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Major Patterns of Body Size Variation Within Arthropod Species: Exploring the Impact of Habitat, Temperature, Latitude, Seasonality and Altitude

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Major Patterns of Body Size Variation Within Arthropod Species: Exploring the Impact of Habitat, Temperature, Latitude, Seasonality and Altitude Major Patterns of Body Size Variation within Arthropod Species: Exploring the Impact of Habitat, Temperature, Latitude, Seasonality and Altitude Submitted in partial fulfilment of the requirements of the Degree of Doctor of Philosophy Curtis Robert Horne June 2017 I, Curtis Robert Horne, confirm that the research included within this thesis is my own work or that where it has been carried out in collaboration with, or supported by others, that this is duly acknowledged below and my contribution indicated. Previously published material is also acknowledged below. I attest that I have exercised reasonable care to ensure that the work is original, and does not to the best of my knowledge break any UK law, infringe any third party’s copyright or other Intellectual Property Right, or contain any confidential material. I accept that the College has the right to use plagiarism detection software to check the electronic version of the thesis. I confirm that this thesis has not been previously submitted for the award of a degree by this or any other university. The copyright of this thesis rests with the author and no quotation from it or information derived from it may be published without the prior written consent of the author. Signature: Date: 2nd June 2017 i Details of collaboration and publications Author contributions and additional collaborators are listed below for each chapter, as well as details of publications where applicable. This work was supported by the Natural Environment Research Council (NE/L501797/1). I use the term ‘we’ throughout the thesis to acknowledge the contribution of others. • Chapter 1: Curtis R. Horne wrote the chapter. • Chapter 2: Curtis R. Horne, Andrew G. Hirst and David Atkinson designed the study and wrote the paper. CRH collected the data and performed the statistical analyses. This chapter has been utilized in publication (see Appendix 7.1). • Chapter 3: Curtis R. Horne, Andrew G. Hirst and David Atkinson designed the study and wrote the paper. CRH collected the data and performed the statistical analyses. This chapter has been utilized in publication (see Appendix 7.2). • Chapter 4: Curtis R. Horne, Andrew G. Hirst, David Atkinson, Aitana Neves and Thomas Kiørboe designed the study and wrote the paper. CRH collected the data and performed the statistical analyses. This chapter has been utilized in publication (see Appendix 7.3). • Chapter 5: Curtis R. Horne, Andrew G. Hirst and David Atkinson designed the study and wrote the paper. CRH collected the data and performed the statistical analyses. • Chapter 6: Curtis R. Horne, Andrew G. Hirst, David Atkinson, Rodrigo Almeda and Thomas Kiørboe designed the study and wrote the paper. CRH carried out the experimental work, collected the data and performed the statistical analyses. • Chapter 7: Curtis. R. Horne wrote the chapter. Although not included as an official chapter, data collected as part of Chapter 2 was also used to examine the temperature dependence of sexual size dimorphism in arthropods. This work was predominantly led by Andrew G. Hirst, the findings from which were subsequently published. Given my contribution both as a co-author, and in collecting the data for this analysis, I also include a copy of this publication at the end of the thesis for reference (see Appendix 7.4). Finally, thank you to my PhD examiners, David Morritt and Christopher Hassall, for their helpful comments and feedback on the thesis. ii Patterns only emerge by ignoring the details. Lawton (1999) iii Major Patterns of Body Size Variation within Arthropod Species: Exploring the Impact of Habitat, Temperature, Latitude, Seasonality and Altitude Curtis R. Horne ABSTRACT Body size affects rates of most biological and ecological processes, from individual performance to ecosystem function. Within species, emergent body size patterns have been formalised into prominent biogeographical and biological rules, including James’ Rule (larger individuals are found at higher, colder latitudes), and the Temperature-Size Rule (individuals reared in warmer conditions grow to a smaller adult size). Body size also varies seasonally and with altitude. Yet, the patterns and drivers of these size gradients, and the degree to which they co-vary and share explanatory mechanisms, have never been systematically evaluated. We undertake the most comprehensive meta- analyses to date of temperature- and biogeographical-size clines within arthropod species. Aquatic species show greater reductions in body size with warming and decreasing latitude compared to terrestrial species, likely an adaptive response to deal