled, understorey or canopy; TOY: time of year of sample, spring, summer, and fall; Tree: tree species sampled, sugar maple or American beech;

Dev.: developmental stage, juvenile or adult.

a) Emblyna sublata (Hentz): 57 individuals tested.

Model

Model ID K AICc Ai AICc LL wi

Hab. type 9 2 53.06 0.00 -24.42 0.29

Size 8 2 53.39 0.33 -24.58 0.24

Dev 7 2 53.60 0.54 -24.69 0.22

Size Hab. type 4 3 54.96 1.91 -24.26 0.11

TOY 10 3 55.09 2.03 -24.32 0.10

Parameter Multimodel Averaging Weighted Reg Coef. Low 95CI Upper CI

Hab. type (Understorey) No effect

Size No effect

Dev (Juvenile) No effect

b) Tetragnatha versicolor Walckenaer: 34 individuals tested.

Model

Model ID K AICc AiAICc LL

99 Size 3 2 40.74 0 -18.177 0.442

Hab. type 2 2 40.86 0.12 18.2387 0.415

Size Hab. type 1 3 43 2.25 18.1002 0.143

Parameter Multimodel Averaging Weighted Reg Coef. Low 95CI Upper CI

Size No effect

Hab. type (Understorey) No effect

c) Philodromus rufus vibrans Dondale: 49 individuals tested.

Model

Model ID K AICc Ai AICc LL wi

Size 2 2 57.29 0.00 -26.51 0.67

Size Tree Hab. type 1 4 59.66 2.37 -25.38 0.20

Parameter Multimodel Averaging Weighted Reg Coef. Low 95CI Upper CI

Size -21.78 -43.45 -0.12

Tree (Maple) No effect

Hab. type (Understorey) No effect

d) Theridion murarium Emerton: 37 individuals tested

Model

Model ID K AICc AiAICc LL wi

Size 4 2 53.16 0.00 -24.41 0.34

Size Hab. type 2 3 54.34 1.17 -23.80 0.19

Dev 6 2 54.83 1.67 -25.24 - 0.15

Size Hab. type Dev 3 4 55.00 1.84 -22.88 0.14

Parameter Multimodel Averaging Weighted Reg Coef. Low 95CI Upper CI

100 Size No effect

Hab. type (Understorey) No effect

Dev (Juvenile) No effect e) Salticidae: 109 individuals tested.

Model

Model ID K AICc Ai AICc LL wi

Size Hab. type 7 3 86.04 0.00 -39.91 0.22

Size 2 2 86.08 0.05 -40.99 0.21

Hab. type 3 2 86.45 0.41 -41.17 0.18

Dev Size Hab. type TOY 1 7 86.65 0.61 -35.77 0.16

Dev Size Hab. type Dev+Size 6 7 87.69 1.65 -36.29 0.10

Parameter Multimodel Averaging Weighted Reg Coef. Low 95CI Upper CI

Size No effect

TOY (Summer) -2.42 -4.38 -0.47

Hab. type (Understorey) No effect

f) Clubiona: 37 individuals tested.

Model

Models ID K AICc AiAICc LL wi

Size 2 2 45.24 0.00 -20.44 0.59

Size Hab. type 1 3 46.12 0.88 -19.69 0.38

Parameter Multimodel Averaging Weighted Reg Coef. Low 95CI Upper CI

Size -5.35 -9.39 -1.31

Hab. type (Understorey) No effect

101 4.10 List of figure captions

Fig. 4.1: Logistic regression of the propensity to balloon according to the body size (mm) of foliage dwelling spiders sampled in a north-temperate hardwood forest.

Fig. 4.2: The ballooning propensity of the most abundant spiders in the canopy and understorey of north-temperate hardwood forests. Spiders, from left to right, are ranked in order of increasing relative abundance in north-temperate hardwood forests. Error bars represent ballooning frequency standard error values.

102 Ballooning frequency 3 4^

W -\

00

o (A N' CD

3o>

OB H era' Ballooning frequency o o o o o r»- o k> ji. b> bo io o o o o o o

Clubiona sp. iW§-\ ^-

Philodromus sp. I—M

Eris militaris

Pelegrina ,m-i proterva o -1^ Tetragnatha versicolor :a^

Theridion murarium B- D D Hentzia O mitrata ffT 3 O Q. T3 CD Philodromus *< CO rufus g-H CD vibrans

Emblyna sublata 4.11 Connecting statement

In Chapter 4,1 identified life history traits that influence ballooning propensity of north- temperate hardwood spiders. With these results on key life history traits that promote high ballooning propensity and after a literature review on spider ballooning, I created subsets of species with either limited or high dispersal capacities. These species subsets representing high and low dispersal capacities along with the results on RADs from

Chapter 3 form the backbone for the hypotheses and predictions on species diversity patterns across multiple spatial scales being tested in Chapter 5.

105 5. Multiple spatial scale metacommunity dynamics of north-temperate

hardwood forest spiders

Maxim Larrivee1 and Christopher M. Buddie1

'Department of Natural Resource Sciences, McGill University, 21,111 Lakeshore Road,

Saint-Anne-de-Bellevue, Quebec, Canada, H9X 3V9

Original paper to be submitted to Journal of Animal Ecology (April 2009)

106 5.1 Preface

Dispersal capacity has direct consequences for local and regional diversity patterns. This original paper puts together the knowledge acquired in chapters 3 and 4 on north- temperate hardwood forest spider diversity and their ballooning propensity to study spider diversty at multiple spatial scales in north-temperate hardwood forests. It also adds tree trunk spider diversity information to the datasets for a more complete portrait of north-temperate hardwood forest spider diversity patterns. Under a spatially hierarchical sampling design, it investigates the patterns and processes of spider diversity patterns at multiple spatial scales (tree, stand, site, and region) following a metacommunity conceptual framework. This paper uses empirical data from Chapter 4 and the ballooning literature to create spider datasets of limited and high dispersal capacity. I demonstrate that novel canopy access techniques now allow temperate canopy ecologist to test ecological hypotheses using large scale and well replicated sampling designs. The results on the influence of dispersal capacity on diversity patterns at small and large spatial scales of generalist predators such as spiders will be of interest to community ecologists and to show that spiders are excellent models to test metacommunity paradigms.

107 5.2 Abstract

Dispersal capacity is intimately linked to local diversity patterns and with patch- dynamics (colonization-competition trade-offs), species-sorting (niche availability), mass-effects, and neutrality paradigms of metacommunity. Spiders are generalist predators that disperse passively through the air or via cursorial means at different rates.

They provide an excellent model community to test the importance of metacommunity paradigms across space. In this study we investigate the influence of dispersal capacity on the diversity of canopy and understorey spider assemblages in north-temperate hardwood forests within a metacommunity framework. We used a hierarchically nested design in space to investigate diversity patterns of local communities including species subsets with limited and high dispersal capacity through nested-multivariate ANOVA, additive diversity partitioning, and analysis of species-abundance distribution curves. Our results all point towards species-sorting processes (i.e., local abiotic gradients, spatial niche and resource availability dynamics) as the drivers of local community spider diversity at the tree and stand spatial scales. Significant changes in species richness, its composition and abundance-distribution curves at the site and regional level indicate that patch-dynamics and mass-effects contribute to spider diversity at the site and regional scale.

