Vol. 567: 79–93, 2017 MARINE ECOLOGY PROGRESS SERIES Published March 13 https://doi.org/10.3354/meps12029 Mar Ecol Prog Ser Predicting seagrass recovery times and their implications following an extreme climate event Robert J. Nowicki1,*, Jordan A. Thomson2, Derek A. Burkholder3, James W. Fourqurean1, Michael R. Heithaus1 1Department of Biological Sciences and Marine Education and Research Initiative, Florida International University, Miami, FL 33199, USA 2School of Life and Environmental Sciences, Deakin University, Warrnambool Campus, Warrnambool, VIC 3280, Australia 3Nova Southeastern University, Guy Harvey Research Institute, Ft Lauderdale, FL 33314, USA ABSTRACT: Extreme temperature events are predicted to become more frequent and intense as climate change continues, with important implications for ecosystems. Accordingly, there has been growing interest in what drives resilience to climatic disturbances. When a disturbance over- whelms the resistance of an ecosystem, it becomes vulnerable during recovery, with implications for ecosystem function and persistence. Understanding what influences ecosystem recovery is particularly important in seagrass ecosystems because of their functional roles, vulnerability, and divergent recovery strategies. Seagrass cover was monitored for 3 yr following a large, heatwave- associated mortality event in Shark Bay, Australia. Although the ecosystem’s historically dominant foundational seagrass, Amphibolis antarctica, is capable of rapid disturbance recovery, this did not occur, likely because of the failure of mechanisms which have driven rapid recovery in other systems (persistence of rhizome beds, sexual reproduction among neighboring beds). Instead, a tropical early successional seagrass, Halodule uninervis, became more common, increasing diver- sity. These changes in the structure of the Shark Bay seagrass ecosystem, and reduction of bio- mass and structural complexity, will have important implications for ecosystem services and com- munity dynamics and indicates that this ecosystem is highly vulnerable to future disturbances. More generally, our work suggests that seagrass ecosystems typified by a mix of early and late successional species may be particularly likely to exhibit a mismatch between recovery of cover per se and recovery of function following disturbance. As such, extreme climatic events have the potential to abruptly alter seagrass community dynamics and ecosystem services. KEY WORDS: Resilience · Disturbance recovery · Climate extremes · Climate change · Seagrass · Disturbance Resale or republication not permitted without written consent of the publisher INTRODUCTION of heat waves, heavy precipitation events and droughts, strength of tropical ocean currents, and Although research into the ecological effects of cli- even the frequency of extremes in the El Niño− mate change has largely focused on how organisms Southern Oscillation cycle (Wu et al. 2012, Cai et al. and ecosystems will respond to changes in average 2014, 2015, IPCC 2014). Such events can induce spe- environmental conditions, there is increasing recog- cies range shifts, species die-offs, or changes in com- nition of the ability of extreme climatic events — such munity composition, phenology, or primary produc- as heat waves and droughts — to rapidly alter ecosys- tivity (e.g. Honnay et al. 2002, Ciais et al. 2005, Inouye tems. Climate change is predicted to alter aspects of 2008, van Mantgem et al. 2009, Augs purger 2013). extreme events, including the frequency and duration This has implications for ecosystem functioning and in *Corresponding author: [email protected] © Inter-Research 2017 · www.int-res.com 80 Mar Ecol Prog Ser 567: 79–93, 2017 some cases can trigger regime shifts to persistent, fun- how ecosystems will respond to and recover from damentally different ecosystem states (e.g. Bennett et such events (Jentsch et al. 2007, Thomson et al. 2015). al. 2015). However, there is considerable uncertainty Return time of damaged seagrass beds can range as to the conditions under which ecological distur- from months to centuries (e.g. Walker & McComb bances trigger such shifts. In order to predict the oc- 1992, Plus et al. 2003, Orth et al. 2006, Short et al. currence of such shifts, it is first necessary to under- 2014). Seagrass life history strategy, in part, heavily stand what influences resilience to disturbances. influences return time. Seagrass species possess a Resilience is defined as the magnitude of distur- wide variety of life history traits and inhabit a contin- bance an ecosystem can withstand without shifting uum of successional capabilities, but can often be into an alternate state (sensu Holling 1973). For clar- categorized as late or early successional species ity, we define disturbances as ‘discrete, extreme (sensu Bazzaz 1979). Late successional seagrasses, events that substantially alter properties of an eco- such as those in the genera Amphibolis, Posidonia, system,’ while we define stressors as ‘continuous or Thalassia, and Zostera, tend to have relatively large near continuous forces that can change ecosystem and perennial canopies, often with large stores of properties or prevent recovery of those properties.’ carbohydrates in their buried rhizome tissue. These Resilience can be broken down into 2 mechanisms: energy stores can confer increased resistance to dis- resistance to disturbance and recovery from distur- turbances by providing the capability to rapidly refo- bance (i.e. return time) (Unsworth et al. 2015). Resist- liate and regenerate shoots from surviving rhizomes ance (sensu Carpenter et al. 2001) is the amount of if an extreme event overcomes their initial resistance external forcing required to change an ecosystem; (e.g. Peterson et al. 2002, Fraser et al. 2014). How- ecosystems with higher resistance can withstand ever, if this initial recovery strategy fails (because of, stronger forcing with no apparent change. When a for example, insufficient rhizome biomass or rhizome disturbance occurs (i.e. resistance has been over- death triggered by the disturbance), rapid (<10 yr) come and the ecosystem has changed), return time, return of these seagrasses to pre die-off abundance defined as the time it takes for a system to recover seems to be heavily dependent on the presence of a from a disturbance (May 1973), becomes the critical seed bank (Preen et al. 1995, Plus et al. 2003, Camp- mechanism of resilience in a system. Ecosystems that bell & McKenzie 2004) or reproductive events from recover rapidly from one disturbance exhibit high nearby beds (e.g. Larkum et al. 2006, Orth et al. 2006, stability and are more quickly able to resist subse- Tanner 2015). This is because many larger, late suc- quent forcing (Plus et al. 2003). It is therefore critical cessional seagrasses are characterized by exces- to understand not only how ecosystems respond to sively slow rhizome elongation rates (Walker et al. extreme events (resistance), but how they recover 2006), limiting the ability of vegetative expansion to from them, particularly as climate disturbances be - lead recovery, particularly when seagrass loss is come more frequent and the risk of exposure to widespread. Importantly, many late successional sea- sequential disturbances increases (Smale & Wern- grasses lack a dormant seed bank, and some genera, berg 2013, IPCC 2014). like Amphibolis, are viviparous and lack seeds alto- Despite their importance as foundations of coastal gether (Larkum et al. 2006). This further highlights ecosystems, seagrass habitats are declining at alarm- how crucial regeneration from below-ground bio- ing rates, largely because of impacts from local stres- mass and recruitment from nearby living beds are as sors such as sedimentation and eutrophication (e.g. mechanisms of rapid return time and resilience of Short & Wyllie-Echeverria 1996, Waycott et al. 2009). late successional seagrasses. Yet, even remote seagrass ecosystems far removed Unlike late successional species, early successional from local human influence can be vulnerable to (sensu Bazzaz 1979) seagrasses have adapted to dis- large disturbance events such as marine heat waves turbance through reliance on rapid disturbance re- (e.g. Fraser et al. 2014, Thomson et al. 2015). Such covery and expansion as opposed to resistance to dis- large events, which often cannot be managed at local turbance itself (Unsworth et al. 2015). These species, scales, illustrate the danger climate change and al- such as those in the genera Halophila and Halodule, tered thermal regimes pose to marine ecosystems, generally have small energy stores in rhizome tissue, something already well appreciated by coral reef instead relying on fast rhizome elongation rates and ecologists (e.g. Glynn 1993, Pandolfi 2015). While the dormant seed banks to rapidly recruit and expand af- potential for extreme climate events to generate ter disturbances (Walker et al. 2006). Early succes- widespread ecosystem shifts is becoming more rec- sional species also form relatively sparse and short ognized, many gaps still remain in understanding beds, generally with much lower structural complex- Nowicki et al.: Seagrass recovery after an extreme climate event 81 ity and standing biomass than those composed of late MATERIALS AND METHODS successional seagrasses. The plant traits associated with early and late successional species not only in- Study system fluence the recovery trajectories of mixed seagrass beds, but the functions associated with these beds as This study was performed