Impact of cyclones on hard coral and metapopulation structure, connectivity and genetic diversity of coral reef fish

Coral Reefs https://doi.org/10.1007/s00338-021-02096-9 REPORT Impact of cyclones on hard coral and metapopulation structure, connectivity and genetic diversity of coral reef fish Gabriele Gerlach1,2,3 Michael J. Kingsford3 • Philipp Kraemer1 • Peggy Weist1 • Laura Eickelmann1 • Received: 8 October 2020 / Accepted: 3 April 2021 Ó The Author(s) 2021 Abstract Cyclones have one of the greatest effects on the biodiversity of coral reefs and the associated species. But it is unknown how stochastic alterations in habitat structure influence metapopulation structure, connectivity and genetic diversity. From 1993 to 2018, the reefs of the Capricorn Bunker Reef group in the southern part of the Great Barrier Reef were impacted by three tropical cyclones including cyclone Hamish (2009, category 5). This resulted in substantial loss of live habitat-forming coral and coral reef fish communities. Within 6–8 years after cyclones had devastated, live hard corals recovered by 50–60%. We show the relationship between hard coral cover and the abundance of the neon damselfish (Pomacentrus coelestis), the first fish colonizing destroyed reefs. We present the first long-term (2008–2015 years corresponding to 16–24 generations of P. coelestis) population genetic study to understand the impact of cyclones on the meta-population structure, connectivity and genetic diversity of the neon damselfish. After the cyclone, we observed the largest change in the genetic structure at reef populations compared to other years. Simultaneously, allelic richness of genetic microsatellite markers dropped indicating a great loss of genetic diversity, which increased again in subsequent years. Over years, metapopulation dynamics were characterized by high connectivity among fish populations associated with the Capricorn Bunker reefs (2200 km2); however, despite high exchange, genetic patchiness was observed with annual strong genetic divergence between populations among reefs. Some broad similarities in the genetic structure in 2015 could be explained by dispersal from a source reef and the related expansion of local populations. This study has shown that alternating cyclone-driven changes and subsequent recovery phases of coral habitat can greatly influence patterns of reef fish connectivity. The frequency of disturbances determines abundance of fish and genetic diversity within species. Keywords Disturbance
Cyclone
Neon damselfish
Coral reef fish
Larval dispersal
Genetic diversity
Connectivity Topic editor Morgan S. Pratchett Supplementary Information The online version contains supplementary material available at https://doi.org/10.1007/s00338021-02096-9. & Gabriele Gerlach 1 Carl Von Ossietzky University Oldenburg, 26111 Oldenburg, Germany 2 Helmholtz Institute for Functional Marine Biodiversity HIFMB Oldenburg, Oldenburg, Germany 3 ARC Centre of Excellence for Coral Reef Studies and College of Science and Engineering, James Cook University, Queensland, Australia Introduction Cyclones are one of the most important key drivers of ecological heterogeneity and ecosystem function (Halford et al. 2004; Fabricius et al. 2008; Halford and Perret 2009; Roff et al. 2015; Puotinen et al. 2016). At the Great Barrier Reef, Australia, tropical storms and cyclones account for 48% of the respective estimated losses of coral cover followed by coral predation by crown of thorns starfish that caused 42% and coral bleaching 10% of coral loss (De’ath et al. 2012); the latter, however, has recently increased dramatically (Torda et al. 2018). Physical abrasion of coral 123 Coral Reefs cover, rolling and tossing of coral boulders and extensive movements of rubble all cause pronounced changes and destruction of a reef architecture. Storm-induced coral loss can have a devastating effect on coral species assemblages due to loss of shelter, habitat and food (Doherty et al. 1997; Woolsey et al. 2012). In contrast to these devastating effects, Connell (1978) predicted that intermediate disturbance such as storms might be beneficial to ecosystem functioning because disturbances create the highest diversity by maintaining coral reefs in a non-equilibrium state with newly appearing niches providing space and shelter to specialized species with high colonization potential. Soon after a severe disturbance, diversity is supposed to be low because the time for colonization is short; only those few species that can cope with reduced shelter, produce propagules fast and happen to be within dispersal range will colonize disturbed habitat after a cyclone. While most ecologists have focused on changes in biodiversity and re-colonization potential after a disturbance event, the integration of evolutionary processes that have shaped species assemblages is much less considered. Yet, genetic variation within populations is the essence of evolution and may affect population viability and adaptability with consequences for the composition of associated communities, their metapopulation structure and ecosystem functioning (see for review Banks et al. 2013). In a modeling approach, Fraser et al. (2018) predicted that species with dispersal on small spatial scales, but rare on larger scales would show no spatial structure on small scales and strong structure on large scales. Furthermore, disturbance would influence the chance of genetic turnover in a population. Our long-term study (2008–2015) on the coral reef fish Pomacentrus coelestis, a common species of the Great Barrier Reef, Australia, offers an ideal opportunity to test these predictions and to understand how disturbances can drive metapopulation dynamics and intraspecific structure. At the Capricorn Bunker Reef (CBR) group (Fig. 1) P. coelestis has a surprisingly short life cycle with an agemaxima of 127–160 days (Kingsford et al. 2017), which means a potential local population extirpation and a population turnover of two to three generations per year (corresponding to16–24 generations in 8 years from 2008–2015). P. coelestis prefer highly disturbed coral reefs (Doherty et al. 1996); the abundance of P. coelestis is generally low when percentage cover of live coral is high (Bell and Galzin 1984; Halford et al. 2004). After a cyclone event, abundance of most other fishes such as macro- and meso-predators of the families Serranidae and Lutjanidae that seek habitat complexity is greatly reduced; therefore, metapopulation structure and connectivity of P. coelestis is mostly driven by habitat availability (Jones et al. 2004). 123 We aimed to understand how stochastic habitat appearance would influence metapopulation structure and genetic diversity. Our approach was to analyze the dynamics of the population genetic structure before and after a cyclone disturbance. We intended to reveal settlement and colonization at reefs affected by storm events and try to locate source-reef populations within the CBR group at the southern tip of the Great Barrier Reef, within an are (...truncated)