Key-words: Spiders, dispersal, hardwood forest, SAD, additive partitioning, patch- dynamics, metacommunity, canopy

108 5.3 Introduction

Species diversity patterns are hierarchically nested in space and driven by different processes, depending on the spatial scale considered (Tokeshi 1999). Metacommunity ecology has generated interest in relationships between regional and local community composition and provides a framework to study regional diversity patterns and their processes at multiple spatial scales. A metacommunity is defined as a set of local communities linked by dispersal within a region (Wilson 1992; Leibold etal. 2004).

Within this framework, local community diversity can be determined by species sorting

(e.g. gradients of local abiotic conditions, resources, and niche space), by patch-dynamics

(e.g. colonization-competition trade-offs where dispersal and colonization capacity play important roles), and by mass-effects (e.g. different immigration and emigration capacity result from varying densities in the species forming the local communities) (Holyoak et al. 2005). These paradigms are not mutually exclusive in metacommunity dynamics and can reflect use of different strategies by different species found in local communities

(Miller & Kneitel 2005). Cadotte (2006) has suggested that as the spatial scale increases, dispersal (mass and rescue effects), and the historical context (priority effects-species assembly, disturbance regime) have increasing influence on species diversity patterns.

Dispersal links diversity patterns across spatial scales through immigration-emigration

(mass and priority effects), and local population persistence (rescue effect) (Brown and

Kodric-Brown 1977; Shmida and Wilson 1985; Drake 1990). Different dispersal capacities are reflected in species interactions, community composition, and species turnover rates (P-diversity) within and between local communities. High dispersal capacities help maintain or increase species diversity across spatial scales, while limited

109 dispersal capacities can result in local extinctions and high species turnovers as spatial scale increases (Hubbell 2001; Mouquet and Loreau 2003, Cadotte 2006).

Dispersal strategies, rates, and capacities vary within and among local communities.

Arthropods use active (controlled walk, flight, and swim) and passive (uncontrolled flight driven by air or water currents, or phoresy) dispersal strategies. For example, zooplankton and spiders colonize new habitats quickly through passive dispersal in the air or water column (Louette and De Meester 2005; Bonte, Lens and Maelfait 2006).

Passive aerial dispersal rates in spiders are influenced by body size, habitat specialization, feeding habits, and over longer time spans it can reflect their phylogenetic history (Bonte et al. 2003; see Chapter 4). The capacity to disperse over long distances is linked to the strategy used. For example, active flyers and passive aerial dispersers will be more prone to long dispersal events than cursorial dispersers (Driscoll 2008). Thus, dispersal capacity community structure and contributes, along with habitat effects, to distribute species populations unevenly across space. Few empirical metacommunity studies address local communities hierchically nested in space but instead have explored the topic on a local to regional spatial scale basis (but see Lindo and Winchester 2008). Species-abundance distributions (SAD), species-area relationships, and multivariate analyses are approaches commonly used to study spatial patterns of diversity in a metacommunity (Hubbell 2001;

McGill etal. 2007).

Species-abundance distribution (SAD) models lend themselves well to studies of the influence of habitat and dispersal on local communities nested in space. Changes in

110 species-sorting and niche apportionment dynamics inside local communities at different spatial scales can be investigated by comparing SADs at different spatial scales within a metacommunity. Departure of the local community SAD from the metacommunity SAD reflects the influence of non-random processes on species composition. Changes in the shape of SADs at the local and regional scales can for example, be related to spatial aggregation of conspecifics (Green and Plotkin, 2007). The metacommunity SAD tends to produce a log-series curve due to high dispersal rates while local communities tend to produce lognorrftal SADs with surpluses of rare species (Hubbell 2001; Bell 2001;

McGill 2003). Recently, lognormal and multimodal SAD's have been unveiled as the spatial scale or sampling effort increases (Connolly et al. 2005; Dornelas, Connolly and

Hughes 2006; Dornelas and Connolly, 2008). Emergence of lognormal distributions is thought by the authors to result from combinations of stochastic and environmental processes. Comparing dispersal driven SADs across different spatial scales will help detect the spatial scale at which dispersal impacts SADs within a metacommunity.

Limited dispersal capacity in invertebrates, especially in passive aerial dispersers, tends to affect species richness negatively with increasing distance between local communities

(McCauley 2006; Vanschoenwinkel et al. 2007; 2008; Engen et al. 2008). Driscoll

(2008) found that richness patterns of actively flying ground beetles were mediated mostly by habitat quality and not by patch isolation supporting species-sorting or mass- effects models, while poor dispersers (flightless) were negatively affected by patch isolation. Dispersal had limited influence on the structure of cladocerans' relative abundance and richness in highly interconnected shallow ponds; highlighting strong

111 species-sorting influences in these local communities (Cottenie and De Meester 2004). In general, distance between local communities increases species turnover diminishing their similarity. However, high dispersal capacity does not always have a large impact on local community abundance distributions which can be strongly driven by species-sorting and patch-dynamic processes (Kneitel and Miller 2003).

Dispersal and the influence of space on community diversity can also be assessed with a and P-diversity values across spatial scales for groups of species with different dispersal capacities. If random processes govern regional diversity, local communities investigated at spatial scales hierarchically embedded in the region are expected to contribute equally to species diversity. Non-random distribution of the species across space indicates spatial aggregation of individuals and potentially limited dispersal. It is predicted that high dispersal capacity homogenizes local communities and creates high a-diversity values and limited species-turnover between the communities increases P-diversity and reduces a-diversity (Hubbell 2001; Mouquet and Loreau 2003). Thus, under high dispersal rates, species-sorting dynamics should govern local community composition. In a study of a prototypical metacommunity of oribatid mites, the two largest spatial (patch and tree) showed greater than expected P-diversity patterns, while the tree scale had the largest contribution to the metacommunity richness (Lindo and Winchester 2008). Beetle P- diversity was greater than expected for ecoregions and among sites within ecoregions while a-diversity was always lower than expected across all spatial scales (tree, stand, site, ecoregion) in hardwood forests of Ohio, United-States (Gering et al. 2003).

Invertebrates, because of their small size, high richness and abundance at small spatial

112 scales, and various dispersal modes (passive and direct flight, cursorial) provide excellent model communities to test metacommunity models. We studied spiders in the canopy and understorey of north-temperate forests to investigate the influence of habitat and dispersal on local community diversity at multiple spatial scales within a metacommunity framework.

The canopy and understorey spider assemblages of north-temperate hardwood forests differ in composition and these assemblages can be separated in species subsets of limited and high dispersal capacity based on their propensity to disperse passively through ballooning (Larrivee and Buddie 2008; see Chapter 4). Also, spiders are all predators at a similar trophic level in the food chain and their diversity is linked to habitat complexity (Buddie et al. 2000; Larrivee et al. 2005). In the present work, we investigate changes in community composition and richness of spider assemblages in north- temperate hardwood forest as a function of spatial scales. Our primary objective is to identify potential biological processes affecting spider diversity at each spatial scale, using a metacommunity framework. To do so, we compare observed local community composition and richness at four spatial scales: tree, stand, site, and the regional species pool represented by our complete dataset. We also compare observed SADs from each spatial scale to predicted lognormal distributions. We use additive diversity partitioning to measure the contribution of each spatial scale to the regional species richness pool and investigate spatial aggregation of conspecifics through P-diversity. Finally, we use species subsets from the complete species pool to investigate the influence of dispersal capacity and habitat type on local community structure across space. We make the

113 following predictions: 1) A lognormal distribution will be revealed as the spatial scale increases as suggested with increased sampling effort of foliage spiders in this system

(Larrivee and Buddie 2009); 2) Canopy and understorey assemblages will not follow similar SAD models due to increased mass and rescue effects in the canopy habitat; 3)

Spatial scales will not contribute equally to the regional richness pool; 4) Species subsets of high dispersers will increase a-diversity and decrease P-diversity homogenizing local diversity across spatial scales; 5) The reverse will be true for limited dispersers.

