Effects of Productivity on Aquatic Food Webs by Colette L. Ward A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Doctor of Philosophy in Integrative Biology Guelph, Ontario, Canada © Colette Ward, April, 2014 ABSTRACT EFFECTS OF PRODUCTIVITY ON AQUATIC FOOD WEBS Colette L. Ward Advisor: University of Guelph, 2014 Professor Kevin S. McCann Ecologists have long sought to understand the effects of productivity on community structure, and the question remains an issue of pressing importance given contemporary patterns of anthropogenic change. Extensive debate has revolved around bottom-up (resource limitation) and top-down (predation) hypotheses for community response to productivity, with the latter now dominating our conceptualization of this question, especially in aquatic ecosystems. Key to this discourse is the principle that top-down control is a fundamental response of communities to rising productivity, and, in the absence of bottlenecks to energy flux, becomes stronger across productivity gradients. I argue that this principle, when projected onto commonly occurring food web motifs, readily predicts (a) common violations of assumptions of classical top-down hypotheses, and (b) that community responses to rising productivity are not conserved across productivity gradients, but are instead context-dependent. Here I use this principle to predict and explore the context-dependent nature of aquatic food web structure across large gradients of productivity. I show that food webs increasingly depart from the fundamental assumptions of classical top-down hypotheses with rising productivity (i.e. strong consumer-resource (especially producer-herbivore) interactions, linearity and singularity of food chains, rarity of omnivory, and productivity-driven lengthening of food chains). Alternative energy channels which arise with productivity subsidize generalist predators, which in turn mediate community structure. I demonstrate this at the scale of large, whole- ecosystem food webs, where increasing productivity is directed into bottom-up controlled detritus channels as primary producers become less edible, subsidizing generalist predators, which in turn exert top-down control on herbivores in an apparent trophic cascade. I also demonstrate this phenomenon in food webs at a sub-ecosystem scale, where subsidies from an alternative energy channel facilitate community compositional turnover from edible to less edible consumers across productivity gradients. I further show that rising productivity causes food chain length to decline as increasing energy flux begets top-heavy biomass pyramids, which favour omnivory. Overall this thesis suggests that, in contrast to conventional thinking, mechanisms of community response to productivity are not conserved across productivity gradients, and instead may be readily predicted by a simple framework for energy flux. ACKNOWLEDGEMENTS I am grateful to my advisor, Kevin McCann, for his support while I completed this thesis. Thanks for believing in me, for sharing your passion, and for introducing me to the beauty of mathematics. I am also grateful to my committee members Neil Rooney and Andrew MacDougall for their substantial guidance, mentorship, and support, and to John Moore for his thoughtful guidance in the early stages of this thesis. My work in seagrass systems would not have possible without the assistance, advice, and empirical insights of Susan Bell and members of her lab group at the University of South Florida. Thanks to the people who processed many of these samples in the lab (Lauren Jarvis, Erika Perrier, Jamie Simpson, Will Barbour, Carling Bieg, Brittney Pakkala) and especially to three fantastic field assistants (Gabriel Gellner, Ian Ward, and Lauren Jarvis). I was incredibly fortunate to be surrounded by good friends and colleagues in the McCann lab. Special thanks to the group who did our PhDs together: Carmen Lía Murall, Amanda Caskenette, Tyler Tunney, Gabriel Gellner, and Tim Bartley. Thanks for pushing me and inspiring me, for the laughs and friendship. Eric, je te remercie pour ton appui, ton encouragement, ton amitié, et ton amour. Merci de pendre soin de moi pendant que je préparais cette thèse. And finally, to my parents, thank you for instilling in me a love of learning and fascination with the world. Thank you for your love and support in everything I do. iii Table of Contents Prologue ................................................................................................................................ 1 Chapter 1. HSS Revisited: Bottom-up control in Detritus-based food chains facilitates Top- down control in Grazing Food Chains across a Productivity Gradient ................................ 12 1.1 Abstract...................................................................................................................... 12 1.2 Introduction ................................................................................................................ 13 1.3 Methods .................................................................................................................... 15 1.4 Results ...................................................................................................................... 18 1.5 Discussion ................................................................................................................. 19 1.6 References ................................................................................................................ 25 1.7 Figures ...................................................................................................................... 30 Chapter 2. A Mechanistic Theory for Food Chain Length .................................................. 35 2.1 Abstract ..................................................................................................................... 35 2.2 Introduction ............................................................................................................... 36 2.3 A Mechanistic Theory for Food Chain Length .......................................................... 