Reefs under Siege—the Rise, Putative Drivers, and Consequences of Benthic Cyanobacterial Mats

Abstract

Benthic cyanobacteria have commonly been a small but integral component of coral reef ecosystems, fulfilling the critical function of introducing bioavailable nitrogen to an inherently oligotrophic environment. Though surveys may have previously neglected benthic cyanobacteria, or grouped them with more conspicuous benthic groups, emerging evidence strongly indicates that they are becoming increasingly prevalent on reefs worldwide. Some species can form mats comprised by a diverse microbial consortium which allows them to exist across a wide range of environmental conditions. This review evaluates the putative driving factors of increasing benthic cyanobacterial mats, including climate change, declining coastal water quality, iron input, and overexploitation of key consumer and ecosystem engineer species. Ongoing global environmental change can increase growth rates and toxin production of physiologically plastic benthic cyanobacterial mats, placing them at a considerable competitive advantage against reef-building corals. Once established, strong ecological feedbacks [e.g., inhibition of coral recruitment, release of dissolved organic carbon (DOC)] reinforce reef degradation. The review also highlights previously overlooked implications of mat proliferation, which can extend beyond reef health and affect human health and welfare. Though identifying (opportunistic) consumers of mats remains a priority, their perceived low palatability implies that herbivore management alone may be insufficient to control their proliferation and must be accompanied by local measures to improve water quality and watershed management.

Nitrogen fixation and diversity of benthic cyanobacterial mats on coral reefs in Curaçao

“…Charpy et al (2012) reported that on the islands of Mayotte, Tulear and La Reunion, coastal eutrophication favored bloom-forming cyanobacterial mats that were capable of fixing vast amounts of atmospheric nitrogen. Continued cyanobacterial but also algal proliferation will further degrade coral reefs (Ford et al 2018) and has been reported to increase the reef's sediment with organic matter (Barott and Rohwer 2012). This in turn will fuel benthic cyanobacterial mat proliferation (Brocke et al 2015;Ford et al 2018) and augment its nitrogen fixation potential (Hanson and Gundersen 1976;O'Neil and Capone 1989;King et al 1990).…”

“…Continued cyanobacterial but also algal proliferation will further degrade coral reefs (Ford et al 2018) and has been reported to increase the reef's sediment with organic matter (Barott and Rohwer 2012). This in turn will fuel benthic cyanobacterial mat proliferation (Brocke et al 2015;Ford et al 2018) and augment its nitrogen fixation potential (Hanson and Gundersen 1976;O'Neil and Capone 1989;King et al 1990). Ultimately, this could result in an undesirable positive feedback that will promote the proliferation of cyanobacterial mat abundance and consequently accelerate coral reef degradation.…”

“…Therefore, cyanobacteria have been suggested to play a key role in the nitrogen cycle of coral reefs (Wiebe et al 1975;Hallock 2005;Charpy et al 2012). Over the past two decades, benthic cyanobacterial mats (BCMs) have become a dominant component on many reefs worldwide (Thacker and Paul 2001;Albert et al 2005;Paul et al 2005;De Bakker et al 2017;Ford et al 2018). Future predictions suggest that BCMs will continue to increase in abundance, as they are favored by changes in environmental conditions associated with direct and indirect anthropogenic impacts (e.g., eutrophication and overfishing) and climate change (e.g., increase in water temperature) (Hallock 2005;Paerl and Paul 2012;Brocke et al 2015;Ford et al 2018).…”

“…Over the past two decades, benthic cyanobacterial mats (BCMs) have become a dominant component on many reefs worldwide (Thacker and Paul 2001;Albert et al 2005;Paul et al 2005;De Bakker et al 2017;Ford et al 2018). Future predictions suggest that BCMs will continue to increase in abundance, as they are favored by changes in environmental conditions associated with direct and indirect anthropogenic impacts (e.g., eutrophication and overfishing) and climate change (e.g., increase in water temperature) (Hallock 2005;Paerl and Paul 2012;Brocke et al 2015;Ford et al 2018). BCMs inhibit coral larvae settlement (Kuffner et al 2006), act as coral pathogens (Carlton and Richardson 1995) and can produce toxins that lead to selective browsing by herbivorous fish Paul 1998, 1999).…”

Scientists’ warning to humanity: microorganisms and climate change

“…Climate change perturbs interactions between species and forces species to adapt, migrate and be replaced by others or go extinct 28,88 . Ocean warming, acidification, eutrophication and overuse (for example, fishing, tourism) together cause the decline of coral reefs and may cause ecosystems shifts towards macroalgae [89][90][91][92][93] and benthic cyanobacterial mats 94,95 . The capacity for corals to adapt to climate change is strongly influenced by the responses of their associated microorganisms, including micro algal symbionts and bacteria [96][97][98] .…”