5.4 Materials and methods

5.4.1 Study site and sampling protocol

This study was completed within the greater Montreal region in southwestern Quebec,

Canada. Following a hierarchically nested spatial design, the canopy and the understorey saplings (i.e., directly under each of 3 mature trees) (tree scale) of sugar maple {Acer saccarrhum Marsh.) and American beech (Fagus grandifolia Ehrh.) were sampled in maple-beech dominated stands (stand scale) replicated 5 times in 3 maple-beech sites

(site scale) located around the greater Montreal region (regional scale). The Mont-St-

Hilaire biosphere reserve (MSH) (45°32' N; 73°09' W), Oka National Park (OKA)

(45°28' N; 74°04' W), and Mont-St-Bruno (MSB) (45°33' N; 73° 19' W) National Park represented the sites within the region. Refer to Larrivee and Buddie (2008) for additional details about the trees that were sampled. The terminology used to identify our spatial scales implies that the distance between each tree within a stand is significantly smaller than their distance to trees from other stands. Also, the distance between each stand within a site was large enough that any movement by a spider individual between stands

114 would be considered an inter-generational movement. The mean distance between stands was more than 500 m which is well beyond the home range of spiders (Hallander 1967;

Hodge 1987; Heidger and Nentwig 1989).

Spiders were sampled in the canopy and the understorey using a beating sheet and sticky traps attached to the trunks. A complete description of the beating procedure can be found in Larrivee and Buddie (2008). On each tree sampled, we nailed, at breast height (~

1.4 m), and at the highest point possible on the tree trunk (20 ± 2 m), a 60 cm long by

22.5 cm wide polyethylene sheet coated with Tree Tangle-foot Pest Barrier (The

Tanglefoot Company, Grand Rapids, MI), centered to the southern exposure (for a description of the Tangle-foot mixture, see Saint-Germain et al. 2006). The traps were active during the entire length of the sampling periods (see below) and were replaced with new ones at the beginning of the next sampling period. When removed from the tree, each trap was covered with a plastic film and brought back to the laboratory. All spiders were removed from the resin and cleaned with Histo-Clear histological clearing agent (National Diagnostics, Atlanta, GA). The beating and sticky trap sampling techniques show high complementarity in the spider fauna they target (Marczewski-

Steinhauss (M-S) complementarity index of 0.61); they sample and provide a more accurate representation of the local spider community (Colwell and Coddington 1994).

The index varies from 0 (identical species list) to 1 (full complementarity of the species list).

115 Canopies were accessed using an aerial lift platform capable of reaching heights of 26 m; this lift could be moved easily from site to site. Each tree (canopy and understorey) was sampled approximately every 21 days during 2005 and 2006 (Larrivee and Buddie 2008).

Spiders were identified to species whenever possible using the keys of Paquin and

Duperre (2003), and Ubick et al. (2005). Classification followed Platnick's World Spider

Catalog V8.5 (Platnick 2008). Voucher specimens are deposited at the Lyman

Entomological Museum (Ste-Anne-De-Bellevue, Quebec) and the Canadian National

Collection (Ottawa, Ontario). Juveniles were assigned to a species following the same protocol as Larrivee and Buddie (2008).

For the purpose of the paper, we separated the data into two subsets. One composed of spider species sharing attributes that promotes high ballooning propensity, thus having high dispersal capacities, and another one of species sharing attributes related to low ballooning propensity, thus having limited dispersal capacities. Species with high dispersal capacities in our dataset were determined with the following criteria: the species is part of the web-building feeding guild, has a small body size (< 3 mm) over most of its development, and/or is a known frequent ballooner in the literature, and/or demonstrated high tiptoe frequency in a lab experiment on pre-ballooning behaviour (tiptoe) of north- temperate hardwood forest spiders (see Chapter 4). Those with limited dispersal potential were determined with the following criteria: the species is part of the hunting feeding guild, has a large body size (> 3 mm) over most of its development, and/or has limited to no tiptoe frequency according to the literature, and/or demonstrated low tiptoe frequency

116 in a lab experiment on pre-ballooning behaviour (tiptoe) of north-temperate hardwood forest spiders (see Chapter 4).

5.4.2 Data analyses

The analyses are based on individuals that could be identified reliably to species level, a procedure commonly used for biodiversity research with arachnids (e.g., Buddie et al.

2000; Beaulieu et al. 2006, Larrivee and Buddie 2008). About 2 400 juveniles (13.5 % of the total collection) could not be identified to species level and were therefore removed from the dataset prior to analyses.

We fitted various models to observed species-abundance distribution (SAD) curves to assess the dominance structure of spider assemblages and compared the curves among assemblages collected in the canopy and in the understorey at every spatial scale. Two lognormal models were fitted to the observed SAD's with the Vegan library in R

(Oksanen et al. 2008): 1) The truncated lognormal model is a fit to the octave-pooled data using a second degree log-polynomial with Poisson error using the function prestonfit; 2)

The left-truncated Normal distribution that fits log2 transformed non-pooled observations with direct maximization of log-likelihood using the function prestondistr. Gray et al.

(2006) recommend using the left-truncated normal distribution to test the fit of the data since it fits every species (i.e., not only the pooled number of species inside an abundance class). For stronger inference, we tested our data using both approaches since the chances of obtaining a departure from the lognormal fit are even lower with the prestonfit function. To facilitate the comparisons between the SADs from every spatial scale, the y- axis displays the relative frequency of the mean number of species present in each

117 abundance class. To verify that the lognormal was a good fit to the observed distributions, we performed Pearson Chi-square tests of the observed and fitted data of the SADs obtained at each spatial scale.

To test the effects of vertical stratification (canopy vs. understorey) and spatial scales on species composition, we performed a nested non parametric multivariate ANOVA with the software PERMANOVA (Anderson 2005) with vertical stratification and tree type acting as crossed factors, and with site and stand spatial scales as nested factors to both crossed factors. The data were Hellinger transformed prior to the analysis (Legendre and

Gallagher 2001). This non-parametric multivariate analysis is highly appropriate for our data since we are considering multiple response variables (spider species) and multiple objects (180 sampling sites), and this approach was successful in our past work in this system (Larrivee and Buddie 2008). The test of significance for all factors and interactions was done through permutation of the rows of the raw data matrix. A total of

9999 permutations were performed for every test of significance. Pair-wise comparisons were performed to test the levels of each factor when a factor or interactions between the factors were significant using a Monte-Carlo randomization permutation (9999 permutations) procedure of the total number samples associated with each set of comparisons.

