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The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance

Journal: Philosophical Transactions B

Manuscript ID: RSTB-2012-0442.R1

Article Type: Review

Date Submitted by the Author: n/a

Complete List of Authors: Connell, Sean; The University of Adelaide, Earth & Environmental Sciences Kroeker, Kristy; University California, Davis, Bodega Marine Lab Fabricius, Katharina; Australian Institue of Marine Science, Kline, David ; Scripps Institution of Oceanography, Russell, Bayden; University of Adelaide,

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OCEAN

Subject: Ecology < BIOLOGY

Keywords: phase shifts, indirect effects, habitat loss

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Submitted to Phil. Trans. R. Soc. B - Issue

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The other ocean acidification problem: CO2 as a resource among competitors for 1

ecosystem dominance 2

3

Sean D. Connell1,*

, Kristy J. Kroeker2, Katharina E. Fabricius

3, David I. Kline

4, and 4

Bayden D. Russell5 5

6

1 Sean D. Connell, Southern Seas Ecology Laboratories, DP418, School of Earth and 7

Environmental Sciences, The University of Adelaide, Adelaide, South Australia 8

5005, Australia 9

2 Kristy J. Kroeker, Bodega Marine Laboratory, University of California Davis, 2099 10

Westside Road, Bodega Bay, CA 94923, USA 11

3 Katharina E. Fabricius, The Australian Institute of Marine Science, Townsville, 12

Queensland, Australia 13

4 David I. Kline, Scripps Institution of Oceanography, University of California, San 14

Diego, Integrative Oceanography Division, 9500 Gilman Drive, MC 0218, La 15

Jolla, CA 92093-0218 16

5 Bayden D. Russell, Southern Seas Ecology Laboratories, DP418, School of Earth 17

and Environmental Sciences, The University of Adelaide, Adelaide, South 18

Australia 5005, Australia 19

20

Short title: CO2 as a resource among competitors for ecosystem dominance 21

Key words: carbon dioxide, competition, phase-shift, multiple stressor 22

23

* Corresponding author ([email protected]) 24

25

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ABSTRACT 26

Predictions concerning the consequences of the oceanic uptake of increasing 27

atmospheric carbon dioxide (CO2) have been primarily occupied with the effects of 28

ocean acidification on calcifying organisms, particularly those critical to the 29

formation of habitats (e.g. coral reefs) or their maintenance (e.g. grazing 30

echinoderms). This focus overlooks direct and indirect effects of CO2 on non-31

calcareous taxa that play critical roles in ecosystem shifts (e.g. competitors). We 32

present the model that future atmospheric [CO2] may act as a resource for mat-33

forming algae, a diverse and widespread group known to reduce the resilience of kelp 34

forests and coral reefs. By combining laboratory and field CO2 experiments we 35

interpret this possibility against ‘natural’ volcanic CO2 vents. We show that mats 36

show enhanced productivity in experiments and had more expansive covers in situ 37

under projected near-future CO2 conditions both in temperate and tropical conditions. 38

The benefits of CO2 likely vary among species of producers, potentially leading to be 39

shifts in species dominance in a high CO2 world. We explore how ocean acidification 40

combines with other environmental changes across a number of scales, and raise 41

awareness of CO2 as a resource whose change in availability could have wide-ranging 42

community consequences beyond its direct effects. 43

44

1. INTRODUCTION 45

Ecosystem collapses often go unanticipated because their drivers are unrecognized, 46

have indirect effects, or combine in unexpected ways to alter interactions between key 47

species [1, 2]. To redress this uncertainty, much work has been done to identify and 48

quantify stressors and their cumulative effects by observing historical change [review 49

on ecosystem collapses, 3], experimentally manipulating drivers [review of synergies, 50

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4] and modeling their outcomes [alternate stable states, 5]. By combining such lines 51

of evidence, ecologists have demonstrated the tractability of identifying drivers of 52

change [6] to develop frameworks for anticipating or managing change [7] 53

54

Ocean acidification, a result of rising carbon dioxide (CO2) [8], is a particularly 55

vexing stressor to assess as a potential driver of future ecosystem change [9]. This is 56

because ocean acidification represents a series of changes in seawater chemistry, with 57

each alteration representing a potential driver of change [10]. The diminishing 58

availability of carbonate ion (CO32), and ensuing reduction in calcium carbonate 59

(CaCO3) saturation states are widely reported to reduce calcification in organisms 60

ranging from small plankton and invertebrates to large habitat-forming species such 61

as corals [11, 12]. To date, much of the focus of ocean acidification research has 62

been on the response of calcifiers, both algae and invertebrates to the changing 63

carbonate system, with a particular pre-occupation on one property: the hydrogen ion 64

concentration [H+], which is frequently reported as pH due to the relative ease of its 65

measurement. Initial insights were derived from manipulative experiments, 66

particularly single-factor manipulations of CO2 levels (i.e. pH) that assess change 67

from a physiological and often single species perspective. These assessments 68

highlight the vulnerabilities of calcifying organisms [e.g. review, 13] and consider the 69

potential extent of ecological change [14]. 70

71

Whilst there is recognition that ocean acidification may alter net primary production, 72

via the increased solubility of biogenic calcareous structures and reduced survival of 73

calcifying species that consume algae [11, 15], it may also alter production via 74

directly, especially under elevated temperature [16]. Several reviews now recognize 75

