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Doctoral Dissertations University of Connecticut Graduate School

5-8-2020

What Makes a ‘Biodiversity Hotspot’ Hot? The Consequences of Trait Variation and Covariation for Individual Performance and Species Coexistence in South African

Kristen Nolting University of Connecticut - Storrs, [email protected]

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Recommended Citation Nolting, Kristen, "What Makes a ‘Biodiversity Hotspot’ Hot? The Consequences of Trait Variation and Covariation for Individual Plant Performance and Species Coexistence in South African Proteaceae" (2020). Doctoral Dissertations. 2520. https://opencommons.uconn.edu/dissertations/2520 What Makes a ‘Biodiversity Hotspot’ Hot?

The Consequences of Trait Variation and Covariation for Individual Plant Performance and

Species Coexistence in South African Proteaceae

Kristen M. Nolting, PhD

University of Connecticut, 2020

The Cape Floristic Region (CFR) in southwestern South Africa is a ‘biodiversity hotspot,’ hosting ~9,000 plant species in an area just over 90,000 km2. What is especially extraordinary about the CFR is that diversity here rivals that in many tropical forests, but it is not located in the highly diverse equatorial regions, making it difficult to identify the ecological and evolutionary processes that generate diversity and maintain it today. One way to better understand variation in species diversity across communities is to evaluate the distribution of the traits species’ possess.

Specifically, trait variation within and across species can indicate how organisms interact with both their abiotic and biotic environments.

For my dissertation I take a trait-based approach to identify how trait variation could influence the performance of in the CFR, and how traits might mediate ecological interactions so as to minimize competition and promote coexistence. I focus on fynbos communities dominated by plants in the family Proteaceae, a family that represents much of the species diversity and abundance in local communities. I identify functional relationships between plant traits, performance, and fitness in a multivariate framework. I find that within species Kristen M. Nolting – University of Connecticut, 2020

variation in traits related to performance might minimize fitness inequalities among co-occurring species, and that the covariance structure of traits might be important in leading to this outcome.

Lastly, I show that trait differences among neighboring individuals are important for predicting performance in local neighborhoods by possibly minimizing competitive effects and also promoting adaptation to the local environment.

What Makes a ‘Biodiversity Hotspot’ Hot?

The Consequences of Trait Variation and Covariation for Individual Plant Performance and

Species Coexistence in South African Proteaceae

Kristen M. Nolting

B.S., University of Evansville, 2010

M.S., Michigan State University, 2014

A Dissertation Submitted in Partial Fulfillment of the

Requirements for the Degree of

Doctor of Philosophy

at the

University of Connecticut

2020

Copyright by

Kristen M. Nolting

2020

ii APPROVAL PAGE

Doctor of Philosophy Dissertation

What Makes a ‘Biodiversity Hotspot’ Hot?

The Consequences of Trait Variation and Covariation for Individual Plant Performance and

Species Coexistence in South African Proteaceae

Presented by

Kristen M. Nolting, B.S., M.S.

Major Advisor ______

Kent E. Holsinger

Associate Advisor ______

Robert Bagchi

Associate Advisor ______

Cynthia S. Jones

Associate Advisor ______

John A. Silander Jr.

Associate Advisor ______

Mark C. Urban

University of Connecticut 2020

iii Acknowledgements

I want to first thank my family, who despite not fully understanding my desire to become a ‘plant doctor,’ has nonetheless supported me on this journey. To my mom, Michaele Nolting: thank you for always being my biggest supporter and cheerleader (I am sorry this journey took me so physically far from home!), and absolutely a fantastic field assistant (completing 1,500 stomatal peels is no easy task!). You are the strongest person I know, and from your example, I have learned that the best way to do a hard thing is to wake up, make some coffee, make a plan, and get to work. To my Dad, Jon Nolting: thank you for encouraging from a young age, my love for reading, writing, and story telling. To my brother, Jason Nolting: thank you for sharing my love of travel and desire to go on adventures and get to know the world. To my sister, Katy Nolting: thank you for your constant love and support, and for being the first to inspire my love of science. To my brother, Josh Nolting: thank you for always, always believing in me, and for sharing my love of nature (especially big, old trees!). To my nieces and nephews, thank you for being a bright spot for me during challenging times.

I want to thank those, past and present, in the EEB department at UConn. From you I have received tremendous mentorship, scholarship, and friendship. I especially need to thank

Elizabeth Jockusch, Carl Schlichting, Morgan Tingley, Paul Lewis, Louise Lewis, Sarah Knutie, and Erin Kuprewicz, who while not on my committee nevertheless were tremendously important for me reaching the finish line and staying somewhat sane along the way. I would also like to highlight the all star administrative team (Pat Anderson, you will always be a magical unicorn in my eyes, not just for your ability to solve any problem I might have, but for always having a hug, smile, and kind word for me on the most difficult days), the awesome students, faculty, and staff

iv with whom I collaborated on teaching (special thanks to Miranda Davis, Susan Herrick, Mary

Brescia, and Mary Ellen Petersen), the incredible greenhouse staff, and the super hero tech support team.