We partitioned the species richness found at each spatial scale within the study region

(tree, stand, and site) to quantify the contribution of each spatial scale to the regional spider richness in north temperate hardwood forests (pool of all sticky and beating

118 samples collected). To do so, we follow the additive partitioning approach to the alpha- beta-gamma relationship (Lande 1996). In the additive approach to richness across spatial scales, all components of the alpha-beta-gamma relationship share the same units (Lande

1996) allowing direct comparison of alpha and beta diversity across spatial scales. Thus, additive partitioning methods can be used to quantify the relative contribution of alpha and beta diversity to gamma diversity (Gering and Crist 2002). Using this approach, regional spider diversity of north-temperate hardwood forests (gamma diversity (y)) represents the sum of the a-diversity at the tree scale, the P-diversity at the stand scale, and the P-diversity at the site scale. y (Regional diversity) = al (within trees) + pi (among trees) + P2 (among stands) + P3

(among sites)

The a-diversity from each spatial scale corresponds to the sum of the P-diversity and the a-diversity of the spatial scale below in the hierarchy (for example: astand = atree+ptree; or an= a(n-l)+P(n-l)) (Wagner et al. 2000). We used the program PARTITION (Veech and Crist 2008; Crist et al. 2003) to partition and test statistically the observed a and p- diversity at each spatial scale investigated for our canopy and understorey datasets, and subsets representing species with high or limited dispersal capacities. Precisely, through

PARTITION, we test the null hypothesis of no spatial scale dependence in the richness patterns of north-temperate hardwood forest spiders; that our observed a and P richness values at each spatial scales do not differ from random distributions of north-temperate hardwood forest spiders. PARTITION generates 10000 random distributions of north- temperate hardwood forest spider species among samples at each spatial scale forming null distributions for a and P richness estimates of each spatial scale within our

119 hierarchically nested design. The proportion of null values that is greater or less than the observed values at a particular spatial scale represents the probability that the observed richness (a and P) differs from a random distribution.

5.5 Results

A total of 15,039 individuals was identified to species and used in our analyses

(Appendix 8.1). This total represented 18 families, 71 genera and 108 species of which

69.4 percent of the sample (i.e., total catch), and 75 species belonged to the web-builder guild (Families: Agelenidae, Amaurobiidae, Araneidae, Dictynidae, Hahniidae,

Linyphiidae, Mimetidae, Tetragnathidae, Theridiidae, Uloboridae), and 30.6 percent of the sample and 33 species were assigned to the hunter guild (Families: Clubionidae,

Gnaphosidae, Liocranidae, Lycosidae, Philodromidae, Pisauridae, Salticidae,

Thomisidae) (Appendix 8.1). A single species of Dictyidae, Emblyna sublata (Hentz), accounted for 40.1 percent of the sample and the 10 most commonly collected species accounted for 84.4 percent of the collection.

The SADs from the understorey datasets progressively unveil a lognormal distribution as the mode widens and diminishes in height as the spatial scale increases until the site and regional scale (Fig. 5.1). SADs were not fitted by the left-truncated Normal distribution at the site spatial scale, and by both the left-truncated Normal and truncated Lognormal distribution at the regional spatial scale (Table 5.1). The SADs from the canopy datasets were not fitted both models until the regional scale where there is a significant difference between the observed and fitted values to the left-truncated Normal distribution (Figure

5.1, Table 5.1 for Pearson Chi-square test). When the canopy and the understorey

120 datasets are pooled together, the SADs were fitted by the truncated lognormal model at all scales but depart significantly from the left-truncated Normal model at the site and regional spatial scales of the study (Fig. 5.1, Table 5.1 for Pearson Chi-square test). The shape of the SADs from the limited and high dispersal datasets show reverse trends as the spatial scale increases. For the limited dispersers, as the spatial scale increases, more of the veil line is revealed to the left and the proportion of singletons diminishes, while for the high dispersers, the veil line moves to the right as the spatial scale increases showing that the number of rare species not sampled is increasing with increasing spatial scale, and the proportion of singletons are maintained (Fig. 5.2). The limited dispersal SADs fit both distribution models at all spatial scales (Table 5.1). The high dispersal SADs fit both distribution models until the regional scale where it only fits the truncated lognormal distribution (Table 5.1).

The nested nonparametric permutational multivariate ANOVA indicates that there is vertical stratification in the species composition; it differs significantly from random expectations for composition between the canopy and the understorey and also at the stand and site spatial scales (Table 5.2). There was no significant interaction between the vertical stratification (i.e., canopy versus understorey) and tree species. When the analyses where performed on the dispersal capacity datasets, composition differed between the canopy and understorey but not tree species, and it differed at the site and stand spatial scales similarly to the complete dataset (Table 5.2). Pair-wise a posteriori comparisons indicated that spatial patterns of composition differ among sites. Canopy

121 and understorey assemblages show different patterns of compositional change among sites (Table 5.3).

Mean and overall richness was greater in the understorey than the canopy at every spatial scale (tree, stand, site, and region) of the hierarchy in our nested design (Table 5.4). Site

P-diversity was the largest contributor to regional richness contributing 43 % and 35 % in the canopy and the understorey respectively (Fig. 5.3). The observed P-diversity was significantly greater than expected from a random distribution in the canopy and understorey only at the site scale (Table 5.4). The site P-diversity spatial scale contributed to the regional diversity of high and limited dispersers in a similar fashion in the canopy and the understorey. For both dispersal capacity subsets, observed P-diversity was significantly greater than expected from a random distribution in the canopy and understorey only at the site spatial scale. Overall, richness was partitioned in a similar fashion to the complete dataset for both dispersal rates (Table 5.4 and Fig. 5.3).

5.6 Discussion

In the canopy and understorey of north-temperate hardwood forests, dispersal capacity does not have a strong influence on the diversity of spiders at small spatial scales (tree and stand scales). The SADs of all north-temperate spider assemblages in our study systematically fit both lognormal models at the tree and stand spatial scales, indicating that dispersal capacity and vertical stratification may not be the main drivers of species- abundance distributions at these spatial scales. These results are consistent with our community composition and additive richness partitioning results which also show that

122 dispersal capacity is not an important factor governing local spider diversity at the tree and stand spatial scales. Statistical theory work on sampling of species abundances shows that similar species-abundance distributions across spatial scales reflect a simple scaling relationship of the processes governing both spatial scales (Green and Plotkin 2007).

Thus, at these spatial scales, north-temperate spider assemblages seem to be governed by species-sorting processes, not dispersal capacity and vertical stratification.

Species-sorting processes involving local abiotic gradients, spatial niche and resource availability dynamics likely have strong influences on spider diversity at small spatial scales. Local spider diversity is often associated with habitat heterogeneity, abiotic factors, resource availability, and predation pressures (Greenstone 1984; Halaj et al.

1998; Larrivee et al. 2005; 2008; Aikens 2008). Species-sorting dynamics are present in sand dune spider communities where persisting species share similar ecological traits

(large body size and longer generation time) and have narrower niche breadth (Bonte et al. 2006). Dispersal capacity does influence diversity patterns beyond the stand spatial scale, suggesting a change in the processes shaping the spider assemblages at larger spatial scales.

The site and regional spatial scales for the understorey and tree assemblages did not fit the left-truncated Normal distribution forcing us to reject our first prediction that a lognormal distribution is unveiled as the spatial scale increases. Departure from the lognormal distribution at the site spatial scale reflects spatial aggregation of species rather than increased dispersal rates since our high dispersal dataset still fits the lognormal

123 distribution at the site spatial scale. At the regional level, all assemblages departed from the lognormal distribution, with the exception of the limited dispersers. This supports

Hubbell's (2001) prediction that metacommunities show a logseries distribution due to the rare status of most species at the metacommunity scale. Species are rare in most of their distribution range as they tend to be spatially aggregated which favors a skew in rare species as the spatial scale increases (McGill and Collins 2003). Intuitively, with individuals being aggregated in space, there is a greater chance of not sampling a species as the spatial scale increases, thus making them appear as rare (Green and Plotkin 2007).

