0034-7744 0034-7744 S0034-77442014000700015 00 09 2014 00 09 2014 62 318 329

Genet and reef position effects in out-planting of nursery-grown Acropora cervicornis (Scleractinia:Acroporidae) in Montego Bay, Jamaica

Efectos de la posición en el arrecife y del linaje en el crecimiento de Acropora cervicornis (Scleractinia:Acroporidae) en una plantación de vivero en Bahía Montego, Jamaica

Andrew M. Ross1*
Abstract

The reef-building coral Acropora cervicornis was a dominant ecosystem element on the Caribbean reef until the 1980s, when it declined by some 97% due primarily to anthropogenic ecosystem changes and disease. This branching species expanded its colony footprint and achieved local dominance largely through fragmentation and regrowth, thus is suited to nursery culture ]]> Acropora cervicornis of four lineages or genets were followed and measured for growth and health over 12 months in 2006 and 2007 on buoyant drop-loop line nurseries at one shallow and one deep fore-reef site in Montego Bay, Jamaica. Sixty-five of these corals were then out-planted to wild reef sites of similar depth and condition to their respective nurseries ]]> Hermodice carunculata predation was the primary problem in the shallow fore-reef, and was combined with a banding syndrome at the deeper site. This syndrome was noted in the samples prior to planting, during a one week storage period on the seafloor. Continued slow decline occurred in the subsequent seven months in the shallow fore-reef site; however, regrowth was noted in ]]>
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Key words: Acropora cervicornis, coral gardening, coral restoration, coral propagation, Hermodice carunculata.

Resumen

La especie constructora de arrecifes de coral Acropora cervicornis era un elemento dominante del ecosistema en el arrecife caribeño hasta la década de 1980, cuando disminuyó en un 97% a nivel regional principalmente debido a ]]> Acropora cervicornis de cuatro linajes fueron seguidos y medidos para el crecimiento y la salud durante 12 meses en 2006 y 2007 en viveros en línea tipo ]]> Hermodice carunculata fue el principal problema en el arrecife frontal poco profundo y se combinó con un síndrome de bandas en el sitio más profundo. Este síndrome se observó en las muestras antes de la siembra, durante un período de almacenamiento de una semana en el suelo marino. A continuación ocurrió un lento descenso en los posteriores siete meses en el sitio de arrecife frontal poco profundo; sin embargo, se observó un rebrote en el sitio más profundo con el material restante. Aún ]]>

Palabras clave: Acropora cervicornis, coral cuerno de ciervo, propagación de cultivo de ]]> Hermodice carunculata.

The Acropora of the tropical ]]> Acropora cervicornis was the dominant coral from 5m through 20m depths, an area coined by Goreau (1959) as the Acropora cervicornis zone, through most of the Caribbean prior to the early 1980s. Today this species is sparse throughout its range with only a handful of such thicketed habitats remaining and some authors paint a bleak picture for its future. They suggest that a naturally relatively low level of sexual reproduction, a lack of larger spawning animals, the distance between them, chronic ]]>

Several authors have explored the potential for coral gardening to begin to preserve or restore these ]]> A. cervicornis material within a single year of nursery growth. It is interesting that corals that grow so well in the nursery are still in decline in the wild (Miller, Bourque & Bohnsack, 2002; ABRT, 2005; Alcolano, Caballero & Perera, 2009). This suggests that one may separate the corals from their problems by simply separating them from the substrate: their issues appear to be particularly benthic and not waterborne or intrinsic to the corals themselves. Planting this growth from the nursery to the reef is the next step in elucidating ]]>

This work is the final in a series of studies in nursery growth of A. cervicornis wherein strong differences in growth rate and susceptibility to temperature, fouling ]]>

Methods

In April 2006, two Buoyant Drop-Loop Line (BDL) nurseries (Ross, 2013a) were set at each of two sites in Montego Bay, Jamaica: a large sand area adjacent to a large ]]>
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Hurricane Dean passed the western tip of Jamaica on August 20, 2007. These maintenance nurseries were sequestered from August 19 for approximately one week by placing them into sediment-free hollows in the reef. Shortly after this storm these corals were planted to adjacent clean reef substrate.