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that ocean acidification can increase carbon fixation rates in some photosynthetic 76

organisms [review, 17, 18], however, the ecological implications of this increase are 77

largely untested. Thus, CO2 may not only act as a stressor, but also as a resource. 78

CO2 may not only limit primary productivity, but also the growth rates of a 79

population. Because such effects are variable among species there is an enormous 80

potential for shifts in species dominance, as some species gain a relative advantage 81

from their response to elevated CO2. Indeed, alteration of resource availability has a 82

fundamental role in regulating the productivity of individuals, populations and, 83

ultimately, communities [19]. 84

85

2. CO2 AS A CARBON RESOURCE 86

CO2 can act as a resource by increasing carbon fixation rates in some photosynthetic 87

organisms. The degree to which this occurs is dependent on the carbon capture 88

strategies and the degree to which carbon is limiting [review, 18]. The relationship 89

between aqueous CO2, photosynthesis, and growth is not simple because not all 90

photosynthesising species require environmental CO2 for their source of carbon (C). 91

The majority of marine algae have carbon concentrating mechanisms (CCMs) that 92

facilitate the active influx of CO2 and/or bicarbonate ions (HCO3-) and elevate C 93

concentrations at the site of C fixation (i.e. Rubisco), with few algae being CO2-only 94

users [20, 21]. For these reasons there has been uncertainty regarding whether algae 95

with CCMs will benefit from CO2 enrichment [22]. 96

97

Despite the prevalence of CCMs, evidence suggests that many algae do respond 98

positively to increasing CO2 [12]. Indeed, the ability of some algae with CCMs to 99

benefit from enriched CO2 lends insight into the potential mechanisms for CO2 100

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effects. Species with CCMs can shift away from HCO3- towards aqueous CO2 when 101

CO2 levels are high [23]. Thus, aqueous CO2 may facilitate CCM C-acquisition or 102

make it less energetically costly, and this capacity varies among species [24]. Such 103

variation among species may be due to species-specific variation in CCMs themselves 104

[25, 26] or the ability of species to acquire other limiting resources (e.g. light or 105

nutrients) [27]. 106

107

As human activities modify environmental conditions, and therefore resource 108

availability, some species of algae may be released from carbon limitations while 109

others are not [28]. This mismatch has the potential to affect competitive abilities and 110

alter community structure. Moreover, the effects of these shifts would be particularly 111

profound if key functional groups, whose interactions structure entire communities, 112

experience contrasting resource limitations. 113

114

Falkenberg et al. [29] reveals how variability in resource limitation may play a 115

substantial role in ‘kelp-to-turf’ phase shifts. Kelps were shown to be limited by a 116

single type of resource (e.g. only nutrients and not CO2), while their alternate state 117

(characterized by turf algae) was co-limited by both nutrients and CO2. This 118

difference in carbon limitation demonstrates the potential for elevated CO2 to 119

influence turf expansion [e.g. 30], especially when amplified by human activities that 120

also increase nutrient loads [31]. This response is characteristic of co-limitation by 121

multiple resources [32]. Therefore, ocean acidification is unlikely to act alone, but 122

instead acts in concert with other environmental conditions (e.g. nutrient pollution) 123

and primary consumers (i.e. herbivores). 124

125

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Indeed, there are a large number of resources that constrain the abundance of marine 126

[review of algae, 33] and terrestrial plants [review, 34] and determine the composition 127

of space-holding species. Combinations of two or, sometimes, three of these limiting 128

factors are often incorporated into models to account for the diversity and 129

composition of plant communities [review, 35]. Thus, interspecific variation in 130

resource requirements is likely to affect relative species abundances in complex 131

communities. Changes in any of these constraints could alter the probability of phase 132

shifts, particularly as many resources are undergoing large, rapid changes because of 133

human activities [36]. 134

135

Mat-forming algae (here defined as low-profile ground-covering macroalgal and turf 136

communities) are fast-growing and effective space competitors in kelp forests and on 137

coral reefs. The hypothesis that phase-shifts towards mat-forming algae are likely to 138

be more common under conditions of high [CO2] is therefore of particular interest. If 139

this model has validity, then enhanced CO2 should cause mats to increase their extent 140

and productivity in both temperate and tropical systems. Supporting evidence 141

requires field observations of natural variation in [CO2] to provide insight into ocean 142

acidification effects at the ecosystem level (e.g. CO2 seeps), and field and laboratory 143

manipulations to establish the physiological reasons for such an effect [e.g. 37]. Until 144

now, such a combination of evidence has not been strongly pursued. 145

146

3. OCEAN ACIDIFICATION AS AN INDIRECT AGENT 147

While categorizing the effects of ocean acidification into direct negative effects (i.e. 148

on calcifiers) and positive effects (i.e. on non-calcifying algae) provides a conceptual 149

starting point, it is manifestly overly simplistic to forecast community persistence or 150

