Marine Pollution Bulletin xxx (xxxx) xxx–xxx Contents lists available at ScienceDirect Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul Review: Host-pathogen dynamics of seagrass diseases under future global change ⁎ Brooke K. Sullivana,b, , Stacey M. Trevathan-Tackettc, Sigrid Neuhauserd, Laura L. Goverse,f a School of Biosciences, The University of Melbourne, Parkville Campus, Parkville, Victoria 3010, Australia b Victorian Marine Science Consortium, 2A Bellarine Highway, Queenscliff, Victoria 3225, Australia c Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Burwood, Victoria, Australia d Institute of Microbiology, University of Innsbruck, Technikerstr. 2, 6020 Innsbruck, Austria e Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Post Office Box 11103, 9700 CC Groningen, The Netherlands f Department of Aquatic Ecology and Environmental Biology, Institute for Water and Wetland Research, Radboud University, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands ARTICLE INFO ABSTRACT Keywords: Human-induced global change is expected to amplify the disease risk for marine biota. However, the role of Global change disease in the rapid global decline of seagrass is largely unknown. Global change may enhance seagrass sus- Halophytophthora ceptibility to disease through enhanced physiological stress, while simultaneously promoting pathogen devel- Labyrinthula opment. This review outlines the characteristics of disease-forming organisms and potential impacts of global Marine infectious disease change on three groups of known seagrass pathogens: labyrinthulids, oomycetes and Phytomyxea. We propose Phytophthora that hypersalinity, climate warming and eutrophication pose the greatest risk for increasing frequency of disease Phytomyxea outbreaks in seagrasses by increasing seagrass stress and lowering seagrass resilience. In some instances, global change may also promote pathogen development. However, there is currently a paucity of information on these seagrass pathosystems. We emphasise the need to expand current research to better understand the seagrass- pathogen relationships, serving to inform predicative modelling and management of seagrass disease under future global change scenarios. 1. Introduction recognised for their ecological function and the provision of human services, including reduction in human and wildlife pathogens (Lamb Human-induced global change facilitates disease outbreaks on a et al., 2017) coastal protection (Christianen et al., 2013), fisheries ha- global scale (Harvell et al., 2002). Mass-mortalities due to disease in bitat (Jackson et al., 2001) and carbon sequestration (Fourqurean et al., keystone species marine species have been reported in corals (Hoegh- 2012). Seagrasses also provide positive feedback mechanisms for Guldberg et al., 2007), marine mammals (Cosby et al., 1988), oysters themselves that drive continued provision of suitable habitat for their (Van Banning, 1991), sea-stars (Hewson et al., 2014) and seagrasses own survival (De Boer, 2007; Maxwell et al., 2016). Despite increasing (Sullivan et al., 2013). Through the negative impacts on these keystone attention to seagrasses as a keystone species, researchers estimate species, the effects of disease may rapidly cascade through ecosystems, nearly 30% of the global seagrass area world-wide was lost between with potentially catastrophic consequences through local species ex- 1879 and 2006 (Waycott et al., 2009). tinction, community regime shifts and disruptions in economically- Under the threat of ongoing global change, ecologists look to un- linked ecosystem services, such as fisheries production (Groner et al., derstand how marine ecosystems will function, and how community 2015; Sullivan et al., 2013). Despite emerging threats to several eco- and population dynamics may be altered in the near and distant future. logically important species, epidemiological studies in marine systems The majority of publications available on the effects of global change in are sparse compared to terrestrial systems (Harvell et al., 1999). coastal ecosystems have focused on the role of abiotic environmental Seagrasses are marine flowering plants that form large swaths of conditions, namely temperature, on the health of marine systems, and grass-like intertidal and subtidal meadows in coastal areas. Seagrass most often at the level of an individual species or population (Harley ecosystems provide vital coastal habitats that are increasingly et al., 2006). Still, research on the role of biologically-mediated ⁎ Corresponding author at: School of Biosciences, The University of Melbourne, Parkville Campus, Parkville, Victoria 3010, Australia. E-mail addresses: [email