At the deep nursery ]]> A. cervicornis was present on the reefal stone, though it was present on the continental shelf some 30m away and no active disease was noted in ]]>

For planting, diseased portions were cut away with clean side-cut pliers 1cm to 2cm ahead of the advancing disease front, as a banding syndrome (likely WBD1) had beset many samples during sequestration. Where the disease front was in the middle of the coral, it was cut into two or more independent fragments, 1cm to 2cm of live-tissue waste was cut away before the advancing disease front in this experiment. In trials at the Doctor’s Cave Beach ]]>

Galvanized masonry nails were immersed in seawater and left outdoors in a mesh bag until they developed a uniform flat grey patina, for approximately two weeks. Fresh galvanized wire or nails will kill the contacting coral tissue; ]]> A. cervicornis planting trials at the Doctor’s Cave Beach Club, Montego Bay, Jamaica (unpublished).

To plant each coral, one pre-aged ]]>
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The nurseries within the buttress system were anchored at 7m depth, thus the nursery corals were growing elevated to between 6.2m and 5.5m from the surface. For Hurricane Dean these shallow nurseries were bundled into a clean, shallow cave at 8m depth within the buttress system. After the storm, these bundles were moved atop a partially urchin-grazed buttress-end at 3m depth at the top, surrounded by caverns on the shoreward sides and a large sand patch on the seaward side all at 9m depth making the planting area ]]> A. cervicornis, both of which were small and stressed, the larger (<0.25m2) hosting a Stegastes planifrons nest. Between 3m and 5m depth and concentrating on the southern face of the planting stone was an area of reasonably urchin- ]]> Diadema antillarum urchins were present.

Small limestone projections, knobs and nodules are common on such shallow patch reef-tops, remnants of small massive and branching corals long dead. In coral planting, such knobs were held firmly and shaken to ascertain the knob’s strength given boring organisms, primarily Cliona ]]>

The planted corals ]]>

The photographs were evaluated using CPCe’s Accumulated Lengths function taking both total skeletal and living tissue lengths. Live and dead lengths were taken for each branch and sources of death were assessed, where possible. No consideration was made for error associated with parallax (Ross, 2012a).

]]> Preliminary analysis of CPCe data was carried out using Microsoft Excel software for Macintosh. Statistical tests, including ANOVA, non-parametric correlations and graphing were performed using SPSS18 statistical software. Nonparametric correlations between i) apical polyp count, ii) worm bite count, iii) active disease front count, iv) total live plus dead length, v) dead length and vi) living coral length were assessed using Spearman’s rho. Correlations between Log base-10 transformation of the initial live and the final live coral lengths were provided by a ]]>

1. There is no significant difference in living coral length between the deep and shallow sites,
]]> 2. There are no significant differences in living coral length between the different visit dates,

3. There are no significant differences in living coral length between the different coral genets,

4. There is no significant interaction between the site, visit and/or genet with regard to living coral length.

Results

The shallow site saw greater survivorship than the deeper site. Sixty-five corals were set in September 2007. Forty-six (70.8%) were still in place and 35 (53.8%) were still alive by the summer of 2008. Of the 36 corals planted at the shallower site, eight were missing and much partial mortality was observed, but all 28 corals present were alive at 11 months (77.8%). At the deeper reefal stone site, of the 29 samples set, 11 were lost (37.9%) and 11 died entirely, leaving only seven surviving (24.1%, Table 1). Damages were observed by the first measurement and continued through the first four months with every coral in this experiment suffering partial mortality.



At both sites partial mortality was substantial, with 47% of tissue lost in the shallow site and 91% in the deep (Table 3). Losses were continuous from planting through the final measure in the deep site even after the initial pulse of predation and ]]> Table 3). The deep site saw a rapid decline early, with disease killing corals entirely. However, after an initial pulse, the continued decline was primarily through remaining or continuing disease and sample loss after the December visit. Lost corals may have been attributed to waves in the shallow site, though curious or clumsy spear-fishermen and recreational snorkelers may also have played culprit. At the deeper site an Antillean Z-trap (fish trap) was removed from atop the reefal stone and samples on one occasion, and ]]>

The September 14 interim observations at the deep site show disease starting either at the benthic contact point, possibly associated with damages incurred during planting, or at the branch tips suggesting vectoring or facilitation by ]]> Hermodice carunculata (Fire-Worm) with pathogen entry at the bite or lesion. H. carunculata attacks were common in this interim visit but were obscured by more general (disease) death by the time of the formal monitoring visit in October. There was no indication that disease started at the points where disease was cut away as an advancing disease front was not necessarily discernable from a H. carunculata bite.