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change. While the detection of direct effects is readily achievable, it will not 151

necessarily shed light on the drivers that will play predominant roles in shaping future 152

communities relative to indirect effects [38]. Indirect effects not only yield 153

“unexpected results”, but also some of the strongest ecological effects (i.e. phase-154

shifts) that have been regarded as “catastrophes” on coral reefs [39] and “collapses” 155

of kelp forests [40]. They are often unanticipated because the impact of one 156

component (e.g. ocean acidification) on another (e.g. kelp decline) requires 157

knowledge of a third species (e.g. kelp-competitors) or mediating factors (e.g. 158

interactions among stressors), which are poorly understood (Figure 1). 159

160

Whilst the indirect climate effects on species interactions were initially surprising 161

[41], we are starting to learn that they commonly lag behind the more intuitive and 162

easily detectable direct effects, and can even reverse the direct climate effects of 163

climate [14, 42]. To date, most research on ocean acidification has focused on the 164

direct environmental impacts on individual species of iconic status (e.g. corals), but 165

the capacity for indirect effects to drive change may rival the known direct effects 166

[38]. 167

168

The indirect effects of ocean acidification may be especially important in 169

communities where CO2 can act as a resource and change competitive outcomes. 170

Competitive ability is contingent on the relative availability of resources and the 171

tolerance to environmental stress. Dominance may switch between subordinate 172

species and their normally dominant competitors, or even change competitive 173

interactions into facilitated interactions [43]. Studies of volcanic CO2 vents reveal the 174

potential for altered competitive balances between space-holders at projected near-175

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future levels of CO2 [750 ppm, 44]. In particular, these studies reveal the potential for 176

increased dominance of mat-forming macroalgae in low pH environments in 177

temperate [45] and tropical zones [46]. 178

179

Indirect effects that account for phase-shifts can be classified into two broad classes: 180

those driven by strong consumer effects (i.e. trophic cascades) and those driven by 181

strong producer effects (i.e. dominance of space) [review, 38]. The former class has 182

attracted considerable attention in both tropical and temperate systems [e.g. 47], but 183

there is profound and widespread variation in its explanatory power [reviews of 184

phase-shifts on coral reefs 48, and kelp forests 49]. Whilst there is merit in 185

understanding the future role of acidification on consumers and potential trophic 186

cascades, there is also merit in examining the breadth of direct and indirect producer 187

effects (Figure 1). This review provides an alternative framework for forecasting 188

community-level impacts of ocean acidification by focusing on producers’ responses 189

through the lens of phase-shifts in kelp forests and coral reefs. By ‘kelp forests’ we 190

refer to canopies of brown seaweeds, including Laminariales and Fucales. 191

192

Our present understanding of the physiological effects of ocean acidification is 193

primarily based on results obtained from closed experimental systems, particularly 194

small laboratory experiments. Beyond physiological predictions, larger field 195

mesocosm studies enable tests of direct and indirect effects that can modify the 196

persistence of species and functional relationships. Together, such experimental 197

knowledge can be compared against the pattern observed in natural systems. Such 198

investigative frameworks have been established in the discipline of macroecology 199

[50] in response to the persistent need to scale from small to larger experimental units 200

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and ultimately ecosystems [51]. For ocean acidification research, this challenge is 201

particularly vexing because the logistic constraints on manipulating large volumes of 202

aqueous CO2 places upper limits on tests of combinations of multiple stressors and 203

species. Thus, there is considerable discussion on methods that integrate experimental 204

research across laboratory, mesocosm and field systems to unravel the complexity of 205

functional relationships under future environmental conditions [9]. Nevertheless, the 206

key question for ecosystems is not just based on the direct effects and fate of 207

individual species, but the stability and persistence of the system as a whole. 208

209

4. MAT-FORMING ALGAE AS COMPETITIVE DOMINANTS 210

We focus on a group of fast-growing algae with quick rates of invasion and growth 211

and wide physiological tolerance. We classify these relatively low-lying algae in a 212

single term, ‘mats’ or ‘mat-forming algae”, to emphasize their similar physiological 213

and ecological properties across the temperate and tropical communities. We propose 214

that if we can identify similarities that occur between kelp forests of the temperate 215

zone and coral reefs of the tropical zone, we open a broader avenue of enquiry about 216

the potential effects of environmental change via altered productivity. 217

218

Mats are characteristically small, with high surface area to volume ratios and high 219

demand for resources relative to surrounding kelps and corals. Physiologically, they 220

require increased resource availability [e.g. nutrients, 52] to enable their normally 221

ephemeral status to become competitively superior to perennial species of kelps and 222

corals. The taxonomic identity potentially includes many tens to hundreds of species 223

[53] from many lineages. Despite their taxonomic diversity, similarities in their 224

biology have been found to be sufficiently large that authors have consistently 225

