The relationship between macroalgae taxa and human disturbance on central Pacific coral reefs
Introduction
The health of coral reef ecosystems is declining worldwide (Aswani et al., 2015; Fenner, 2012; Hoegh-Guldberg et al., 2018; Hughes et al., 2019; Williams et al., 2015). Threats to coral reefs include both global pressures (such as climate change and ocean acidification) and local pressures (such as overfishing, sedimentation, and eutrophication). In addition to threatening the livelihoods and source of food for millions of people (Cinner, 2014), many of these threats can kill coral and reduce habitat complexity, influencing the ability of reefs to protect shorelines (Alvarez-Filip et al., 2009; Ferrario et al., 2014). Additionally, the potentially additive properties of these impacts may make corals and coral reef ecosystems less resilient to natural disturbances like storms (Scheffer et al., 2015, but see Côté and Darling, 2010).
Global sea temperatures have been rising for the past century and are projected to continue to rise (IPCC, 2014). This is leading to more frequent and severe heat waves and heat stress (Easterling et al., 2000; Donner et al., 2005; Maynard et al., 2015a) which can cause coral bleaching, coral mortality, and a reduced resilience to other stressors (Carpenter et al., 2008; Hughes et al., 2007; Magris et al., 2015; Toth et al., 2015). As a result, ongoing research is aiming to identify management actions that could confer coral reef resilience to climate change (e.g.; Bruno et al., 2019; Guest et al., 2018; Maynard et al., 2015b; McClanahan et al., 2012; Van Oppen and Gates, 2006). Applying these actions, however, depends on robust estimators of reef status. There has been disagreement in the literature about the relative role of local human activities in coral reef degradation with some articles reporting that local impacts are important (e.g. Fabricius et al., 2005; Scheffer et al., 2015; Williams et al., 2015; Crane et al., 2017), and other articles finding that local impacts are negligible in comparison to the impacts of climate change (e.g. Aronson and Precht, 2006; Carpenter et al., 2008; Bruno and Valdivia, 2016).
The debate about the relative role of local and global threats may in part stem from disagreements over the metrics of reef health, as well as the very definition of a healthy reef. Total macroalgae cover is commonly used to indicate that reefs are ‘unhealthy’ or have a different benthic composition than what was found prior to disturbance (e.g. McCook et al., 1997; Mumby et al., 2005; Hughes et al., 2007; Bruno and Valdivia, 2016). However, the broad category of “macroalgae cover” used in many field studies includes a variety of alga with different sensitivities to disturbance and life history strategies (Diaz-Pulido et al., 2010). The use of this coarse category could lead to the mischaracterization of reefs as unhealthy versus healthy. It neglects the differences within algae communities, overlooks other key reef organisms such as cyanobacteria and turf algae which are common on degraded reefs, and disregards the important role some algal assemblages may play in reef ecosystem function (e.g. Perry et al., 2016). Some reefs with high macroalgae cover are not necessarily degraded; in fact, some reefs far from human disturbance may have high percentages of macroalgae cover (Vroom et al., 2006; Vroom and Braun, 2010; Williams et al., 2015).
The difficulties in defining ‘healthy’ reefs are also influenced by the debate about what reefs may have looked like before the Industrial Revolution. Some studies argue that some reefs may have naturally high macroalgae cover (Howe, 1912; Setchell, 1928; Vroom, 2011; Finnegan et al., 2015), while others argue that macroalgae has increased at the expense of live coral even on the most remote reefs due to recent climate change (Aronson and Precht, 2006; Carpenter et al., 2008; Bruno and Valdivia, 2016). However, while phase shifts from hard coral- to macroalgae-dominated reefs after disturbances are well documented in the Caribbean (Hughes, 1994; Hughes et al., 2007; Suchley et al., 2016), these may be uncommon in the Indo-Pacific (Bruno et al., 2009; Smith et al., 2016). It is possible that disturbances may instead cause coral reefs to shift towards other dominant taxa, such as sponges (Bell et al., 2013; Powell et al., 2014), corallimorphs (Work et al., 2008), or corals with ‘weedy’ life history strategies (Darling et al., 2012; Davenport and Haner, 2015; Crane et al., 2016).