The trend over time for mean live coral length is great initial partial mortality, followed by a levelling out in mortality and slight growth at the deep site but a continued slow reduction at the shallow site ( Table 4). In the month after planting, the shallow buttress site saw growth, with a per-coral average increase of 3.4%, or 2.4cm per coral. However, in the following period H. carunculata worms found these new corals and consumed some 30.8% of the total crop over two months; an average of 22.2cm per coral. This site continued to decline slightly in average live coral length through the remainder of the experimental period through ]]> H. carunculata predation.

The deeper site saw damage almost immediately with disease present in the first photo. Between loss, disease and H. carunculata feeding this site’s mean coral length declined by some 82.6% in the first six weeks and a further 28.6% by December. However, from this greatly depressed state it was able to regrow by some 10.7% in the remaining seven months (Table 4) during which it was monitored.

New apical polyp ]]>
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Both the shallow and deep sites saw an increase in the average number of apical polyps per coral between the third and final visits as the remaining tissue started to re-grow (Fig. 1). The difference between this and Table 3 at the shallow site was that, as apical polyp and branch formation continued, predation also continued.
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A decline was noted generally through the experimental period in each genet. At the shallow site, Orange and Green lost 28% and 41% tissue respectively until day 110 (visit 3). Orange then held at 28% while Green declined by 61% by the final visit. Blue lost 21% of its average length by day 110 and declined a further 25% by the final visit. White also declined by 21% by day 110 but had regained an average of some 3.1cm per coral by the final visit (Table 5).

At the deep site, Orange again remained relatively steady between days 110 and 340, with 77% and 78% loss respectively. White and Blue saw greater losses, losing 94% and 89% respectively at day 110, with White remaining steady through day 340 while Blue improved its average coral size by some 3.8cm per coral. Green expired entirely within the experimental period at this site. A marked decline in dead skeleton length was noted between days 110 and ]]>

General Linear Model (GLM) ANOVA testing (Adjusted R Squared 0.235) showed the live length to be significantly different between sites (p <0.001), between different measurement visits (p <0.001) and between genets (p= 0.008). Post hoc testing showed that Blue, White and Green genets made up the subset with the least coral length and White, Green and Orange made up the ]]> Figures 4 and 6, these post hoc differences were largely associated with uneven initial amounts of coral and the particular failure of the Green genet at both sites. A significant interaction between site and day (p= 0.022) speaks to rapid disease onset in the early measurements at the deeper site and H. carunculata attack in between visits at the shallower site.
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The differences between the genets seen in Table 4 are illustrated in Figure 2, whereby a rapid decline in live coral length is seen in the deep site in all genets with a continued fall in the Green genet to zero, but a mild increase in the Blue genet to the final visit. In the shallow site a brief period of growth may be seen in the White and Orange genets and a mild decline in ]]>
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There was no correlation between recent H. carunculata attack and length of living tissue occurring through the 11 months (Spearman’s rho r= -.064, p= 0.356). This was in part due to the worm’s apparent lack of preference in coral size, but also that once the coral was attacked the amount of living coral for ]]> H. carunculata bites and the apical polyp count (Spearman’s rho r= -0.333, p <0.001) as the worms actively ate the branch tips.

The worms in this reef patch were ]]> Fig. 3A) and were the primary factor limiting coral growth at the shallow site.

Disease was negatively correlated to living tissue length (Spearman’s rho r= -0.396, p <0.001). This did not mean that disease tended to occur in smaller corals, but rather disease shortened the living portion of the coral for assessment. Similarly, the count of disease fronts was negatively correlated with the number of apical polyps (Spearman’s rho r= -0.387, p <0.001) as apical polyps were either killed by the disease or associated with worm ]]> Fig. 3B).