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referred to them as ‘turf-forming algae’ or ‘turfs’, ‘epilithic algal matrix’ or ‘mats’ 226

[53]. These terms emphasize the carpet-like nature of these algae which we call 227

‘mats’. 228

229

The ‘coral-algal phase shift’ occurs as a function of reduced herbivory and water 230

quality that independently, or in combination, enhances net production of algae [54]. 231

Ephemeral algae that form dense carpet-like mats are a key mechanism that creates 232

physically stressful conditions for corals [55, 56]. On the Great Barrier Reef, ‘mats’ 233

of algae (10 – 50 cm high) that bloom across large areas of coral reefs on coastal and 234

inshore fringing reefs [56] as well as the idiosyncratic role of turfs (5 – 10 cm high) 235

are known to overgrow established corals and prevent coral recruitment [57]. In the 236

Caribbean, greater emphasis is placed on turf-forming algae that are comprised of 237

filaments of benthic algae and cyanobacteria (< 1 cm high) that prevent settlement of 238

coral planulae [58]. 239

240

Kelps and corals form three-dimensional structures that are episodically disturbed and 241

readily reassemble after natural disturbances. The loss of corals and kelps can occur 242

when mats of algae colonising bare substrata after a disturbance, hence preventing 243

recruitment by occupying purchases for attachment and smothering remnant corals. 244

Many mat-forming species are normally subordinate to kelps and corals (e.g. 245

ephemeral or early successional species) but increased resource availability enable 246

their physiology and life history to become competitively superior [31, 59]. 247

248

The ‘kelp-turf phase shift’ occurs on coasts associated with water pollution because 249

the altered water conditions favour a suite of turf-forming species, which due to their 250

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physiology (i.e. fast uptake of nutrients) and life history (ability to withstand high 251

sediment loads) are well suited for polluted environments [31, 60-62]. These ‘turfs’ 252

are similar to the types of ‘turfs’ on Caribbean coral reefs [i.e. 63] in that nutrient 253

overloading also causes turfs to expand over extensive areas and subsequently cause 254

recruitment failure of the primary habitat in kelp forest [59] and coral reef systems 255

[63]. 256

257

5. LINES OF EVIDENCE: CO2 INCREAESES NET PRODUCTIVITY 258

(a) Comparison among methods; vents vs. field mesocosms vs. laboratory 259

Here, we compare the effects of CO2 enrichment on mat-forming algae among several 260

projects, combining findings from laboratory experiments and mesocosms with those 261

of natural field studies. For field studies, we use observations of benthic communities 262

around volcanic seeps that have been shaped by decades-long exposure to fine bubble 263

streams of CO2 seeping from the seabed, which cause local alterations in the seawater 264

chemistry [45, 46]. These seep sites complement and improve the interpretive value 265

of laboratory experiments. While lab studies can be carefully controlled, the range of 266

testable ecological interactions is quite limited. Conversely, field studies at CO2 vents 267

include interactions within acclimatized natural communities, but spatial and temporal 268

variation in pH does not behave exactly the same as future ocean conditions [64]. 269

The limitations of lab and field assessments suggest that combining both approaches 270

will provide a more informed model. 271

272

Our comparisons focus on benthic communities exposed to similar elevations in CO2 273

concentrations that are within the forecasted range of change by the end of this 274

century [44, 65]. Relative to ambient conditions (8.0-8.1 pHT), two levels of 275

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projected future pH were compared in warm temperate [Mediterranean, 45] and 276

tropical regions [Papua New Guinea, 46] (Table 1). The future pH conditions were 277

chosen to represent the projected near future conditions anticipated for the end of the 278

21st Century (pCO2 ~ 580-1080 pCO2, depending on emission scenarios, IPCC 2007). 279

Near future conditions were represented as 7.7-7.8 pHT (temperate) and 6.8 – 7.8 pHT 280

(tropical). Experimental mesocosms in temperate [24] and tropical zones [i.e. the 281

Coral Proto -Free Ocean Carbon Experiment, 66] are compared to the vents and their 282

laboratory counterparts (Figure 2). 283

284

Experimental and observational results are not directly comparable because they 285

estimate responses from mats grown over different periods of time using different 286

techniques. Laboratory experiments used similar techniques [16], but mesocosm 287

experiments used floating docks in temperate conditions [24] and a Free Ocean 288

Carbon Experiment in tropical conditions [66]. Observations at volcanic vents 289

quantified the percentage cover of mats within space that would otherwise be suitable 290

for recruitment (e.g. coral planualae settlement on space lacking live coral). At 291

tropical vents, mats were quantified within 25××××25 cm quadrats randomly assigned 292

among reef without live coral. At temperate vents, mats were quantified after 3.5 293

months of development on uncolonised 15××××15 cm volcanic rock tiles [45]. 294

295

(b) General CO2 effects on net production of mats 296

Mats responded positively to conditions of ocean acidification among all studies 297

reviewed here. Mats covered nearly 40% more space at temperate vents and 50% 298

more space at tropical vents (Fig 2a, b). In both cases, mats expanded their covers 299