with increased metabolic demand in the warm and the greater difficulty to uptake oxygen in water than in air. Voltinism explains variation in laboratory temperature- and latitudinal-size clines in terrestrial species. While size decreases with warming and with decreasing latitude in multivoltine terrestrial arthropods, size increases on average in univoltine species, consistent with predictions from size vs. season-length trade-offs. In the globally distributed sub-class Copepoda, seasonal temperature-size (T-S) gradients differ between current-feeding calanoids and ambush-feeding cyclopoids, suggesting that differences in the size- and temperature-dependence of alternative feeding strategies may influence the T-S response. Finally, through experimentation, we explore the progression of the T-S response of Copepoda during ontogeny. The T-S response is more strongly generated in particular life stages, and even reduced in some periods, providing evidence that the temperature-dependence of growth and developmental rates is modified during ontogeny. Ultimately, close similarities between T-S responses measured in controlled laboratory conditions, and seasonal and biogeographical size clines in the field across different arthropod taxa, suggests that these patterns share similar selective pressures. iv CONTENTS CHAPTER 1 1 General Introduction 1 CHAPTER 2 8 Temperature-size responses match latitudinal-size clines in arthropods, revealing critical differences between aquatic and terrestrial species Introduction 9 Methods 13 Results 17 Discussion 27 CHAPTER 3 34 Seasonal body size reductions with warming co-vary with major body size gradients in arthropod species Introduction 35 Methods 39 Results 47 Discussion 55 CHAPTER 4 62 A global synthesis of seasonal temperature-size gradients in copepods Introduction 63 Methods 68 Results 71 Discussion 83 v CHAPTER 5 89 Altitudinal body size trends in arthropods are much more variable than laboratory, latitudinal and seasonal temperature-size gradients Introduction 90 Methods 94 Results 97 Discussion 107 CHAPTER 6 114 Temperature-size responses signal rapid developmental shifts in the thermal- dependence of life history rates Introduction 115 Methods 117 Results 123 Discussion 130 CHAPTER 7 138 General Conclusions 138 References 148 vi FIGURES 2.1. Temperature-size responses and latitudinal-size clines in arthropod species, categorized by taxonomic order. 18 2.2. Species-specific temperature-size responses and latitudinal-size clines expressed as a function of organism dry mass. 20 2.3. Species-specific temperature-size responses and latitudinal-size clines categorized by voltinism. 22 2.4. Species-specific temperature-size responses and latitudinal-size clines vs. dry mass in terrestrial arthropods, categorized by voltinism. 24 2.5. Order-specific temperature-size responses vs. latitudinal-size clines in terrestrial and aquatic arthropods. 25 3.1. Examples of seasonal variation in adult dry mass and environmental temperature in multivoltine arthropods. 38 3.2. World map indicating the location of studies from which seasonal temperature-size gradients were recorded. 42 3.3. Comparison of aquatic and terrestrial seasonal temperature-size gradients with laboratory temperature-size responses and latitudinal-size clines in multivoltine arthropods. 48 3.4. Total proportional change in body mass vs. annual temperature range in aquatic and terrestrial arthropods. 50 3.5. Order-specific seasonal temperature-size gradients vs. laboratory temperature-size responses and latitudinal-size clines in arthropods. 52 4.1. World map indicating the location of studies from which seasonal temperature-size gradients were recorded. 72 4.2. Species-specific seasonal temperature-size and chlorophyll-size gradients averaged by taxonomic order. 75 4.3. Seasonal temperature-size gradients of adult copepods for individual species, including both males and females, categorized by order. 78 4.4. Species-specific seasonal temperature-size gradients expressed as a function of organism dry mass, categorized by taxonomic order. 80 4.5. Male and female species-specific laboratory temperature-size responses vs. seasonal T-S gradients in planktonic copepods. 82 5.1. The predicted effects of i) decreasing temperature, ii) decreasing oxygen partial pressure and iii) decreasing season length with increasing altitude on size at maturity in arthropods. 92 vii 5.2. World map indicating the location of studies from which altitudinal-size clines were recorded. 98 5.3. Altitudinal-size clines of individual arthropod species, including both males and females, categorized by taxonomic order and voltinism. 100 5.4. Order-specific altitudinal-size clines, divided by voltinism. 103 5.5. Mean altitudinal-size clines in arthropods with one generation or less per year vs. those with multiple generations per year, and in flightless vs. flying species. 104 5.6. Order-specific altitudinal-size clines
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