In general, our SADs show a high proportion of singletons at all spatial scales but not of common species. The passive (random) aspect of long distance aerial dispersal in spiders could be responsible for this excess of rare species at all spatial scales in our study. The lognormal remains the best fit in all datasets at small spatial scales, even though at every spatial scale the largest number of species is represented by only one individual. This provides more support for species-sorting processes and overrules mass-effects at small spatial scales since dispersal is not responsible for the diversity patterns at small spatial scale in our study.

The limited dispersal curves of fitted values gradually unveiled a lognormal distribution as the spatial scale increased; this is a shift of the veil line to the left, which corroborates our first prediction. This is supported by the lognormal as the best fit at all spatial scales pointing again to species-sorting processes as the main drivers of species abundances for limited dispersal assemblages within the metacommunity. Patch-dynamics and dispersal limitations may be relevant at spatial scales beyond the stand level as their SADs

124 contained smaller proportions of singletons as the spatial scale increased. Proportions of singletons were consistent across spatial scales for high dispersers indicating the presence of mass-effect dynamics. As such, SADs for the high dispersal capacity became more veiled as the spatial scale increased and did not fit the left-truncated lognormal distribution at the regional scale. This reflects the prediction by neutral models that at the metacommunity scale, the logseries prevails as species maintain their local occurrence at low abundance values across the metacommunity through mass effects (Hubbell 2001;

Bell 2005). A large study on tropical coral and reef fish abundance distributions unveiled a lognormal distribution as the spatial context increased (Connolly et al. 2005).

According to Connolly et al. (2005), following the Central Limit Theorem (May 1975), the emergence of the lognormal distribution was the consequence of multiple interactions among stochastic environmental variables associated to population growth. In our study, beyond the influence of space, we show that dispersal capacity, a biological process, can significantly modify the shape of SADs. In a study offish abundance distribution through time, species subsets with different life history traits also produced SADs that departed from a lognormal distribution (Magurran and Henderson 2003).

The composition of spider assemblages changed significantly in vertical space (canopy and understorey) at stand and site spatial scales, and when the analyses were performed on high and limited dispersal species subsets, the results were similar. This was somewhat surprising since high dispersal capacity can reduce compositional differences in space by homogenizing diversity across spatial scales (Kneitel and Miller 2003;

Cadotte 2006). Consequently, this leads us to expect no differences between spatial scales

125 with the high dispersal capacity dataset. Our results therefore indicate that strong species- sorting dynamics are present between the canopy and understorey habitats but also across spatial scales since compositional patterns were similar for all datasets. At high dispersal rates, dominant competitors or generalist predators can access all local communities and reduce the richness increase often generated by high dispersal capacity (Kneitel and

Miller 2003; Cadotte and Fukami 2005; Cadotte et al. 2006). Spiders are well known generalist predators and their diversity is linked with habitat heterogeneity (Buddie et al.

2000) and they can control phytophagous insect populations in natural habitats (Riechert and Lockley 1984). On the other hand, habitat generalist spiders have higher aerial dispersal propensities compare to habitat specialists (Bonte et al. 2003) supporting the patch-dynamic tenant of colonization ability trade-offs between species. Yet, in an experimental study, dominant spiders of north-temperate hardwood forests showed no habitat affect (canopy vs. understorey) on their propensity for aerial dispersal but small body size and feeding guild life history traits had a strong effect (see Chapter 4).

The spatial scales considered in our study did not contribute equally to the regional species pool of north-temperate hardwood forest spiders. Significantly higher than expected P-diversity values at the site spatial scale indicated aggregated spatial distributions of conspecifics. Oribatid mites also showed higher than expected P-diversity at the third spatial order of a study on forest floor and suspended canopy soil mite diversity (Lindo and Winchester 2008). In contrast with our species composition results, observed a and P richness values did not differ from expected random values of richness at the stand scale (note: the tree scale could not be tested in the multivariate nested

126 ANOVA; it was the unit of replication). Agafri, richness partitioning of limited and high dispersal capacity species subsets offered similar results to the complete dataset. We interpret this to mean that limited dispersal was not a main cause in the higher than expected P-diversity at the site scale, refuting our prediction that our limited dispersal subset would show higher than expected P-diversity as the spatial scale considered increased.

Our partitioning results point towards species-sorting dynamics as the important processes shaping richness turnover in north-temperate hardwood spiders. Contrary to our results, P-diversity of sand dune spider assemblages was reduced significantly by mass-effects that allowed specialist species of disturbed sand dune patches to co-exist with species from stable sand dune patches (Bonte et al. 2006). Variation in competitive ability is difficult to demonstrate empirically and we can only speculate on the mechanisms. However, dominant spider species from this habitat type have varying ballooning propensities (see Chapter 4), a sign of potential trade-off between colonization ability and competition. If habitat heterogeneity increased at larger spatial scales (i.e., providing more available niches) mean richness per site would also have been higher than predicted by random sampling. This was not the case, allowing us to reject the species- sorting paradigm as an explanation for the significantly higher richness turnover at the site scale.

Increased dissimilarity due to reduced spatial autocorrelation with increasing spatial scale

(Legendre et al. 2004) could also explain the higher than expected turnover. Oka

127 assemblages differed from MSB and MSH more often than MSB and MSH did in our a posteriori pair-wise analyzes, perhaps because they were closer in space. However, if spatial autocorrelation was an important process, we could predict that the high dispersal species subset would have showed reduced richness turnover compared to the limited dispersal dataset (Mouquet and Loreau 2003; Kneitel and Miller 2003; Cadotte 2006), but this was not the case in our study. In a study of community richness of rock pool invertebrates (passive dispersers), environmental conditions explained 50 % of the variation, while space explained only 11 % of the variation, supporting species-sorting processes (Vanschoenwinkel et al. 2007). Similarly to rock pool invertebrates, high dispersal capacity in spiders results from passive dispersal (Bell et al. 2005; Bonte et al.

2003; Chapter 4).

In this multiple spatial scale study, we show that species-sorting dynamics are the most likely ecological processes governing spatial patterns of diversity at small spatial scales

(tree and stand) for north-temperate hardwood forest spiders. These species-sorting processes are highlighted by significant changes species composition and mean richness turnover P-diversity at the site scale regardless of the dispersal capacity of spiders, providing evidences of spatial aggregation of conspecifics that are habitat rather than dispersal driven. Moreover, species-abundance distributions only depart from the lognormal distribution beyond the stand scale, again regardless of dispersal capacity supporting our composition and richness analyses. From a metacommunity perspective, our results indicate that north-temperate hardwood forest spider diversity is regulated in large part by species-sorting dynamics and not dispersal capacity below the site spatial

128 scale. Patch-dynamics and mass-effects may contribute to spider diversity at the site and regional scale notably because of the presence of many rare species and the departure of the species-abundance distribution from the lognormal. Space availability becomes a significant factor in determining spider assemblage composition at the stand scale and significantly higher than random richness turnover occurs at the site spatial scale irrespective of dispersal capacity. As such, according to our results the stand scale should be used to define local spider communities of north temperate hardwood forests.

5.7 Acknowledgements

The authors would like to thank K. Robert, K. Brochu, K. Aikens, B. Schroeder, Z.

