Spatial refuges and associational defenses promote harmful blooms of the alga Caulerpa sertularioides onto coral reefs

Abstract

Extreme population fluctuations, or outbreaks, are driven by interacting processes that are often more complex than isolated changes in consumer or resource control. Blooms of the macroalga Caulerpa sertularioides in the eastern tropical Pacific overgrew and killed reef-building corals, with blooms onto reefs corresponding to cool La Niña phases of inter-decadal fluctuations of the El Niño-Southern Oscillation. We quantified factors responsible for the maintenance of C. sertularioides patches in off-reef areas, namely an associational mutualism with an epiphytic cyanobacteria (Lyngbya majuscula), coupled with spatial refuges at the scales of individual thalli and habitat. Maintenance of near reef algal populations with a strong response to nutrient addition showed that these populations were primed to bloom onto reefs in response to enhanced nutrient delivery, such as those potentially associated with La Niña conditions. However, our experiments demonstrated that no single factor related to consumer or resource control was likely to stimulate bloom formation in isolation. Rather, we propose a novel model of reef bloom formation where off-reef blooms are sustained by processes reducing consumer control, and then bloom onto reefs through an interaction between increased allochthonous nutrient input and an uncoupling of consumer control by an association with epiphytic cyanobacteria.

Two species of Halimeda, a calcifying genus of tropical macroalgae, are robust to epiphytism by cyanobacteria

“…This contrasts with Aquat Ecol (2013) 47:433-440 437 recent studies that have shown natural abundances of epiphytic cyanobacteria can have strong negative effects on herbivory rates, and, by providing an associational refuge from herbivory, contributed to the persistence of blooms of Acanthophora spicifera (Fong et al 2006) and Caulerpa sertularioides (Smith et al 2010) on coral reefs of the Eastern Tropical Pacific. In these studies, neither A. spicifera, a highly palatable macroalga (Hay 1984;Boyer et al 2004), nor C. sertularioides, a chemically defended alga (Erickson et al 2006), could maintain populations on reefs without protection by epiphytic cyanobacteria.…”

“…We predicted that cyanobacterial epiphytes would reduce herbivory rates on Halimeda, though we expected this benefit to be modest compared to that afforded more palatable species (Fong et al 2006;Smith et al 2010). Further, we predicted that the presence of cyanobacterial epiphytes would decrease net growth rates of both species of Halimeda due to competition for light or nutrients.…”

“…Other studies have demonstrated ecosystem and population-level benefits of epiphytic associations, including increased primary productivity of ecosystems (Jones 1980), enhanced supply food for grazers (Brawley and Adey 1981;Yamamuro 1999), reduced desiccation, increased protection from UV radiation (Orth and Van Montfrans 1984), and provision of an associational refuge from herbivory (Fong et al 2006;Smith et al 2010). While many studies have focused on either the relative costs or benefits of epiphytic associations (e.g., Pereira et al 2010), few to our knowledge have simultaneously studied both costs and benefits (but see Fong et al 2006;Smith et al 2010).…”

“…The few studies done on tropical reefs found that cyanobacterial epiphytes strongly limit the grazing activity of consumers (Paul 2008), a well-established force controlling algal proliferation on coral reefs (for a review see Fong and Paul 2011). By providing an associational defense, cyanobacterial epiphytes contribute to the formation and persistence of blooms of host algal species (Fong et al 2006;Smith et al 2010). At present, this research has focused on palatable (Fong et al 2006) or chemically defended hosts (Smith et al 2010), not on both physically and chemically defended species.…”

“…By providing an associational defense, cyanobacterial epiphytes contribute to the formation and persistence of blooms of host algal species (Fong et al 2006;Smith et al 2010). At present, this research has focused on palatable (Fong et al 2006) or chemically defended hosts (Smith et al 2010), not on both physically and chemically defended species. As the incidence of cyanobacterial blooms is increasing, especially in response to climate change (Paerl and Paul 2011), it is essential to understand the effects they may have on other key primary producers.…”