Ocean warming and acidification have complex interactive effects on the dynamics of a marine fungal disease

Abstract

Diseases threaten the structure and function of marine ecosystems and are contributing to the global decline of coral reefs. We currently lack an understanding of how climate change stressors, such as ocean acidification (OA) and warming, may simultaneously affect coral reef disease dynamics, particularly diseases threatening key reef-building organisms, for example crustose coralline algae (CCA). Here, we use coralline fungal disease (CFD), a previously described CCA disease from the Pacific, to examine these simultaneous effects using both field observations and experimental manipulations. We identify the associated fungus as belonging to the subphylum Ustilaginomycetes and show linear lesion expansion rates on individual hosts can reach 6.5 mm per day. Further, we demonstrate for the first time, to our knowledge, that ocean-warming events could increase the frequency of CFD outbreaks on coral reefs, but that OA-induced lowering of pH may ameliorate outbreaks by slowing lesion expansion rates on individual hosts. Lowered pH may still reduce overall host survivorship, however, by reducing calcification and facilitating fungal bio-erosion. Such complex, interactive effects between simultaneous extrinsic environmental stressors on disease dynamics are important to consider if we are to accurately predict the response of coral reef communities to future climate change.

Keywords: bio-erosion; climate change; coral reef; coralline fungal disease; ocean acidification; temperature.

Figure 1.

Location of Palmyra Atoll and the permanent monitoring sites established in 2008 (1–5 = shallow terrace; 6 = backreef; 7–12 = forereef).

Figure 2.

(a) Field signs of CFD. The active lesion is shown by the two black arrows. Day-old exposed substrate becomes colonized by microalgae and turf algae (1) and appears bleached white when freshly exposed (2), while the CCA tissue remains healthy looking on the leading edge of the lesion (3). Scale bar, 1 cm. (b) Appearance of isolated fungal hyphae associated with CFD (1000× magnification using light microscopy). Scale bar, 15 µm. (c) Section of a coralline algal infected with CFD and positively confirmed as a fungal infection using Grocott's methenamine silver. Note the fungal hyphae invading the algal thallus and conceptacles (arrows). Cu, cuticle. Scale bar, 30 µm. (Online version in colour.)

Figure 3.

Representative in situ temperatures at Palmyra Atoll at 10 m on the forereef and SST from satellite-derived sources during 2008, 2009 and 2010, and the associated change in CFD occurrence (forereef-wide mean number of cases m⁻² of CCA are shown by black arrows).

Figure 4.

(a) Mean (±s.e.) calcification rate for diseased and healthy CCA in experimental aquaria (n = 12). Change in weight shown as mg CaCO₃ week⁻¹ for each thallus. Asterisk indicates when response within treatment differs significantly between diseased and healthy specimens (table 1). (b) Mean (±s.e.) lesion lateral expansion rate for diseased CCA in experiments. Using the ambient air × 28°C treatment as a control value, the asterisk indicates a significant effect of elevated temperature (Dunn's Z = 3.156, p = 0.0048).