Research Article: Filamentous calcareous alga provides substrate for coral-competitive macroalgae in the degraded lagoon of Dongsha Atoll, Taiwan

Date Published: May 16, 2019

Publisher: Public Library of Science

Author(s): Carolin Nieder, Chen-Pan Liao, Chaolun Allen Chen, Shao-Lun Liu, Sebastian C. A. Ferse.

http://doi.org/10.1371/journal.pone.0200864

Abstract

The chemically-rich seaweed Galaxaura is not only highly competitive with corals, but also provides substrate for other macroalgae. Its ecology and associated epiphytes remain largely unexplored. To fill this knowledge gap, we undertook an ecological assessment to explore the spatial variation, temporal dynamics, and diversity of epiphytic macroalgae of Galaxaura divaricata on patch reefs in the lagoon of Dongsha Atoll, a shallow coral reef ecosystem in the northern South China Sea that has been repeatedly impacted by mass coral bleaching events.

Twelve spatially independent patch reefs in the Dongsha lagoon were first surveyed to assess benthic composition in April 2016, and then revisited to determine G. divaricata cover in September 2017, with one additional Galaxaura-dominated reef (site 9). Four surveys over a period of 17 months were then carried out on a degraded patch reef site to assess the temporal variation in G. divaricata cover. Epiphytic macroalgae associated with G. divaricata were quantified and identified through the aid of DNA barcoding at this degraded site.

Patch reefs in the Dongsha lagoon were degraded, exhibiting relatively low coral cover (5–43%), but high proportions of macroalgae (13–58%) and other substrate (rubble and dead corals; 23–69%). The distribution of G. divaricata was heterogeneous across the lagoon, with highest abundance (16–41%) in the southeast area. Temporal surveys showed consistently high covers (mean ± SD = 16.9 ± 1.21%) of G. divaricata for 17 months. Additional photographic evidence suggested that overgrowth of G. divaricata can persist for 3.5 years. Yet, G. divaricata provides substrate to other macroalgae (e.g., Lobophora sp.) that also limit the growth of corals.

Our study demonstrates that an allelopathic seaweed, such as G. divaricata, can overgrow degraded coral reefs for extended periods of time. By providing habitat for other harmful macroalgae, a prolonged Galaxaura overgrowth could further enhance the spread of macroalgae, and strengthen negative feedback loops, decreasing the recovery potential of degraded reefs.

Partial Text

Coral-macroalgae competition is a natural ecological process on coral reefs [1]. However, anthropogenic disturbances, e.g., climate change, overfishing, and pollution, have intensified space competition between macroalgae and corals and in turn led to a phase shift from a coral-dominated to a macroalgae-dominated ecosystem [2]. The recovery of corals on degraded reefs is strongly influenced by the type of dominant macroalgae, i.e., allelopathic versus non-allelopathic [3,4]. Allelopathic macroalgae produce lipid-soluble secondary metabolites, e.g., loliolide derivatives or terpenes that are poisonous to corals (known as allelochemicals). Such allelochemicals are capable of bleaching and killing coral tissue [5], decreasing the photosynthetic efficiency of zooxanthellae [6], and altering the coral microbiome, ultimately decreasing coral health [7,8]. Allelopathic macroalgae are considered most detrimental for the resilience of coral reefs [9], as these types may perpetuate their dominance by deterring coral larval settlement, and inhibiting the growth and survival of juvenile recruits, key processes of coral reef recovery [10–12].

Our study shows that most patch reefs in the lagoon of Dongsha Atoll are degraded. Many of the lagoon patch reefs (ca. 63% of the surveyed areas) exhibit relatively low coral cover (< 30%) and high proportions of macroalgae, dead corals, and rubble, all of which are signs of reef degradation [36]. This is consistent with previous surveys that reported degraded conditions of lagoon patch reefs at Dongsha Atoll [37,38]. The filamentous form of Galaxaura divaricata showed highest abundance in the southeast lagoon. Galaxaura overgrowth was also observed in other locations in the southeast lagoon in previous surveys (Keryea Soong, personal communication; our own macroalgae inventory in 2012). The exact causes for this localized condition are not well understood. However, a potential explanation may be that the southeast lagoon is sheltered by a 2 km-wide reef flat, harboring very shallow (1–5 m) and calm waters that may provide suitable growth conditions for G. divaricata. The proliferation of macroalgae is likely the consequence of an initial coral decline [39,40]. The synergistic effects of thermal stress, overfishing, and typhoon damage may have caused the decline of the once pristine corals in the Dongsha lagoon, followed by a proliferation of G. divaricata and other macroalgae. Thermal stress on corals has increased over the past decades, with waters surrounding Dongsha Atoll warming at a faster rate than other areas of the South China Sea [37,41,42]. Recurrent bleaching events have caused high coral mortality and eradicated thermo-sensitive coral genera from the lagoon [43]. Overfishing and the extensive use of dynamite and cyanide, prior to the establishment of the Dongsha Atoll National Park in 2007 reduced fish, and destroyed large areas of coral framework [20,44]. Insufficient grazing by fish after disturbance can lead to the establishment and full outgrowth of macroalgae beyond their early stages [45]. Galaxaura is known to be largely unpalatable for various herbivorous fishes due to its calcareous thallus and low nutritional content [46–48]. Local herbivorous fish population in the Dongsha lagoon may not be effective to control the outgrowth of Galaxaura in certain areas. Our observations illustrated that the allelopathic and unpalatable filamentous seaweed, Galaxaura divaricata, can become dominant on degraded reefs in shallow, sheltered, and calm environments. We show that G. divaricata provides suitable substrate for a variety of macroalgae, further facilitating macroalgae growth and abundance on degraded reefs. Thus, a prolonged proliferation of Galaxaura could potentially enhance negative feedback loops, thereby perpetuating reef degradation. Several common epiphytic macroalgae on Galaxaura are allelopathic and known to frequently overgrow corals. Macroalgal assemblages, such as the Galaxaura-epiphyte system, warrant further investigation to better understand their ecological implications on the resilience of coral reefs, especially of shallow atoll lagoons. There are 439 listed coral reef atolls on earth; among them are 335 with semi-enclosed lagoons [65]. Atoll lagoons are highly productive and serve as valuable nursery habitat for marine life; however, they are most vulnerable to the effects of climate change [50,66]. Results from our study can be informative for the management and conservation of lagoons and shallow, inshore coral reef ecosystems, especially in the South China Sea and the Pacific Ocean, where filamentous Galaxaura is very common.   Source: http://doi.org/10.1371/journal.pone.0200864