37 2.3.1 Towards a General Theory for Food Chain Length ........................................... 37 2.3.2 Species Richness and FCL Mechanisms ........................................................... 37 2.3.3 An Energy-Driven Mechanism for Food Chain Length ...................................... 38 2.3.4 The Relationship between Existing Hypotheses and Energy-Driven FCL Theory .................................................................................................................................... 41 2.3.5 The Context Dependency of FCL: Ecosystem Size or Productivity? ................. 42 2.3.6 Summary ........................................................................................................... 44 2.4 Empirical Methods .................................................................................................... 45 2.4.1 Food Web Data .................................................................................................. 45 iv 2.4.2 Evaluating support for the Species Richness Mechanism for Food Chain Length .................................................................................................................................... 46 2.4.3 Evaluating predictions for the Energy Flux theory for Food Chain Length ........ 47 2.5 Empirical Results ...................................................................................................... 49 2.6 Discussion ................................................................................................................ 51 2.7 References ............................................................................................................... 54 2.8 Figures ..................................................................................................................... 59 Chapter 3. Seagrass Benthic Community Response to Eutrophication is characterized by Rising Dominance of an Inedible Consumer ....................................................................... 65 3.1 Abstract ..................................................................................................................... 65 3.2 Introduction ............................................................................................................... 66 3.3 Diamond modules in natural settings........................................................................ 68 3.4 Methods .................................................................................................................... 70 3.4.1 Study System ..................................................................................................... 70 3.4.2 Field Collections ................................................................................................ 72 3.4.3 Stable Isotope Analysis ..................................................................................... 74 3.4.4 Statistics ............................................................................................................ 75 3.5 Results ..................................................................................................................... 78 3.5.1 Eutrophication Gradient ...................................................................................... 78 3.5.2 The Focal Diamond Module............................................................................... 78 3.5.3 Alternative energy channels................................................................................... 79 3.5.4 Generalist consumer coupling into alternative energy channels ............................ 79 3.5.3 Compositional Turnover ..................................................................................... 80 3.6 Discussion ................................................................................................................ 81 v 3.7 References ............................................................................................................... 84 3.7 Figures ..................................................................................................................... 89 Epilogue .............................................................................................................................. 98 Appendix 1. Descriptions and Selection Criteria for Marine Food Webs derived from Network Models ................................................................................................................ 103 List of Figures Fig. 1.1. Predicted patterns for alternative hypotheses for trophic control in coupled grazing and detritus-based energy channels across a productivity gradient.................................... 30 Fig. 1.2. Relationships between total primary production and functional group biomass.. .. 31 Fig. 1.3. The relationship between total primary production and the fraction of top predator diets derived directly or indirectly from detritus. .................................................................. 32 Fig. 1.4. The relationship between total primary production and the fate of primary production. .......................................................................................................................... 33 Fig. 1.5. The relationship between total primary production and a) total herbivory among grazing channel consumers, and b) total predation on grazing channel consumers. ......... 34 Fig. 2.1. Equilibrium results from Eqn. 2.1 for the effect of increases in any a, e, or K on a) biomass pyramid shape, b) omnivory, c) food chain length, and d) stability (for systems with and without omnivory). ................................................................................................ 59 vi Fig. 2.2. The simultaneous effects of increasing ecosystem productivity (i.e. increasing K) and decreasing ecosystem size (i.e. increasing a ) on biomass pyramid shape, omnivory, PC and food chain length. ........................................................................................................ 