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from a minority space holder (i.e. ∼10-20% cover), to a majority space holder (i.e. 300

∼60%) regardless of sources of loss. 301

302

The effect of enriched CO2 in field mesocosms was to increase rates of growth (mg 303

per day dry weight) by 2-3 times that of ambient conditions (Fig 2c, d). In the 304

laboratory, net productivity was substantially greater, probably due to fewer sources 305

of loss (e.g. herbivory), but the increased growth rate under enriched treatments was 306

about twice that of ambient conditions (Fig 2e, f). These consistently strong effects 307

suggest that CO2-induced increases in productivity maybe quite general among a class 308

of algae renown for its taxonomic diversity, variation in morphology and life-history 309

characteristics. 310

311

An unexpected and preliminary result is the similarity in magnitude of response 312

between climes and experimental protocols (i.e. effect-sizes based on relative change 313

in growth or percent cover between ambient and elevated CO2 conditions ranged from 314

0.70 to 0.88; Table 1). We caution over interpretation of these similarities because 315

the responses are derived from mats grown over different periods of time (Electronic 316

Supplementary Material 1). In addition, the magnitude of CO2-induced increases in 317

productivity is likely to be contingent on the availability of nitrogen and light, as well 318

as species identity. Nevertheless, the consistency in direction of strong effects is 319

clearly suggestive that mat-forming algae have the potential to respond positively to 320

predicted levels of CO2. 321

322

323

324

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(c) CO2 effects on community composition and cover 325

Mat-forming algae appeared to expand (i.e. higher percentage cover) under projected 326

near-future conditions at CO2 seeps, regardless of any differences in herbivory 327

(Fig. 2). At the temperate vents, estimates of percent cover of mats on the natural 328

substrate were similar among ambient and low pH zones [mean percent cover was 329

26% and 33% respectively, 45]. However, the differences among these zones were 330

readily apparent in a study of succession, which monitored the development of rocky 331

reef assemblages on uncolonised tiles of rock in each pH zone. During succession, 332

calcareous taxa (primarily crustose coralline algae and barnacles) maintained similar 333

percent cover in both the ambient and low pH zones for the early stages of succession 334

(until approximately 3.5 months) but were rapidly overgrown by mat-forming algae 335

(Fig. 2) in the low pH zone during the later stages [45]. At the tropical vents, mats 336

were comprised of non-calcifying macroalgae which were more expansive under near 337

future conditions than at control sites (Fig. 2), whilst calcareous algae showed the 338

opposite pattern [46]. 339

340

In both tropical and temperate regions, shifts in the benthic communities surrounding 341

the vents were consistent with proposed direct and indirect effects of ocean 342

acidification on mat-forming algae. Mat-forming algae at temperate vents may limit 343

the percent coverage of calcified taxa, which at the end of a year of development were 344

26% in the ambient pH zones and 17% in the low pH zones [45]. Hence, mat-forming 345

algae appear to inhibit other taxa [45]. Among the tropical vents, at a pH below 7.7 346

(i.e. conditions beyond those expected for the end of the 21st Century), no coral reef 347

development was found, and the benthos was dominated by seagrasses, ephemeral 348

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macroalgae and volcanic sand, and a few individual colonies of robust coral species 349

(massive Porites and Favites pentagona) [46]. 350

351

(d) Herbivores 352

As anticipated, the densities of calcareous benthic grazers (e.g. sea urchins and 353

gastropods) are substantially sparser in extremely low pH conditions in both 354

temperate [45, 67] and tropical regions [68]. However, in the projected near future 355

conditions presented in these analyses (Fig. 2), sea urchin densities are similar to 356

control sites at tropical vents (Fabricius, unpublished data) and temperate vents 357

(Kroeker et al. in revision). In addition, the abundances of small mobile grazers 358

(primarily gastropods) do not differ among the low pH and control sites at the 359

temperate vents [69]. Differences in herbivorous fish populations are unknown at both 360

these vents, however herbivorous fish can easily access all areas of the temperate and 361

tropical vents and did not appear to avoid areas of low pH (Kroeker pers. obs., 362

Fabricius, pers. obs.). The observation that calcareous benthic grazers are sparser at 363

extremely low pH levels suggests that there is merit in understanding the conditions in 364

which herbivory may be altered by enriched CO2. 365

366

6. DISCUSSION 367

(a) Ocean acidification and resource availability 368

Human-driven environmental changes are producing regional combinations of 369

environmental conditions that may push many ecological systems outside the 370

environmental envelope in which they evolved. The relative abundances of sessile 371

plants often reflect resource limitations, but many of these constraints are undergoing 372

large, rapid changes capable of causing phase-shifts [70]. These new environmental 373

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conditions appear to favor species with fast rates of colonization, growth and short 374

generation times that can competitively displace slower growing and longer living 375

space-holders when resource availability is increased [31, 36, 54]. 376

377

The effects of CO2 enrichment that we synthesized here were derived from 378

substantially different species, regions and experimental protocols (Electronic 379

