Biological responses of the coral Montastraea annularis to the removal of filamentous turf algae.

Coral reef degradation increases coral interactions with filamentous turf algae (FTA) and macroalgae, which may result in chronic stress for the corals. We evaluated the effects of short (2.5 month) and long (10 month) periods of FTA removal on tissue thickness (TT), zooxanthellae density (ZD), mitotic index (MI), and concentration of chlorophyll a (Chl a) in Montastraea annularis at the beginning and end of gametogenesis. Ramets (individual lobes within a colony) consistently surrounded by FTA and ramets surrounded by crustose coralline algae (CCA) were used as controls. FTA removal reduced coral stress, indicated by increased TT and ZD and lower MI. The measured effects were similar in magnitude for the short and long periods of algal removal. Ramets were more stressed at the end of gametogenesis compared with the beginning, with lower ZD and Chl a cm(-2), and higher MI. However, it was not possible to distinguish the stress caused by the presence of FTA from that caused by seasonal changes in seawater temperature. Ramets surrounded by CCA showed less stress in comparison with ramets surrounded by FTA: with higher TT, Chl a cm(-2) and ZD, and lower MI values. Coral responses indicated that ramets with FTA suffered the most deleterious effects and contrasted with those measured in ramets surrounded by CCA. According to published studies and our observations, there could be at least six mechanisms associated to FTA in the stress caused to M. annularis by FTA. Owing to the high cover of FTA (in contrast to macroalgae and CCA) in the Caribbean, the chronic stress, the overgrowth and mortality that this functional algal group can cause on M. annularis species complex, a further decline of this important reef-building coral in the Caribbean is expected

The effect of filamentous turf algal removal on the development of gametes of the coral Orbicella annularis.

Macroalgae and filamentous turf algae (FTA) are abundant on degraded coral reefs, and the reproductive responses of corals may indicate sub-lethal stress under these conditions. The percentage of gametogenic stages (PGS) and the maximum diameter of eggs (MDE; or egg size) of Orbicella annularis were used to evaluate the effect of long- (7-10 months) and short-term (2.5 months) FTA removal (treatments T1 and T2, respectively) at both the beginning (May) and the end (August) of gametogenesis. Ramets (individual lobes of a colony) surrounded by FTA (T3) or crustose coralline algae (CCA; T4) were used as controls. The removal of FTA enhanced the development of gametes (i.e., a larger and higher percentage of mature gametes (PMG)) of O. annularis for T1 vs. T3 ramets in May and T1 and T2 vs. T3 ramets in August. Similar values of PGS and MDE between gametes from T3 and T4 in both May and August were unexpected because a previous study had shown that the same ramets of T4 (with higher tissue thickness, chlorophyll a cm-2 and zooxanthellae density and lower mitotic index values) were less stressed than ramets of T3. Evaluating coral stress through reproduction can reveal more sensitive responses than other biological parameters; within reproductive metrics, PGS can be a better stress indicator than egg size. The presence of turf algae strongly impacted the development of gametes and egg size (e.g., PMG in ramets with FTA removal increased almost twofold in comparison with ramets surrounded by FTA in August), most likely exerting negative chronic effects in the long run due to the ubiquity and permanence of turf algae in the Caribbean. These algae can be considered a stressor that affects coral sexual reproduction. Although the effects of turf algae on O. annularis are apparently less severe than those of other stressors, the future of this species is uncertain because of the combined impacts of these effects, the decline of O. annularis populations and the almost complete lack of recruitment

Graphic representation of the ramets used in the four treatments.

<p>Treatments included <i>Montastraea annularis</i> ramets with monthly/fortnightly removal of filamentous turf algae (FTA) surrounding the coral tissue (FTA removal), ramets with FTA in contact with the coral tissue (FTA presence), and ramets with crustose coralline algae (CCA) in contact with the coral tissue (CCA presence). Ramets were collected in May 2010 and August 2010 (arrows) at the beginning and the end of the <i>M. annularis</i> gametogenesis cycle. Treatments: T1M and T1A = long-term treatment of FTA removal over 7 and 10 months, respectively; T2M and T2A = short-term treatment of FTA removal over 2.5 months in May 2010 and August 2010, respectively; T3M and T3A = control ramets in constant contact with FTA; and T4M and T4A = control ramets in constant contact with CCA. n = 7 collected ramets per date per treatment.</p

Experimental design used for <i>Orbicella annularis</i> ramets, with four treatments.

<p>The experiment included <i>O</i>. <i>annularis</i> ramets with filamentous turf algae removal from their periphery (FTA removal), ramets surrounded by FTA (FTA presence), and ramets with coralline crustose algae surrounding coral tissue (CCA presence). Experimental ramets were collected in May and August 2010 (arrows) to evaluate the development of gametes at the beginning (first four rows of treatments) and the end (last four rows of treatments) of <i>O</i>. <i>annularis</i> gametogenesis, respectively. Treatments: T1 = ramets with long-term FTA removal during 7 and 10 months before the beginning (T1M) and the end (T1A) of gametogenesis, respectively; T2 = ramets with short-term FTA removal during 2.5 months before the beginning (T2M) and the end (T2A) of gametogenesis; T3 = control ramets in permanent contact with FTA (T3M and T3A); and T4 = control ramets permanently surrounded by CCA (T4M and T4A).</p

<i>Orbicella annularis</i> gametogenesis.