protected] (B.K. Sullivan), [email protected] (S.M. Trevathan-Tackett), [email protected] (S. Neuhauser), [email protected] (L.L. Govers). http://dx.doi.org/10.1016/j.marpolbul.2017.09.030 Received 1 April 2017; Received in revised form 11 September 2017; Accepted 13 September 2017 0025-326X/ © 2017 Elsevier Ltd. All rights reserved. Please cite this article as: Sullivan, B.K., Marine Pollution Bulletin (2017), http://dx.doi.org/10.1016/j.marpolbul.2017.09.030 B.K. Sullivan et al. Marine Pollution Bulletin xxx (xxxx) xxx–xxx environmental conditions (Alsterberg et al., 2013; Eklöf et al., 2012; In fact, while the importance of the microbiome in seagrass is gaining Sunday et al., 2017) suggests that organism-to-organism interactions momentum (Fahimipour et al., 2017), the role of pathogenic disease is are important in understanding both direct and indirect effects of global often left out of seagrass research entirely, and is largely missing or change on the functional capacity of coastal and marine ecosystems. overlooked in reviews and analyses of global change impacts in seagrass ecosystems (Bjork et al., 2008; Brown et al., 2013; Short et al., 2016). 1.1. Known global change impacts to seagrass Still, there is recognition of the vulnerability of seagrass to global change scenarios (Short et al., 2016), which is alarming, given multiple Abiotic drivers potentially affecting seagrass resilience under future evidence of accelerating risk of emerging infectious diseases in terres- scenarios include increasing ocean temperatures, sea level rise, in- trial and marine systems, largely through range expansion and human creased frequency of storms, ocean acidification (increased CO2 and introduction (Anderson et al., 2004; Hoegh-Guldberg and Bruno, 2010). decreased pH) and changes to salinity (Duarte, 2002; Harley et al., We theorise that since human-induced changes to global systems 2006; Koch et al., 2013; Short et al., 2016). Increasingly, studies are pose major threats to seagrasses in the future (Orth et al., 2006; Short emerging to quantify the effects of global change on seagrasses. These et al., 2016), they may decrease seagrass resilience and fitness (De Boer, include theoretical investigations of seagrass physiology, communities 2007; Ehlers et al., 2008; Fraser et al., 2014; Ruesink, 2016) and thus, and populations (Duarte, 2002; Edwards, 1995; Harley et al., 2006; increase the risk of susceptibility to disease (Harvell et al., 2002). Occhipinti-Ambrogi and Savini, 2003; Orth et al., 2006; Short and Multiple and repeated disturbances, such as those that may occur as Neckles, 1999) and modelling and experimentation (Jordà et al., 2012; global change progresses, are known to further reduce seagrass resi- Koch et al., 2013; Palacios and Zimmerman, 2007; Rasheed and lience (Eklöf et al., 2010; Fraser et al., 2014) and may create hotspots of Unsworth, 2011). seagrass disease. In addition to enhanced susceptibility of the host, Firstly, elevated seawater temperatures will affect plant physiology, global change may also promote infection and transmission of diseases reproduction, growth and geographic distribution (Short and Neckles, by promoting pathogen development, survival and reproduction (Burge 1999). For some seagrasses, warmer waters may be beneficial, resulting et al., 2014; Harvell et al., 1999). Combined effects of global change on in increased growth rates (Short and Coles, 2001) and reproduction host, pathogen and host-pathogen relationships in seagrass diseases are (Diaz-Almela et al., 2007). However, plants growing at the edges of understudied. Still, available research points to significant effects for their geographical range are found to experience increased mortality seagrasses from temperature, salinity, eutrophication and biological due to drought stress (de Fouw et al., 2016) and heat waves (Collier and interactions, such as disease. This research reveals the urgency for Waycott, 2014; Fraser et al., 2014). continued and inclusive investigations into the potential roles of disease Secondly, increasing atmospheric CO2 levels are increasing the in seagrass ecosystems, especially those under direct stress from global amount of dissolved CO2 in coastal waters, resulting in a lower pH (Orr change phenomena. et al., 2005). Although the effects of ocean acidification are unfavour- able to calcifying marine organisms, they are known to enhance resi- 2. History of seagrass disease research lience of seagrasses (Alsterberg et al., 2013). Seagrasses themselves are expected to benefit from high CO2 levels that result in increased plant Disease events in seagrass ecosystems have been observed for nearly production (Garrard and Beaumont, 2014;