Supplementary Material 1). The consistency of positive effects on productivity alone 380

suggests that previous reports of CO2 effects on expansive covers of algae on 381

temperate and tropical rocky coasts [e.g. 67, 68] and increasing dominance of mats 382

over corals [e.g. 28] may not represent an idiosyncratic set of case examples. 383

Naturally ephemeral mats may not only displace recovering kelp forests under 384

elevated nutrients [31, 59], but this loss may be strengthened by future CO2 385

concentrations [i.e. nutrient × CO2 synergy, 71]. Similarly, mats may have variable 386

effects on corals recovering from disturbance under current conditions [72], but CO2 387

may strengthen their negative effects on corals via increased growth rates of mats [28] 388

coupled with decreased growth rates of corals [73]. Together, these studies provide 389

insight into ecological drivers that to date have attracted comparatively little study, 390

but represent potentially profound drivers of the ecology of these diverse ecosystems. 391

392

(b) Indirect effects on herbivores 393

The role of herbivores in the trends presented here is a current gap in understanding. 394

The studies from the CO2 seeps report that herbivores are present in end-of Century 395

pH conditions, and at least some species are in similar abundance between the low pH 396

and control sites. This suggests the increased dominance of mats in the projected 397

near-future conditions is not predominantly due to the absence of calcareous grazers. 398

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However, decades of research have highlighted the importance of grazers in 399

mediating competitive interactions between benthic space holders [74, 75] and 400

research is needed to assess whether an increased supply of resources (e.g. CO2) can 401

change these ecosystems from predominant consumer control to predominant 402

resource control [e.g. nutrients, 76]. 403

404

There are several ways in which herbivores could contribute to or counter the trends 405

reported here that deserve further attention. For example, changes in abundance or 406

behavior (resulting in reduced per capita herbivory) could contribute to the dominance 407

of mat-forming algae. However, laboratory experiments reveal that gastropods reared 408

on turfs grown in various CO2 concentrations removed more algae per herbivore 409

under elevated CO2; an effect that was driven by the indirect effect of CO2 via 410

changes to C:N ratios in the algae rather than the direct effect on the herbivore [77]. 411

Thus, increased herbivory could compensate for increased growth by mats, although 412

this was not apparent at the CO2 seeps. Furthermore, some diatoms produce tissue 413

with lower nutrient concentrations in response to elevated CO2 [78]. If acidification 414

were to similarly affect the nutrient status of benthic algae, individual herbivores 415

would need to increase per capita rates of consumption to acquire sufficient protein 416

and other nutrients for growth and development. Conversely, reduced nutrient content 417

of algae could cause herbivores to grow more slowly and suffer higher mortality in 418

the process, or even selectively graze certain species of algae. Elevated CO2 can also 419

affect the production of chemical herbivore deterrents in marine plants [79], which 420

could further influence the interaction between herbivores and algae. Last, the effects 421

of ocean acidification on herbivores are likely to be influenced by concurrent changes 422

in temperature [80] that can affect population size and per capita rates of 423

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consumption. While there is multitude of potential interactions and indirect effects of 424

acidification on herbivores that require further attention, the results from CO2 seeps 425

suggest that an increased dominance of mat-forming algae is a likely emergent effect. 426

427

(b) Multiple stressors: ocean acidification as a non-additive stressor 428

Most ecological systems are exposed to multiple stressors. The projected rates of CO2 429

absorption in the future [81], suggest that ocean acidification represents a relatively 430

slow driver of future ecological change. However, the gradual trend in ocean 431

acidification will be overlaid on additional stressors to marine ecosystems (e.g. 432

temperature, fishing and nutrients) as well as short-term perturbations that occur at 433

local to regional scales (e.g. storms, coral bleaching, coral disease and mass urchin 434

mortalities). Many stressors combine in synergistic ways. Recent reviews reveal non-435

additive effects in about three-quarters of factorial experiments involving two stressor 436

combinations [82], which increases to three-quarters when two or more stressors are 437

considered [4]. Indeed, it is probably a simple function of sample-size (n) that the 438

frequency of synergistic and antagonistic effects will increase with an increase in 439

number of stressors. Hence, the potential for acidification-related phase-shifts in 440

response to gradual acidification is likely to increase with additional stressors [83]. 441

442

Not surprisingly, the potential for synergistic effects between multiple stressors 443

increases the probability of phase shifts [e.g. 54]. When combined with elevated 444

nutrients, elevated CO2 can release mats from co-limitation with nitrogen loading [29] 445

to accelerate expansion at a rate that is greater than the sum of the effects of each of 446

the two stressors acting separately [e.g. 71]. In addition, projected warming is likely 447

to enhance mat productivity because mats are not only better suited to the increasing 448

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availability of CO2 [29], but these effects are enhanced under warmer temperatures 449