Sylvain, J. Bowden, and J.F. Aublet for their relentless effort and dedication over two summers of field and laboratory work. We also thank Dr. C. Dondale for assistance with spider identification and Dr. P. Mason from the Canadian National Collection for support. We thank the Centre d'etude de la foret for its support. The research was funded by the Fonds Quebecois de Recherche en Nature et Technologies (FQRNT) to ML, the

National Science and Engineering Research Council of Canada (NSERC) (discovery grant to CMB), the Canadian Foundation for Innovation New Opportunities Grant

(Project #9548, to CMB), and the Department of Natural Resource Sciences (McGill

University).

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134 135 5.9 Tables

Table 5.1

Pearson Chi-square test of observed and predicted SADs following the Truncated Lognormal distribution* and the Left-truncated

Normal distribution** at the tree, stand, site, and regional spatial scales of the study.

Tree Stand Site Region df p-value df p-value df p-value df p-value Complete dataset Canopy Truncated lognormal 6 NS 8 NS 9 NS 11 NS Left-truncated Normal distribution 6 NS 8 NS 9 0.0744 11 O.0001

Understorey Truncated lognormal 5 NS 8 NS 9 NS 11 0.025 Left-truncated Normal distribution 5 ' NS 8 NS 9 0.029 11 <0.0001

Tree Truncated lognormal 7 NS 11 NS 12 NS 12 NS Left-truncated Normal distribution 7 NS . 11 NS 12 0.013 12 0.007

Limited dispersal Truncated lognormal 5 NS 8 NS 9 NS 10 NS Left-truncated Normal distribution 5 NS 8 NS 9 NS 10 NS

High dispersal Truncated lognormal 6 NS 10 NS 10 NS 11 NS Left-truncated Normal distribution 6 NS 10 NS 10 0.081 11 0.015 * The truncated lognormal model is a fit to the octave pooled data using a second degree log-polynomial with Poisson error. ** The left-truncated Normal distribution is a fit to a log2 transformednon-pooled observations with direct maximization of log-likelihood

136 Table 5.2

Results from a nested nonparametric permutational multivariate ANOVA testing spider species composition found at each sampling location in southern Quebec sugar maple forests. Vertical stratification (canopy and understorey) and tree type (sugar maple and

American beech) are crossed factors and the spatial scales site and stand are nested within the crossed factors. Each unit of replication represents the pooled beating and sticky trap sampling efforts of 2005 and 2006. (MC) = Monte-Carlo randomization. High dispersal

= analysis performed on a dataset composed of species sharing attributes of high ballooning propensity. Limited dispersal = analysis performed on a dataset composed of species sharing attributes of low ballooning propensity.

Source df F P(MC)

Full dataset

Vertical stratification 1 53.2886 0.0001

Tree 1 1.53 NS

Site (Vertical stratification x Tree) 8 2.6876 0.0001

Stand (Vertical stratification x Tree x Site) 48 1.994 0.0001

Vertical stratification x Tree 1 0.5986 NS

Residual 120

Total 179

High dispersal

Vertical stratification 1 37.9964 0.0001

Tree 1 1.3634 NS

137 Site (Vertical stratification x Tree) 8 2.7274 0.0001

Stand (Vertical stratification x Tree x Site) 48 1.3252 0.0029

Vertical stratification x Tree 1 0.7928 NS

Residual 120

Total 179

Limited dispersal

Vertical stratification 1 54.416 0.0001

Tree 1 1.1122 NS

Site (Vertical stratification x Tree) 8 5.5662 0.0001

Stand (Vertical stratification x Tree x Site) 48 1.4045 0.0012

Vertical stratification x Tree 1 0.3314 NS

Residual 120

Total 179

138 Table 5.3

A posteriori pair-wise comparisons of north-temperate hardwood forest spider composition at the site spatial for interaction factors Habitat and Tree. Monte-Carlo randomization permutation (9999) procedures were performed for each pair-wise comparison.

Complete dataset High dispersal Limited dispersal

t P(MC) t P(MC) t P(MC)

Site (Beech Canopy)

MSB vs. MSH 0.9568 NS 0.9595 NS 1.4774 NS

MSB vs. Oka 1.7665 0.0328 1.7334 0.042 2.3134 0.0107

MSH vs. Oka 1.5901 0.0556 1.7846 0.0351 1.857 0.0236

Site (Beech Understorey)

MSB vs. MSH 1.1368 NS 1.3279 NS 1.146 NS

MSB vs. Oka 2.108 0.0055 1.9155 0.0136 2.6794 0.0017

MSH vs. Oka 2.2708 0.0033 2.5918 0.0015 2.7785 0.0017

Site (Maple Canopy)

MSB vs. MSH 0.9829 NS 1.1124 NS 1.3909 NS

MSB vs. Oka 1.6902 0.0373 1.8038 0.0236 1.6596 0.0533

MSH vs. Oka 1.4424 NS 1.8298 0.0245 2.3001 0.0057

Site (Maple Understorey)

MSB vs. MSH 0.9791 NS 1.0354 NS 1.1414 NS

MSB vs. Oka 2.2741 0.002 2.0409 0.0062 3.1769 0.001

139 MSH vs. Oka 2.101 0.0043 1.9637 0.0083 3.4821 0.0003

140 Table 5.4

Additive partitioning results for north-temperate hardwood forest canopy and understorey spider assemblages from the complete, high and limited disperser datasets of the study.

Significance of observed richness partitioning is based on expected values generated from 10 000 randomized permutations with the PARTITION software. Values for P3, P2, pi, and al spatial scales represent average richness values within each spatial scale in the hierarchical design.

Complete dataset High dispersers Limited dispersers

Canopy Unders. Canopy Unders. Canopy Unders.

Tree a 9.3 17.7 7 14.1 3.0 5.7

TreeP 9.8 15.5 6.8 12.3 2.9 5.5

Stand |i 20.1 25.9 15.7 18.2 5.2 7.7

Site P 29.8*** 32.9*** 22.5*** 23.4** ytf*** 7 j**

Region (y) 69.0 92.0 52.0 68.0 19.0 26.0

* denotes significantly different from expected (* p<0.05; **p<0.01; ***p<0.0001)

141 5.10 List of figure captions

Fig. 5.1: Species-abundance distributions bar plots for spiders collected in the understorey, canopy, and trees (understorey and canopy samples pooled) of pooled beating and sticky trap samples on sugar maple and American beech trees at the tree, stand, site, and regional spatial scales in sugar maple forests of southern Quebec, Canada during the 2005 and 2006 sampling seasons. Y-axis represents the relative proportion of species in each abundance class on the x-axis (log2 number of individuals).

Fig. 5.2: Species-abundance distribution curves of the observed and fitted values for limited (a) and high (b) dispersal subsets of spiders. Subset represent pooled (understorey and canopy samples) beating and sticky trap samples on sugar maple and American beech trees at the tree, stand, site, and regional spatial scales in sugar maple forests of southern Quebec, Canada during the 2005 and 2006 sampling seasons. Y-axis represents the relative proportion of species in each abundance class on the x-axis (log2 number of individuals).

Fig. 5.3: Proportion of richness components alpha and beta to overall gamma diversity for the complete dataset, high and limited dispersers of canopy and understorey spiders in north-temperate hardwood forests over pooled sampling years of 2005 and 2006 in southern Quebec, Canada.

142 Fig. 5.1

Understorey

5- 04 Stand Site Region I 0.3. I- ix ils 0.1 iXx.T..

