Escaping herbivory: ocean warming as a refuge for primary producers where consumer metabolism and consumption cannot pursue Nicole L. Mertens, Bayden D. Russell & Sean D. Connell
Oecologia ISSN 0029-8549 Oecologia DOI 10.1007/s00442-015-3438-8
1 23
Your article is protected by copyright and all rights are held exclusively by SpringerVerlag Berlin Heidelberg. This e-offprint is for personal use only and shall not be selfarchived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”.
1 23
Author's personal copy Oecologia DOI 10.1007/s00442-015-3438-8
GLOBAL CHANGE ECOLOGY - ORIGINAL RESEARCH
Escaping herbivory: ocean warming as a refuge for primary producers where consumer metabolism and consumption cannot pursue Nicole L. Mertens1 · Bayden D. Russell1,2 · Sean D. Connell1
Received: 15 October 2014 / Accepted: 30 August 2015 © Springer-Verlag Berlin Heidelberg 2015
Abstract Ocean warming is anticipated to strengthen the persistence of turf-forming habitat, yet the concomitant elevation of grazer metabolic rates may accelerate per capita rates of consumption to counter turf predominance. Whilst this possibility of strong top-down control is supported by the metabolic theory of ecology (MTE), it assumes that consumer metabolism and consumption keep pace with increasing production. This assumption was tested by quantifying the metabolic rates of turfs and herbivorous gastropods under a series of elevated temperatures in which the ensuing production and consumption were observed. We discovered that as temperature increases towards nearfuture levels (year 2100), consumption rates of gastropods peak earlier than the rate of growth of producers. Hence, turfs have greater capacity to persist under near-future temperatures than the capacity for herbivores to counter their growth. These results suggest that whilst MTE predicts stronger top-down control, understanding whether consumer–producer responses are synchronous is key to assessing the future strength of top-down control. Keywords Climate change · Phase shift · Stability · Trophic cascade · Metabolic theory
Communicated by Deron E. Burkepile. * Sean D. Connell
[email protected] 1
Southern Seas Ecology Laboratories, School of Biological Sciences, University of Adelaide, Adelaide, SA 5005, Australia
2
Swire Institute of Marine Science and School of Biological Sciences, University of Hong Kong, Hong Kong SAR, China
Introduction Primary productivity and subsequent consumption are underpinned by metabolic demands and activity, which are in turn regulated by the physiochemical environment. Basic metabolic theory predicts that warming will increase metabolic activity until a threshold is exceeded (Angilletta et al. 2002). Organisms that are more metabolically active will also have greater energetic demands and should therefore need to increase their feeding or photosynthetic rates (Brown et al. 2004). Because heterotrophic respiration and autotrophic productivity are scaled differentially to temperature (Allen et al. 2005), predictions of the metabolic theory of ecology (MTE) suggest that producers will show a weaker temperature response than their consumers (LópezUrrutia et al. 2006; Yvon-Durocher et al. 2010). Based on this theory, future warming is likely to lead to an increase in top-down control of marine producers (O’Connor 2009; Carr and Bruno 2013). However, if metabolism and consumption do not scale equivalently with increasing temperature, grazing pressure may actually decrease through reduced grazer fitness (Lemoine and Burkepile 2012). Every organism has a thermal window in which biological processes can occur. This range encompasses upper and lower critical thermal limits, outside of which mortality occurs, as well as an optimum temperature for biological performance (Angilletta et al. 2002; Pörtner and Farrell 2008). Warming may therefore increase the performance of an organism by increasing its metabolic rate, yet this is only true until a threshold is reached. Animals operating near their upper thermal limits, such as high-intertidal species, are therefore generally considered to be most at risk from global warming, whilst subtidal animals with lower thermal limits may actually show a greater capacity to respond to
13
Author's personal copy Oecologia
increased temperatures if they are currently operating well below their thermal optima (Somero 2005, 2010). Furthermore, the width of an organism’s thermal range, optimal temperature and sensitivity to changes in temperature will vary between populations, species and trophic levels (Pörtner and Farrell 2008; Kordas et al. 2011). In temperate Australian waters, changes to abiotic conditions can cause phase shifts where kelp-dominated systems transition to algal mats or algal turfs. Where nitrogen or carbon resources are elevated, these normally ephemeral turfs can persist and prevent re-establishment of kelp forests by juvenile recruits (Gorman and Connell 2009; Connell and Russell 2010). Whilst warming has negative impacts on kelp ecophysiology and erodes their resilience (Wernberg et al. 2010, 2011), turfs have been shown to increase their productivity over similar temperature increases (i.e. 2–4 °C), occupying more of the substrate usually available for kelp recruitment (Connell and Russell 2010). However, these turfs form the diet of many marine grazers including turbinid gastropods, which are common to rocky reefs and consume many common algal groups (Worthington and Fairweather 1989; Wernberg et al. 2008). Ectotherms such as gastropods are greatly influenced by external temperature changes (Huey and Kingsolver 1989). If this system responds to future warming according to predictions of MTE, an increase in primary productivity and growth may be mitigated by increased consumer respiration and subsequent grazing (O’Connor et al. 2011). We assess how future warming will impact the strength of this producer–grazer interaction. The purpose of this study was to test whether consumer metabolism and consumption keep pace with increasing primary production under warming conditions. We quantified the metabolic rates of algal turfs and an herbivorous gastropod under a series of elevated temperatures in which the ensuing production and consumption were observed. If the optimal temperatures for grazer activity differ from those for turf productivity, we propose this difference could increase the probability of shifts in the strength of grazer control of algal growth under future warming.
Materials and methods Experimental design and maintenance The effects of temperature on the productivity of turfs versus the consumption of gastropod grazers were tested in a microcosm experiment. Five microcosms were used per treatment, each containing one grazing gastropod and three 5 × 20 cm panels on which algal turfs grew, comprised of densely packed filaments of algae (
