Most scleractinian corals and many other cnidarians host intracellular photosynthetic dinoflagellate symbionts (“zooxanthellae”). The zooxanthellae contribute to host metabolism and skeletogenesis to such an extent that this symbiosis is well recognised for its contribution in creating the coral reef ecosystem. The stable functioning of cnidarian symbioses is however dependent upon the host’s ability to maintain demographic control of its algal partner. In this review, I explain how the modern envelope of seawater conditions found within many coral reef ecosystems (characterised by elevated temperatures, rising pCO2, and enriched nutrient levels) are antagonistic toward the dominant host processes that restrict excessive symbiont proliferation. Moreover, I outline a new hypothesis and initial evidence base, which support the suggestion that the additional “excess” zooxanthellae fraction permitted by seawater pCO2 levels beyond 260 ppmv significantly increases the propensity for symbiosis breakdown (“bleaching”) in response to temperature and irradiance extremes. The relevance of this biological threshold is discussed in terms of historical reef extinction events, glacial-interglacial climate cycles and the modern decline of coral reef ecosystems.