I also want to thank my lab family and the friends that became family along the way.

Nora Mitchell, thank you for always having an answer to any question I had (especially early on, when I was learning the ropes), being ever supportive and encouraging, and always down for a

‘lunch beer’ on a bad day. Katie Taylor, Kaitlin Gallagher, and Lauren Stanley: thank you for the often-needed ice cream breaks, dinners, walks around campus, and constant support and love over the last several years. I have to especially thank Tanisha Williams who I first got to know as my brilliant, dedicated, and awesome lab sister, but who I am fortunate to have since gotten to know as a ‘bad ass’ field assistant, housemate, and the best friend I could have made during my time here in Storrs. I could not have done any of this without you and ‘our boys’ (#Monte #Carlo

#BayesCats). Thank you to my “fr-amily” who I got to know and love from my time in

Michigan: Emily Dittmar, Heather Stadden, and Carina Baskett you are the best friends I could have or know. I look forward to being able to take a vacation with you all now that I am

[hopefully] going to be less stressed and more open to fun and laughter.

Thank you to my colleagues and friends in South Africa, who not only made this research possible, but who helped make my field work an [mostly] enjoyable and always a tremendously fun experience. I have to especially thank Tony Rebelo, Pat Holmes, Guy Midgley, Martina

Treurnicht, Jasper Slingsby, Karen Esler, and other colleagues and support staff at the University of Cape Town, Stellenbosch University, SANBI, and Cape Nature. Guy, particularly, I could not have done this work without your support: both with respect to loaning me lab space and equipment, teaching me how to trouble-shoot using said equipment (I will forever remember

v how you walked me through LiCor ‘surgery’ on ‘Pandora’ over the phone during my first real week of field work), and also just being tremendously supportive and encouraging along the way. Your energy and enthusiasm for all things science, and especially fynbos, is contagious.

Lastly, I need to thank my committee. Cindi Jones, thank you for teaching me SO many amazing things about plants that I had never considered. Because of your teaching and mentorship, I finally feel confident owning the #iamabotanist label, and I love passing on what I have learned from you both in and out of the classroom to other aspiring botanists. To John

Silander, thank you for being my ‘Devil’s Advocate,’ but always in a way that pushed my science farther, even if I found it frustrating in the moment. To Robi Bagchi and Mark Urban: thank you for always being willing to talk through difficult conceptual problems, quantitative problems, and challenging me to bring my research into the context of the broader literature.

Finally, I have to thank my advisor, Kent Holsinger. I often joke that I decided to come to

UConn for the basketball (and I have sure loved being able to support the UConn women’s basketball team in person the last six years!), but in actuality, I came specifically because I wanted to work with Kent. Kent, you are one of the most brilliant people that I have ever met, but also have the rare phenotype of simultaneously being incredibly humble, kind, and generous.

You have taught me so much. You taught me that I don’t actually hate math, models, statistics, and theory (you tricked me into this, I think…). You encouraged me to go after the questions I found most interesting. You let me struggle, but never too much (it is all about the ‘productive struggle’ after all). You never were able to teach me how to be a morning person…but I am still working on it. You inspired me to have confidence in myself, and also inspired me to have confidence that science can be a fun place to work, and there is a place for me in it. Thank you for everything.

vi

“It is interesting to contemplate an entangled bank, clothed with many plants of many kinds, with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other, and dependent on each other in so complex a manner, have all been produced by laws acting around us.”

Darwin (1859)

"In all works on Natural History, we constantly find details of the marvellous adaptation of animals to their food, their habits, and the localities in which they are found. But naturalists are now beginning to look beyond this, and to see that there must be some other principle regulating the infinitely varied forms of animal life. It must strike every one, that the numbers of birds and insects of different groups, having scarcely any resemblance to each other, which yet feed on the same food and inhabit the same localities, cannot have been so differently constructed and adorned for that purpose alone. Thus the goat-suckers, the swallows, the tyrant fly-catchers, and the jacamars, all use the same kind of food, and procure it in the same manner: they all capture insects on the wing, yet how entirely different is the structure and the whole appearance of these birds!”

Wallace (1853)

“Alles ist blatt.” – All is leaf.