^ C.l Tf OS (O ^ » 8 « tfl IWtf>*r£J-*Oi<» 0.0 • Canopy OS •

Tree Starcd Site Region H I C2: ,1. <%• .,!•, i 0.1 i a J, x H J. 0.0 ; 8 s> {J W « r M '

Tree

Tree i j S&nri Site Region

iAJ,

'(^TO>W^'To5»M'«-»i!

Number of individuals (Log?)

143 Fig. 5.2

Tree Stand Region

High dispersal obs.

Id a LI a, » <3 3 S3 5 8 S S S 8 8

Tree Site Region

High dispersal fitted

0.1 i i^i

Q> 3 CO : ;vi i •* ' » S B 8 | > C.3 ' :y Tree Site Region .«_• « Stand

S38S

Stand Site Region

Limited dispersal fitted

raas; Number of individuals (Log,)

144 Fig. 5.3

100% '3 16 "!•> 0 80% -\ 15 S) 18 21 It Tree a 60% P§S xJSs 27| • Tree p ESsS m RXjXg s 0 40% iii ^ H Stand p 5 m B Site S 20% E43i :433 35: 3* 271 0% C | U C | U

Complete dataset High disp. Low disp.

145 6. Summary

In the past, limited replication in canopy ecology studies reduced the spatial scale for inference, limiting the extent to which ecological hypotheses could be tested. The methodology used in this thesis to access the tree canopies was unique in its ability to use a combination of direct and indirect sampling methods in mature temperate hardwood tree crowns. Most importantly, it permitted extensive spatial replication of canopy samples in a short time span at a regional spatial scale. Thus, I could standardize direct sampling methods in the canopy and the understorey in real time with similar levels of replication. This supports high inferential strength to the statistical tests used to test the ecological hypotheses in my thesis. This thesis also provides the first comparison of intra- and interspecific ballooning propensity of spider species across many families in North

America. It is also the first study to demonstrate and quantify the ballooning propensity of forest spiders, and especially canopy spiders. My investigation of dispersal capacity and spider diversity patterns across multiple spatial scales is the first study testing the influence of dispersal on spatial diversity patterns using empirical data about spider ballooning propensity.

The distinct assemblages found in the canopy, and the difference in composition between the canopy assemblages of sugar maple and American beech, indicate that spatial patterns of diversity in mature forest tree crowns differ from those of understorey saplings. The passive aerial dispersal behaviour of spiders and their tendencies to disperse across landscapes were linked to specific life history "constraints" and used to test the

146 explanatory power of commonly employed adaptive models (mixed ESS and bet- hedging). The impact of dispersal on local spider diversity was evaluated through the study of variation in dispersal capacity, as detected in Chapter 4.

Spiders proved to be excellent models for understanding the metacommunity processes behind spatial diversity patterns across multiple spatial scales. Overall, spiders offer many advantages for ecologists in dealing with significant questions in modern community ecology. They provide opportunities for stimulating field and laboratory work to develop simple models that can be tested against empirical data. Their small size, abundance, ubiquity, natural history, and diversity of spiders facilitate the quest for levels of replication necessary to produce analytically sound multiple scale studies.

6.1 Synthesis

6.2.1 Diversity of canopy and understorey spiders

My results show that canopy spider diversity is distinct from that in the understorey and that canopy assemblages also differ significantly between sugar maple and American beech. Significant differences in the shape of the canopy and understorey RADs along with the models that best fitted both distributions indicate a less stable habitat in the canopy. The RAD resulting from all samples collected was best fitted by the lognormal distribution, highlighting the complementarity of the canopy and the understorey fauna.

This result is important; it demonstrates that one must consider the canopy fauna for a

147 complete portrait of spider diversity in mature temperate hardwood forests. Differences in canopy species composition was in part linked to differences in structure and microhabitats found in sugar maple and American beech canopies. Some spider species were significantly more common in the canopy or the understorey. For example, the jumping spider Hentzia mitrata (Hentz) was, by far the most abundant spider in the canopy though, previously thought to be an uncommon understorey species. The canopy samples from Chapter 3 also yielded a specimen of the bolas spider {Mastophora hutchinsoni Gertsch) a species not known from Canada previously, as well as two new species records (Theridion alabamense Gertsch and.Archer; Araneus guttulatus

Walckenaer) previously not known from Quebec (Paquin et al. in press).

6.2.2 Ballooning propensity of canopy and understorey spiders

Chapter 4 served multiple purposes. It was meant to test if spiders living in the canopy and understorey have different ballooning propensity, and to identify which life history traits affect the balloon propensity of north-temperate hardwood forest spiders. These objectives were based on previous work demonstrating that generalist spiders and those associated with unstable open habitats had higher ballooning frequencies (Greenstone

1982; Bonte et al. 2003; 2006a). In Chapter 4,1 also identified processes responsible for the diversity patterns of the canopy and understorey assemblages, as documented in

Chapter 3. Chapter 4 also explored the explanatory powere of mixed ESS and risk- spreading (or bet-hedging) strategies with spider species that have populations in both habitats. Intraspecific variation in ballooning propensities indicated that different

148 dispersal strategies were maintained within the spider populations of both habitats.

Finally in Chapter 4,1 identified life history traits with the strongest effects on ballooning propensity of north-temperate hardwood spiders. Subsets of species with either limited or high dispersal capacities were created based on their life history traits. These species subsets were used in Chapter 5 to test predictions of metacommunity paradigms.

Results from Chapter 4 showed that habitat stability did not have a strong effect on spider ballooning propensity. Similar ballooning propensities in both habitats thought to experience different environmental conditions suggest the presence of mixed ESS in the dispersal mode of the populations from both habitats. The results of Chapter 4 lead me to reject increased risk spreading as a tactic in canopy or understorey spider populations.

Evidence of risk-spreading would have consisted of higher ballooning frequencies in canopy spiders to compensate for the less predictable nature of their habitat. Data in

Chapter 4 corroborate previous work suggesting that small body size and web-building have a strong positive effect on ballooning propensity (Greenstone 1987; Roff 1991). It indicates that ballooning, while deeply rooted in spider phylogeny, is a highly plastic behavioral trait. Development stage had a strong negative effect on species with large- bodied adults, but sex and seasonality did not influence ballooning propensity, contrary to conclusions of previous field studies. The results from Chapter 4 associating life history traits to ballooning propensity linked directly with Chapter 5 addressing multiple scale spatial diversity patterns of spiders within a metacommunity context.

6.2.3 Multiple spatial scale metacommunity dynamics

149 I consider Chapter 5 as the "flagship" study of the thesis. I relied on information from the previous chapters to test multiple predictions about species diversity patterns at different spatial scales. I investigated how vertical stratification and dispersal capacity influence diversity patterns across spatial scales. Results from Chapter 5 clearly demonstrate that dispersal capacity does not strongly influence diversity patterns of temperate hardwood forest spiders at either the tree or stand spatial scale. Species diversity patterns at these spatial scales are driven by species-sorting processes. Nonsignificant changes at the stand level in a- and P-diversity (mean number of species within and among stands) and significant changes in composition at the stand spatial scale suggest that niche availability

(space and resources) is the main driver of spider diversity at those spatial scales. Patch- dynamics and mass effects through increasing dispersal capacity become apparent at the site and regional scales. Mass-effects dynamics were related to my observation that SADs departed from the lognormal distribution, and shared increasing proportions of rare species. Changes in species composition and turnover in richness were significantly greater than predicted by random distributions and indicated that patch-dynamics reflected spatial aggregation of species and conspecifics. Generally speaking, according to Chapter 5 results, in north-temperate hardwood forests, space and dispersal capacity contribute significantly to spider diversity at the stand scale and beyond. Spider diversity has been repeatedly correlated to habitat complexity; however, results in Chapter 5 suggest that local spider diversity is also strongly affected by local factors related to species-sorting dynamics.