The existence of remote Pacific atolls with negligible local impacts has allowed researchers to contrast coral and fish communities between pristine and more disturbed Pacific reefs (Houk and Musburger, 2013; Martin et al., 2017; Pecl et al., 2017; Sandin et al., 2008; Williams et al., 2013). The atolls of Majuro and Arno in the Republic of the Marshall Islands (RMI) provide a unique opportunity for targeted analysis of possible indicators of reef health and the relative threats posed by climate change and human disturbance. Only 19 km apart, the two atolls have comparable climatic and oceanographic experiences but a diversity of local human disturbance histories. In 2014, the most extensive thermal stress event in recorded history impacted the RMI. Abnormally high sea surface temperatures from July through December 2014 led to Bleaching Alert Level II warnings from NOAA Coral Reef Watch for September through November for the entire country, although heat stress was not as high in the southern atolls, including Majuro and Arno (Coral Reef Watch, 2017). There were some reports of possible shallow water bleaching-related coral mortality based on limited observations in Majuro and Arno (Fellenius, 2014), but the overall effect of the heat stress event on coral and algal communities remains unclear.
In this study, we examined how human disturbance impacts the composition of coral and algae communities across the more populated Majuro Atoll and more pristine Arno Atoll to explore the local impact of these disturbances and their effect on the recovery of reefs after the 2014 thermal stress event. We first investigated patterns in percent cover of key coral and alga taxa and their relationship with metrics of human influence across 25 sites in Majuro and Arno. We then examined how size structure of the coral communities varies across sites within each atoll and between the two atolls. Finally, we assessed the recovery from the recent (2014) thermal stress event by comparing percent cover surveys of key benthic life forms from 2007 in Arno and 2014 in Majuro to our data from 2016, at a subset of the original sites. The results provide insight into the limitations of macroalgae as an indicator of reef health and the impacts of human activities on coral communities in the central Pacific.
Section snippets
Background
The RMI is a nation of 29 atolls and five oceanic islands in the northwest tropical Pacific, just north of the Gilbert Islands of Kiribati and east of the Federated States of Micronesia. The Marshallese people depend heavily on surrounding coral reefs for food, as fishing is a major source of sustenance (Gillett, 2008; Martin et al., 2017), and for protection from storms and rising seas (Pinca et al., 2005).
The RMI have been inhabited for approximately 3000 years (Ratzel, 1896). Majuro Atoll,
Benthic cover
Macroalgae (including Halimeda spp.) cover ranged from 0% to 88% (Fig. 2a) across all sites. Halimeda spp. was the most commonly observed macroalgae, ranging from 0% to 77% of all benthic cover across all sites. Live coral cover ranged from 1% to 54% across all sites (Fig. 2a). In Arno, massive Porites were common, while in Majuro, Acropora was more prevalent (Fig. 2b). In general, sites in Arno had more macroalgae cover than sites in Majuro (Fig. 2c). Halimeda was common in both Majuro and
Discussion
The results indicate that differences in benthic composition and coral size-structure across Majuro and Arno may be related to a combination of local human disturbance and exposure to wind and waves. However, total macroalgae cover, a metric commonly used for characterized unhealthy or disturbed reefs, is not correlated with local human disturbance. Instead, local human disturbance is a predictor of the composition of the macroalgae community across sites and the presence of particular taxa of
Conclusion
This study identifies a relationship between local human disturbance, exposure, and the benthic community composition and coral size structure in reefs across Majuro and Arno Atolls. Degraded sites were dominated by turf algae, cyanobacteria, and sponges (particularly Terpios hoshinota) and in general had low cover of macroalgae. We also found variation in which genera of macroalgae were found at disturbed sites. Hypnea was statistically correlated with high disturbance, while Halimeda was more
Funding
This work was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant (S. Donner), a Winifred Violet Scott Estate grant to M. Beger, and the Australian Research Council for Environmental Decisions (CE110001014).
Acknowledgements
The authors would like to thank our local collaborators Florence Edwards, Emma Tibon, Kalena DeBrum, Benedict Yamamura and the staff at MIMRA, collaborators Diana Thompson and Emma Reed at Boston University, and Karl Fellenius of Hawaii Sea Grant and Martin Romain with the Marshall Islands Conservation Society for sharing photos collected at Majuro's sewage outfall. We would also like to thank Leonora King and Wesley Skeeter for assisting with ArcGIS and Eric Leinberger for his help with
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