Figure 4A suggests that there is little difference between the genets with respect to worm attack, which may be expected in a coral reliant on rapid growth and overgrowth as its strategy for reef dominance: it would not invest much in chemical ]]> Figure 4B suggests a weak trend towards Green being more susceptible to disease than the other genets. This would corroborate its general weakness, though Orange trends towards being the least susceptible to disease.

There was a significant positive correlation between the initial live and the final live coral lengths (Pearson r= 0.387, p= 0.023).

Occasional partial mortality with banding disease was seen where portions of the total coral were not killed. These were often sections that were somehow physically separated from the primary coral, e.g. sections broken away by fish-pot or diver damage or broken portions of the drop-loop overgrowth held attached by the underlying nylon line without tissue contact.
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Bleaching occurred at the shallow site likely associated with the stress of sequestration, a reduction in depth from the shallow nursery at some 5m and 6m depth to the planting site at 5m to 3m depth and from the seasonal temperatures regardless of relocation activities, though these factors were not assessed in this study. Bleaching did not kill any samples and was only prevalent in the Green genet.

]]> Discussion

Publishing or inclusion of negative outcomes and experimental failures in reporting and published literature is necessary to build a larger picture of the lessons learned by the restoration and manipulation community (Edwards & Gomez, 2007), but also to shed larger light on the factors affecting ]]>

At first glance this study may suggest that propagative coral enhancement of A. cervicornis is folly, as the successes of the nursery are not immediately translated into successes on the planted reef. In fact the opposite is true. The amount of coral initially harvested from the wild reef for 65 fragments at five cm each, some 325 linear centimetres, with nursery growth yielded some 4 277.5 centimetres for planting after a preliminary harvest for nursery re-sets and disease pruning. After 11 months, 1 521.15cm remained, giving a net increase of 1196cm or 4.7-fold from the initial wild harvest. Had this been a direct parent-to-planting relocation without an interim nursery phase, the 64.48% decline seen here would ]]>

In this study the corals of the shallow, buttress-end reef grew and attached to the substrate for the first measurements, but by day 100 were heavily set upon by at least ]]> Hermodice carunculata (fire-worm) that consumed much of the branch and apical material, essentially halting growth. After the initial attack period these corals remained at a similar size, with no particular re-growth or further decline noted in the 11 months in mean coral length, though some apical growth and further worm bites were noted. This suggests that a critical mass of coral may be planted on an appropriate area that will maintain a reasonably steady population ]]>

At the deeper reefal stone site fewer worm attacks were combined with a banding syndrome that was apparently inherent in the sediments, as per Patterson et al. (2002), and possibly exacerbated by macroalgae as this site was largely ungrazed (Nugues et al., 2004) as some corals were showing disease during pre-planting storage, before they were planted to the reef. This ]]>

Control of corallivores is a vital aspect of restoration of Acropora, and the first, simplest ]]>

Larger corals had significantly more living tissue at the end of the experiment. This suggests that a restoration programme use the largest fragments possible to maximize the amount of material remaining after predation or disease, as well as ]]> H. carunculata only bites as far as it may engulf the branch, thus larger corals should be less susceptible per unit length to this type of attack. Relatedly, once a branch has been bitten it will not be attacked again: the coral’s own exposed, dead skeleton protects it from further attack so long at the next worm is not larger. ]]>

The patterns of strong (Blue and White) and weak (Orange and Green) genets seen in the nursery (in Ross, 2013c) were not overtly apparent in these wild out-plants. Predation and disease were the primary issues and apparently not subject to genet influences, as opposed to the bleaching and fouling abrasion seen in the nurseries. The Green genet was the only genet to bleach with the ]]>

Acknowledgments

This author would like to thank the late Kevin Kohler for adding the “combined lengths” function to CPCe in a single afternoon, the Doctor’s Cave Beach Club for their logistical support and Dale Webber of the Centre for Marine Sciences, UWI Mona, for pointing out that there is valuable data in photographic notes. The author would further like to thank the reviewers of this manuscript for their time and guidance.
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1. Seascape Caribbean; ross.andrew@mac.com
Received 15-VIII-2013 Corrected 14-III-2014 Accepted 24-III-2014
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