150 6.2 Conclusions and Suggested Future Directions

My work on canopy spider diversity of north-temperate hardwood forests shows that temperate canopy fauna is distinct and complementary to the rest of the spider fauna of north-temperate hardwood forests. It also demonstrates that passive aerial dispersal capacity influences spider diversity patterns mainly at the site and regional spatial scale in my study while local abiotic and biotic processes are strong determinants of spider diversity at the tree and stand spatial scales. This research depended on being able to access the canopy and collect large replicated samples in a short period of time over a regional scale. My thesis also demonstrates that spiders are ideal models for testing many different biological hypotheses, ranging from hypotheses about the evolution of local dispersal adaptations to the most recent theories on species diversity patterns. I hope that this thesis is only the tip of the iceberg in a much expanded study of temperate canopy arthropods in North America.

Future research in temperate canopy ecology should consider the following avenues:

• Direct measurements of abiotic conditions (temperature, moisture, light, and wind

speed) to compare environmental conditions in the canopy and understorey.

• Experimental manipulations of resource and space availability at local scales by

reducing or supplementing richness and composition of spiders in habitats of

reduced or enhanced structural complexity to provide insight about the species-

sorting dynamics that shape local community diversity.

151 • Population genetic studies of the common north-temperate hardwood species

distributed in the canopy and understorey at multiple spatial scales to test the

distinctiveness of canopy and understorey populations.

• Stable isotope marker studies could be used to map the vertical distribution of the

trophic levels in north-temperate hardwood forests and also track seasonal

movements of spider populations across vertical gradients in hardwood forests.

Ecological knowledge of temperate canopies ecology has lagged behind that for tropical canopies because the drastic seasonality in the temperate region results in a species-poor habitat. Erwin (1983) labeled tree canopies as the "Last Biotic Frontier" in ecology because it offered so many unknown species and potentially new ecological patterns. In temperate canopies, more complex ecological hypotheses can be tested, across broader spatial scales, as canopy diversity is easier to measure.

Members of many other insect orders were collected during the sampling for this thesis and these will be used, in the future, to produce the first inventories of these orders in canopies of north-temperate hardwood forests. Preliminary identifications in other insect groups by specialists already suggest that the canopy of the north- temperate forest is host to extremely rare species generally found in the extreme south of the Canadian border. Even though more data are needed, these first results suggest that northern range extension of species might be possible through canopy habitats as they may provide similar viable conditions to those found farther south. I could not have imagined this potentially new ecological pattern without my research into north-

152 temperate tree tops. Clearly, study of temperate canopies has a lot more to offer to the ecological world.

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163 8. Appendices

8.1 Species collected on foliage and trunk of sugar maple and American beech

canopy and understorey:

Pooled number of individuals and species sampled during the 2005 and 2006 sampling

seasons in the canopy and understorey of American beech and sugar maple trees in sugar

maple forests of southern Quebec, Canada. For Guild: W= Web-builder; H=Hunter, For

Disp.: High= High dispersal capacity; Lim.=Limited dispersal capacity, Hab.: Habitat in

which the species was collected, Beech: American beech, Maple: sugar maple, Unders.:

Understorey.

Beech Maple Family Species Guild Disp Hab. Foliage Trunk Total Canopy Under. Canopy Unders. Agelenidae Agelenopsis potteri (Blackwall) W High Both 3 27 1 33 39 25 64 Agelenopsis utahana (Ch. & Iv.) W High Both 0 9 1 23 17 16 33 Amaurobiidae Callobius bennetti (Blackwall) W Low Trunk 0 4 0 2 0 6 6 Coras aerialis Muma W Low Trunk 0 0 0 1 0 1 1 Coras montanus (Emerton) W Low Trunk 0 0 0 1 0 1 1 Araneidae Araneus corticarius (Emerton) W High Foliage 0 0 0 1 1 0 1 Araneus diadematus Clerck W High Foliage 5 6 2 15 28 0 28 Araneus guttulatus (Walckenaer) W High Foliage 1 0 3 1 5 0 5 Araneus marmoreus Clerck W High Both 2 50 3 48 102 1 103 Araneus saevus (L. Koch) W High Foliage 3 42 5 39 89 0 89 Araniella displicata (Hentz) W High Both 54 58 210 97 416 3 419 Cyclosa conica (Pallas) W High Both 32 57 27 78 192 2 194 Eustala anastera (Walckenaer) W High Both 14 8 15 8 42 3 45 Hypsosinga rubens (Hentz) W High Trunk 0 1 0 0 0 1 1 Larinioides cornutus (Clerck) W High Foliage 0 0 0 1 1 0 1 Larinioides patagiatus (Clerck) W High Foliage 1 0 1 0 2 0 2 Larinioides sclopelarius (Clerck) W High Foliage 0 0 1 1 2 0 2 Mangora placida (Hentz) W High Foliage 0 3 0 7 10 0 10 Mastophora hutchinsoni Gert. W High Both 2 0 1 0 1 2 3 Neoscona arabesca (Wale.) W High Foliage 6 7 2 2 17 0 17 Clubionidae Clubiona canadensis Emerton H Low Both 0 4 1 3 5 3 8 Clubiona obesa Hentz H Low Both 3 4 2 2 5 6 11 Clubiona pygmaea Banks H Low Both 4 0 3 0 1 6 7

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166 8.2 List of generalized linear dispersal models (Chapter 4):

Generalized linear dispersal models tested at species level analyses. Dev: Development stage, juvenile or adult; Size: spider body size; Hab. type: habitat where spider sampled, understorey or canopy; TOY: time of year of sample, spring, summer, and fall; Tree: tree species sampled, sugar maple or American beech.

Emblyna sublata (Hentz) models

Model Model ID Dev+Size+Hab. type+TOY + Dev:TOY + Size:TOY + Dev:Size 1 Dev+Size+Hab. type + Dev: Size 2 Size+Hab. type+TOY + SizeTOY 3 Size+Hab. type 4 Size+Hab. type+TOY 5 Dev+Size+TOY + DevTOY + SizeTOY + Dev:Size 6 Dev 7 Size 8 Hab. type 9 TOY 10

Tetragnatha versicolor Walckenaer models

Model Model ID Size + Hab. type 1 Hab. type 2 Size 3

Philodromus rufus vibrans Dondale models

Model Model ID Size + Tree + Hab. type 1 Size 2 Size + Tree + Hab. type + Tree:Hab. type 3 Size 4

Theridion murarium Emerton models

Model Model ID Size + Hab. type + dev + Size:dev 1 Size + Hab. type 2 Size + Hab. type + dev 3 Size 4 Hab. type 5 Dev 6

167 Salticidae models

Model Model ID Dev + Size + Hab. type + TOY 1 Size 2 Hab. type 3 Dev + Size + Hab. type + TOY + Dev:TOY + Size:TOY + Dev:Size 4 Size + Hab. type + TOY + Size:TOY 5 Dev + Size + Hab. type + Dev:Size 6 Size + Hab. type 7 Size + Hab. type + TOY + Size:TOY 8

Clubiona models

Models Model ID Size + Hab. type 1 Size 2 Hab. type 3 169