[16]. Such synergistic effects of CO2 with other stressors may increase the 450

probability of phase shifts. 451

452

A positive aspect of potential synergistic effects of ocean acidification with local 453

stressors is that local management may ameliorate the effects of CO2 enrichment by 454

reducing local stressors. For example, although CO2 and eutrophication can yield 455

synergistic responses [71], a reduction of the appropriate local stressor (e.g. nutrients) 456

ameliorates the synergistic effects on mat growth [24]. These results suggest that the 457

management of local stressors (e.g. water pollution and overfishing) may have a 458

greater contribution in determining the ecosystem effects of ocean acidification than 459

current thinking allows. Such findings empower local managers because they show 460

that reducing local stressors (e.g. nutrient pollution and overfishing) can reduce the 461

effects of global stressors not under their governance (e.g. ocean acidification and 462

temperature). 463

464

(c) In conclusion 465

Ocean acidification is often considered in terms of its direct negative effects on the 466

growth and calcification of organisms with calcareous shells or skeletons. We argue 467

that this focus overlooks the important role of ocean acidification as a resource, which 468

can enhance the productivity of algae known to influence the status of kelp forests 469

and coral reefs (i.e. mat-forming algae or mats). We have highlighted how ocean 470

acidification can indirectly tip the competitive balance towards dominance by mats 471

through mechanisms that generate new space (e.g. disturbance or storm events) that 472

enable colonization and persistence of mats rather than the original kelp or coral state. 473

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474

Ocean acidification, therefore, has the capacity to act as a resource that shifts the 475

status of subordinates into dominant competitors. Consequently, human activities that 476

alter the availability of resources have important implications for the relative 477

competitive abilities of major ecosystem components. We suggest that additional 478

stressors will influence the effect of ocean acidification on producers, and that many 479

cumulative impacts may be synergistic. Contrary to conventional wisdom, we argue 480

that if these synergies involve local stressors, environmentally mediated ecosystem 481

shifts may be greatly ameliorated by managing local stressors. Nevertheless, there are 482

few assessments of whether management of local processes can weaken the feedbacks 483

that reinforce altered state and enable the reversibility of phase shifts. Importantly, we 484

suggest that in the face of changing climate (e.g. ocean acidification and temperature), 485

effective management of local stressors (e.g. water pollution and overfishing) may 486

have a greater contribution in determining ecosystem states than currently anticipated. 487

Thus, we highlight how ocean acidification has the potential to influence competitive 488

abilities via changes in resource availability, with implications for the stability and 489

persistence of the system as a whole. 490

491

ACKNOWLEDGMENTS 492

The authors acknowledge the funding agencies and collaborators; Australian Research 493

Council (SDC, BDR, DIK), the Monterey Bay Aquarium Research Institute (DIK, 494

BDR, SDC), the Australian Institute of Marine Science (KEF), the Bodega Ocean 495

Acidification Research Group (KJK), the Pacific Blue Foundation (DIK), and the 496

National Science Foundation (DIK). 497

498

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responses within a benthic marine community to ocean acidification. Proc Natl 720

Acad Sci U S A 108(35), 14515-14520. (doi:10.1073/pnas.1107789108). 721

70. Vitousek P., Mooney H., Lubchenco J., Melillo J. 1997 Human domination of 722

earth's ecosystems. Science 277, 494-499. 723

71. Russell B.D., Thompson J.I., Falkenberg L.J., Connell S.D. 2009 Synergistic 724

effects of climate change and local stressors: CO2 and nutrient driven change 725

in subtidal rocky habitats. Global Change Biology 15, 2153-2162. 726

72. Bender D., Diaz-Pulido G., Dove S. 2012 Effects of macroalgae on corals 727

recovering from disturbance. J Exp Mar Biol Ecol 429, 15-19. 728

(doi:10.1016/j.jembe.2012.06.014). 729

73. Schneider K., Erez J. 2006 The effect of carbonate chemistry on calcification 730

and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol 731

Oceanogr 51(3), 1284-1293. 732

74. Lubchenco J. 1978 Plant species diversity in a marine intertidal community: 733

Importance of herbivore food preference and algal competitive abilities. . Am 734

Nat 112, 23-39. 735

75. Carpenter R.C. 1986 PARTITIONING HERBIVORY AND ITS EFFECTS ON 736

CORAL-REEF ALGAL COMMUNITIES. Ecol Monogr 56(4), 345-363. 737

(doi:10.2307/1942551). 738

76. Worm B., Lotze H.K. 2006 Effects of eutrophication, grazing, and algal blooms 739

on rocky shores. Limnol Oceanogr 51, 569-579. 740

77. Falkenberg L.J., Russell B.D., Connell S.D. in review CO2 enrichment alters rates 741

of marine herbivory: disentangling direct and indirect effects Mar Ecol-Prog 742

Ser. 743

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78. Rossoll D., Bermudez R., Hauss H., Schulz K.G., Riebesell U., Sommer U., Winder 744

