Farming of the fire-coral Millepora alcicornis for reef restoration purposes: the influence of inclination on growth

Reef environments around the world have been suffering from anthropogenic impacts, which may result in reduction in species diversity and abundance (Hughes, Graham, Jackson, Mumby & Steneck 2011). Several methodologies to enhance reef recovery have been proposed, but the combination of coral transplantation with substrate stabilization has been argued to be the most effective method (Rinkevich 2005; Williams & Miller 2010). However, transplantation always involves some impact for the donor population. Therefore, Rinkevich (1995) suggested that mariculture in nurseries might be more effective for coral restoration programs. Branching corals would be particularly useful for this application, due to their fast growth, asexual propagation and creation of 3D complex structures (Oliveira, Leão & Kikuchi 2008; Shaish, Levy, Katzir & Rinkevich 2010).

Fragment orientation and light irradiance affect axial corallite development (growth and shape) in branching acroporids (Kaniewska, Campbell, Fine & Hoegh-Guldberg 2009). Therefore, it is important to consider colony or fragment orientation in zooxanthellate coral nurseries, since their photosynthetic capacity and growth rates are directly related to light. Despite its relevance, few coral farming studies have focused on the effect of orientation in branching zooxanthellate coral nubbins (Kaniewska et al. 2009). Consequently, the effect of inclination on growth and shape and their relevance in restoration programs has been largely ignored (Shafir, Edwards, Rinkevich, Bongiorni, Levy & Shaish 2010).

This study compared growth rates and shape of nubbins from the fire coral Millepora alcicornis Linnaeus growing on vertical and horizontal positions. The hypothesis was that fragments placed horizontally would receive more light as they would have a larger surface transversal to the light source than vertical ones and, consequently, would display higher growth rates.

Millepora alcicornis nubbins were prepared by collecting fragments, with their original position being mainly vertical, from 10 different colonies from Recife de Fora, Porto Seguro, Brazil (16°24′ S; 038°59′ W). Each fragment (15–80 mm long) was fixed in a tubular PVC base (80 × 20 mm) using underwater epoxy (Tubolit Ltda, Rio de Janeiro, Brazil). Between four and eight nubbins from each colony (totalling 96 coral nubbins) were placed in three racks on a shallow patch reef (16°24′ 47″ S; 038°59′ 15″ W) near Recife de Fora, at 20–30 cm of depth at low tide. Each rack supported 16 coral nubbin pairs, each pair from the same colony, with similar shape and size, one horizontally and the other vertically oriented.

Each nubbin was weighed to quantify growth (buoyant weight method; Davies 1989), at the beginning and end of the experiment, totalling 100 days (July–November 2010). The number of new growth tips was counted at the end of the experiment. Three HOBO Light loggers (Onset, Cape Cod, MA, USA) were placed on the reef to evaluate irradiance differences.

The amount of light received by vertical and horizontal nubbins was different. Direct light, received by the tips on vertical nubbins and the sides facing the light of horizontal ones was almost 10-fold higher than the scattered light received by side facing down and sideways in horizontal and vertical nubbins, respectively (F_[2] = 57.540; P < 0.0001; One-way repeated measures anova) without significant differences between scattered light facing sideways and facing down.

No dead coral nubbins were found during the study, showing that it is feasible to farm M. alcicornis nubbins in field nurseries using small branches for recovery purposes in coral restoration programs (from 15 to 80 mm).

Growth patterns and rates in M. alcicornis were dependent on branch orientation. Horizontal nubbins showed more new growth tips (6.16 ± 0.69; average ± SD) than vertical (2.97 ± 0.39) ones (One-way repeated measures anova; F_[1] = 14.924; P < 0.0001) demonstrating differences in growth patterns between treatments. In addition, new growth tips on horizontal nubbins were significantly higher on the side facing the light (4.43 ± 0.34) than on the side facing down (1.73 ± 0.18; Paired T-test t = 7.482; df = 28; P < 0.0001) suggesting a relation between light and new tips arising. Contrary with the occurrence of new growth tips, growth rates were significantly higher in vertical nubbins (One-way repeated measures anova; F_[1] = 6.103; P < 0.05; Fig. 1).

Since horizontal fragments had a relatively larger surface area to receive direct light, they should have displayed higher growth rates compared with vertical ones, as observed by Edmunds (1999). However, the opposite trend was found here, with vertical nubbins displaying higher growth rates than horizontal, while horizontal had greater number of new growth tips. Several reasons could explain differences in growth rates after a shift in light regime in scleractinian corals. It could be related with photoacclimation, such as changes in zooxanthellae size, density and distribution, and their chlorophyll concentration (Winters, Beer, Zvi, Brickner & Loya 2009), which may affect colony growth and shape (Rosenfeld, Yam, Shemesh & Loya 2003). However, differences in allocation of resources for skeletal growth and/or tissue differentiation could play an important role in milleporids, since they have much higher calcification rates near growth tips (Goreau 1963). Growth in branching scleractinians is generally determined by energy allocation for tissue growth, which shows a positive skeletal deposition with negative tissue growth, at least for small branches (Anthony, Connolly & Willis 2002). This condition may also occur in milleporids, where growth in M. alcicornis would be limited by the energetic cost of tissue growth.

The change in branch orientation to a horizontal position could have shifted the resource allocation to growth from the original growing tip to the area facing the greatest amount of light, a phenomenon also coupled with photoacclimation processes of their zooxanthellae. After a period of decreased calcification, it would be expected that skeletal growth would be greatly increased by zooxanthellae photoacclimation and by the number of new branches that could greatly influence the formation of complex 3D structures. Such structures provide instant shelter for several reef organisms and rapidly regenerate reef physiognomy (Shaish et al. 2010).

These results are key to the development of successful coral restoration programs. The choice of coral nubbin inclination may result in faster growth (or shorter implantation times), or in the production of more new branches (or faster reaching of 3D complex structures). Therefore, the effect of inclination on growth speed and shape should be considered in restoration programs involving coral nursery and coral fragment transplantation. We suggest that horizontal fire-coral nubbins should be used to produce colonies for branch donation, while vertical fire-coral nubbins should be used for transplantation in whole colony short-term coral restoration programs.