Goethe (1787)

vii TABLE OF CONTENTS

INTRODUCTION………………………………………………………………………………...1

Outline of Chapters………………………………………………………………………..6

Significance…………………………………………………………………………..……8

References…………………………………………………………………………………9

CHAPTER 1: Intraspecific trait variation influences physiological performance and fitness in the

South Africa shrub genus (Proteaceae)………………………………………….……….15

Title Page…………………………………………………………………………...……16

Abstract……………………………………………………………………………….….17

Introduction……………………………………………………………………...……….19

Materials and Methods…………………………………………………………...………21

Statistical Analyses………………………………………………………………………30

Results……………………………………………………………………………………33

Discussion………………………………………………………………………….....….38

Conclusions………………………………………………………………………………42

Acknowledgements………………………………………………………………………45

References…………………………………………………………………………..……46

Tables…………………………………………………………………………………….52

Figures……………………………………………………………………………...…….54

Supplementary Materials………………………………………………………...………59

CHAPTER 2: Multiple ways to ‘pet’ a cat: trait covariances promote functional and species diversity within plant communities by producing similar individual performance……...………64

viii Introduction………………………………………………………………………………64

Materials and Methods……………………………………………………………...……67

Results……………………………………………………………………………………73

Discussion…………………………………………………………………………..……76

Conclusions………………………………………………………………………………80

References……………………………………………………………………………..…82

Tables……………………………………………………………………………….……95

Figures……………………………………………………………………………………98

CHAPTER 3: Individual-level trait differences mediate density effects among co-occurring shrubs and may promote coexistence in a ‘biodiversity hotspot’………………………………102

Introduction………………………………………………………………………..……102

Materials and Methods…………………………………………………………….……105

Results……………………………………………………………………………..……111

Discussion………………………………………………………………………………115

Conclusions…………………………………………………………………………..…122

References………………………………………………………………………………124

Tables………………………………………………………………………………...…135

Figures………………………………………………………………………………..…138

ix Introduction

The excitement generated through the exploration and identification of earth’s biodiversity has arguably been the most influential muse moving ecological and evolutionary research forward.

Darwin (1859), Wallace (1853), and even the poet-turned-developmental-morphologist van

Goethe all took inspiration from the diversity they encountered in the natural world. While there is often an emphasis on identifying the total numbers of species in different places around the world, what these early workers observed – along with so many before and after them – was that the diversity of form and function of organisms is equally exciting and perhaps more inspiring, as it can help us to understand how these natural entities have come to be and how they persist in their environments in the present day. While the function of certain aspects of variation in form and function can be quite obvious (e.g. birds having hard beaks to help them crack open seeds) the function of other aspects of trait variation remain somewhat more elusive without more careful study (e.g. the slight variation in beak shape that makes some individuals better able to crack open large seeds versus small seeds). It is important to not only characterize trait variation within and among species to understand the taxonomic relationships among species, but this variation can also have significant functional roles for both the organism and the ecosystem in which it occurs.

Functional traits are morphological, physiological or behavioral aspects of an organism that provide an indication of how a species is linked to its abiotic and biotic environment (Violle et al., 2007). In plant ecology, functional traits have been measured extensively and there is evidence of relationships between traits and physiology and between traits and environmental covariates across both global and taxonomic scales (Reich et al., 1997; Wright et al., 2004;

1 Chave et al., 2009). Additionally, functional traits may be used to suggest how species partition niche space in local communities, aiding in continued coexistence. For example, variation in beak size in Galapagos finches (Lack, 1947), variation in body size in Anolis lizards in the

Caribbean (Schoener, 1968), and Sonoran Desert rodents (Brown, 1975; Bowers and Brown,

1982) reflect differences in species that enable them to acquire resources and share habitats differently, and thus presumably coexist.

In plant communities, the variation in morphological and structural traits among co- occurring species in tropical rainforests often spans the breadth of variation in traits observed across all of angiosperm species (Marks and Lechowicz, 2006). The observation that a single community can host such a high degree of trait variation has led to the conclusion that trait differences among species within a community maintain coexistence through niche partitioning.

However, there are also instances in which the trait composition of communities is much more narrow than would be expected (Kraft et al., 2008), which may indicate that species have similar traits that allow them to persist in a shared environment.

A common conclusion used to justify these contrasting results is that certain traits reflect variation needed for niche partitioning, while others reflect larger-scale adaptations to an environment that are shared by all members of the community (Swenson and Enquist, 2009). An alternative explanation could be that the measured traits are not actually associated with overall performance measures and are not related to fitness within a given environment. Thus evaluating patterns of trait distributions to infer processes leading to observed community structure may not be appropriate without first identifying the degree to which the measured traits matter for plant performance (Ackerly et al., 2000). Further, trait differences among species are often evaluated in isolation, such that a difference between a pair of species in a single trait is associated with a

2 difference in a single aspect of their physiology, reflecting how these species differ on a single niche axis. Recent