M. 2012 Ocean Acidification-Induced Food Quality Deterioration Constrains 745

Trophic Transfer. Plos One 7(4). (doi:e34737 746

10.1371/journal.pone.0034737). 747

79. Arnold T., Mealey C., Leahey H., Miller A.W., Hall-Spencer J.M., Milazzo M., 748

Maers K. 2012 Ocean acidification and the loss of phenolic substances in 749

marine plants. Plos One 7(4). (doi:e35107 750

10.1371/journal.pone.0035107). 751

80. O'Connor M.I. 2009 Warming strengthens an herbivore-plant interaction. 752

Ecology 90(2), 388-398. 753

81. Feely R.A., Sabine C.L., Lee K., Berelson W., Kleypas J., Fabry V.J., Millero F.J. 754

2004 Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 755

305(5682), 362-366. 756

82. Darling E.S., Côté I.M. 2008 Quantifying the evidence for ecological synergies. 757

Ecology Letters 11(12), 1278-1286. (doi:10.1111/j.1461-0248.2008.01243.x). 758

83. Hughes T.P., Linares C., Dakos V., van de Leemput I.A., van Nes E.H. in press 759

Living dangerously on borrowed time during slow, unrecognized regime shifts. 760

Trends Ecol Evol 1608. 761

84. Cohen J. 1988 Statistical power analysis for the behavioural sciences. 2nd ed. ed. 762

Hillsdale, NJ., Lawrence Erlbaum Associates. 763

764

765

766

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FIGURE LEGENDS 767

Figure 1. Diagram showing the indirect effect of enriched CO2 on habitat forming 768

species (i.e. kelps and corals) via mat-forming algae. CO2 facilitates the growth of 769

mat-forming algae, which in turn inhibit the recruitment of kelps and corals. The 770

indirect effects of CO2 may rival the direct effects of CO2, particularly where CO2 771

combines with other stressors in synergistic ways. 772

773

Figure 2. Elevated net productivity and cover of mat-forming algae under enriched 774

CO2 conditions. In the natural environment, the percentage cover is greater at CO2 775

vents in temperate (a. Ischia, Mediterranean) and tropical seas (b. Papua New 776

Guinea). Growth rates are greater under CO2 enriched treatments within temperate 777

(c) and tropical (d) field manipulations and temperate (e) and tropical (f) laboratory 778

manipulations. ‘Control’ represents current CO2 conditions (∼ 300-410 pCO2) and 779

‘Future’ end of this century conditions (∼ 550-830 pCO2). 780

781

782

783

784

785

786

787

788

789

790

791

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Table 1. The TA and pCO2 were increased, and pH decreased, in treatments 792

where CO2 was elevated. The effect on algae was similar among the methods (i.e. 793

vents, vs field vs laboratory) and climes (i.e. temperate vs tropical). 794

795

Temperate Tropical

TA pH pCO2 ES TA pH pCO2 ES

Vents 0.70 0.82

Elevated 2560 7.76 805 2302 7.83 748

Ambient 2563 8.01 305 2297 8.00 401

Field mesocosm 0.88 0.81

Elevated 2357 7.91 647 2320 7.87 779

Ambient 2276 8.15 307 2320 8.10 416

Laboratory 0.82 0.73

Elevated 2585 7.96 557 2260 7.84 828

Ambient 2263 8.14 300 2258 8.16 342

Measured: total alkalinity (TA) and pH. 796

Calculated: concentration (ppm) of pCO2 797

Calculated: effect-size (ES) of the treatments on algae. The magnitude of the 798

effect-size (r) was calculated using Cohen's d for two independent groups (i.e. 799

the difference between means divided by standard deviation [Cohen's d 84]. 800

801

802

803

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Supplementary 1. Further details of the location (locality), duration (days), 804

temperature (oC) and references for a more detailed description (description) of the 805

observations of mats among vents (vents) and field mesocosms (field) and laboratory 806

experiments (laboratory). 807

Locality Days Substratum oC Description

Vents Ischia,

Mediterranean

(temperate)

430

settlement

plates

13-

25

Kroeker et al. [45]

Papua New

Guinea

(tropical)

-

natural reef 29 unpublished data from

Fabricius et al. [46]

Field

Adelaide

Australia

(temperate)

90

settlement

plates

15-

22

Falkenberg et al. [24]

Heron Island

Great Barrier

Reef

(tropical)

10

settlement

plates

23

Kline et al. [66]

Laboratory Adelaide

Australia

(temperate)

76

settlement

plates

17

Connell and Russell

[16]

Heron Island

Great Barrier

Reef

(tropical)

15

settlement

plates

25

unpublished data

808

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mat-forming algae kelps/corals CO2

× synergies

Facilitate Inhibit

Inhibit

Figure 1

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0

2

4

6

0

1

2

3

C o n t r o l F u t u r e 0

1 0

2 0

3 0

C o n t r o l F u t u r e 0

1 0

2 0

3 0

0

2 0

4 0

6 0

8 0

0

2 0

4 0

6 0

8 0

Levels of CO2

Gro

wth

(mg

per d

ay)

Perc

enta

ge c

over

Temperate Tropical

(c) Field mesocosms

(a) CO2 vents

(e) Laboratory

(b)

(d)

(f)

Figure 2 Page 36 of 36



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