60 Fig. 2.3. Summary of the context-dependent nature of food chain length across gradients of increasing energy availability .......................................................................................... 61 Fig. 2.4. The relationship between food chain length and fish species richness in a) marine bounded systems and b) lakes.. ............................................................................. 62 Fig. 2.5. The relationships between environmental gradients mediating energy flux and biomass pyramid shape, fish omnivory, and food chain length for marine bounded systems. ........................................................................................................................................... 63 Fig. 2.6. The relationships between food chain length and environmental gradients mediating energy flux for lake systems. .............................................................................. 64 Fig. 3.1. Predicted outcomes of rising productivity in a focal diamond module .................. 89 Fig. 3.2. Locations of Halodule and Thalassia meadows sampled. .................................... 90 δ15 Fig. 3.3. N values of epiphytic algae indicate gradients of increasing eutrophication in Halodule and Thalassia systems.. ...................................................................................... 91 Fig. 3.4. The relationship between eutrophication and biomass of members of the focal diamond module in Halodule and Thalassia systems:. ....................................................... 92 vii Fig. 3.5. The relationship between eutrophication and biomass of members of the alternative epiphytic algae energy channel: ........................................................................ 93 Fig. 3.6. The relationship between eutrophication and coupling of diamond module consumers into alternative energy channels. ...................................................................... 94 Fig. 3.7. Benthic community composition across eutrophication gradients in Halodule and Thalassia systems ............................................................................................................... 95 Fig. 3.8. Conceptual representation of seagrass community structure across the eutrophication gradient in Halodule systems sampled in 2010. . ....................................... 96 viii Prologue How does productivity structure ecological communities? This question has been a central focus of inquiry in ecology for 175 years (e.g. Liebig 1840, Haeckel 1866, Lotka 1925, Elton 1927, Volterra 1926, Lindeman 1942, Hutchinson 1959, Slobodkin 1961, Fretwell 1977, Persson et al. 1996) and remains a question of pressing importance given contemporary patterns of global change (e.g. anthropogenic changes in the cycling of limiting nutrients; Vitousek et al. 1997, Rabalais et al. 2009). The notion that resources limit the biomass and diversity of consumer populations, first articulated as Liebig’s Law of the Minimum (1840), was widely accepted and underlay ecologists’ conceptualization of nature for a century. This concept was later extended and formalized as the bottom-up control hypothesis (Elton 1927, Lindeman 1942), which predicted cascading bottom-up effects on the biomass of consumers at successive trophic levels (e.g. Elton’s pyramid of numbers). This bottom-up view of ecological communities was challenged when Hairston, Smith, and Slobodkin (‘HSS’; 1960), noting a ‘green world’ and pondering why herbivores do not simply remove all plant biomass, posited that predation prevents herbivore biomass from reaching levels permitting runaway grazing. Later refinement to this top-down control hypothesis recognized that energy transfers between trophic levels are inherently inefficient and therefore limiting. Rising energy inputs should therefore result in the addition of successive trophic levels of consumers, which would, in turn, control the trophic level immediately below, resulting in alternating patterns of top-down and bottom-up control of producer biomass with rising productivity and successive predator additions (Fretwell 1977, Oksanen et al. 1981, Oksanen & Oksanen 2000; the ecosystem exploitation hypothesis, or ‘EEH’). 1 This top-down (EEH) theory builds from 4 key assumptions: (i) that consumptive links between consumers and their resources, especially the link between herbivores and plants, are always strong, (ii) that food chains are linear, or that communities are accurately represented as single, unbranched food chains, (iii) that omnivory is rare, and (iv) that changes in productivity manifest foremost as changes in vertical diversity (i.e. the addition and subtraction of trophic levels, which alter food chain length) but not functional horizontal diversity (i.e. the addition and subtraction of parallel food chains). This top-down control theory has come to underlie much of our conceptualization of community structure and response to changing productivity, especially in aquatic ecosystems. However, the hypothesis has been controversial and has generated substantial debate. Primary producers and consumers often employ chemical, morphological, and behavioural defenses against grazing and predation, and rising productivity can facilitate the dominance of these defended groups (e.g. Phillips 1974, Lubchenco & Gaines 1981, Leibold 1989 & 1996, Van Donk et al. 2001, Karban et al. 2014). Because these defenses necessarily weaken consumptive interactions, their existence contradicts the fundamental assumption of the HSS and EEH hypotheses that consumer-resource links are always strong. Among producers, these defenses result in the accumulation of unconsumed biomass, which becomes detritus on senescence and fuels detritus-based food chains (Cyr & Pace 1993, Cebrian 1999). Grazing channels are often characterized by factors which facilitate top-down control, while detritus channels are often characterized by factors which facilitate bottom-up control (Strong 1992, Hairston & Hairston 1993, Polis & Strong 1996, Cebrian 1999, Shurin et al. 2006, De Bruyn et al. 2007); moreover, 2