<p>A) Stage I oocyte located between the mesoglea (m) and the gastrodermis (g); B) Stage II oocyte; C) Stage IV oocyte (next to a Stage III spermary); D) Stage V oocyte with nucleus (N) and nucleolus (red small circle) in its periphery; E) Stage III spermary with spermatocytes surrounding its periphery; and F) Stage IV spermary with spermatocytes homogeneously distributed. Microphotographs: NP Cetz-Navarro. Scales: A = 10 μm; B = 20 μm; C = 75 μm; D and E = 50 μm; F = 25 μm.</p

Reclutamiento del coral Acropora palmata sobre sustratos de dos materiales

During recruitment of corals, substrate characteristics influence the density and the spatial distribution of recruits. The influence of the material (limestone and sand) and of 4 groups arrangements (limestone/up, limestone/down, sand/up and sand/down) in the distribution of the Acropora palmata recruits in 4 areas of the substrate used (upper face, side faces, bottom faces and base) was evaluated. The number of recruits per substrate was higher in limestone (median= 15.0) than in sand (2.0). Regarding the areas of recruitment, the upper face in limestone and the upper and side faces in sand presented greater number of recruits than the other areas of the substrate; notably the upper faces received more light during the conditioning of the substrates. Concerning the groups, the number of recruits per substrate was higher in limestone groups (limestone/up ≈ limestone/down) than in sand groups (sand/up > sand/down). The relatively low number of A. palmata recruits obtained (12500 m-2) was, however, 3-4 orders of magnitude higher than the recruits obtained in Caribbean coral reefs (3-39 m-2), with an abundance dominated by opportunistic corals that do not provide the ecological qualities fulfilled by A. palmata. The implantation in the field of recruits obtained in aquarium remains as a viable alternative to recover populations of this critically endangered coral species, which substantially contributes to the structural complexity of Caribbean coral reefs.Durante el reclutamiento de los corales, las características de los sustratos influyen en la densidad y la distribución espacial de los reclutas. Se evaluó la influencia del material (conchuela y arena) y de 4 combinaciones denominadas grupos (conchuela/arriba, conchuela/abajo, arena/arriba y arena/abajo) en la distribución de los reclutas del coral Acropora palmata en las 4 áreas de los sustratos utilizados (cara superior, caras laterales, caras inferiores y base). En los materiales utilizados, el número de reclutas por sustrato fue mayor en la conchuela (mediana= 15,0) que en la arena (2,0). En las áreas del sustrato, la cara superior en la conchuela y las caras superior y laterales en la arena tuvieron mayor número de reclutas que las otras áreas del sustrato; cabe señalar que las caras superiores fueron las que recibieron más luz durante el acondicionamiento de los sustratos. En los grupos, el número de reclutas por sustrato fue mayor en los grupos de conchuela (conchuela/arriba ≈ conchuela/abajo) que en los de arena (arena/arriba > arena/abajo). El relativo bajo número de reclutas de A. palmata que se obtuvo (12500 m-2) fue, sin embargo, 3-4 órdenes de magnitud mayor que la obtenida en arrecifes del Caribe (3-39 m-2), con una abundancia dominada por corales oportunistas que no proveen las cualidades ecológicas de A. palmata. La siembra en el campo de reclutas obtenidos en acuario permanece como una alternativa viable para recuperar las poblaciones de esta especie en peligro crítico de extinción, la cual contribuye sustancialmente en la complejidad estructural de arrecifes coralinos del Caribe

Mean percentage values of gamete stages of <i>Orbicella annularis</i> during gametogenesis.

<p>A) Gamete stages found in May, the beginning of gametogenesis: Stage I oocytes (SI o) + Stage II oocytes (SII o) = 100%, and B) gamete stages found in August, the end of gametogenesis: Stage IV oocytes (SIV o) + Stage V oocytes (SV o) + Stage III spermaries (SIII s) + Stage IV spermaries (SIV s) = 100%. Treatments: T1) ramets with long-term removal of FTA, T2) ramets with short-term removal of FTA, T3) control ramets always surrounded by FTA, and T4) control ramets always surrounded by CCA. Lower-case letters (a-b for May, and a-b and c-d for August) above pair of bars indicate treatments that were significantly different (P ≤ 0.005). n = 7 collected ramets per treatment on each date.</p

Two-way analyses of variance evaluating the effects of sampling date and experimental treatment on biological parameters of <i>Montastraea annularis</i> ramets.

<p>ns = not significant. Treatments are described in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0054810#pone-0054810-g002" target="_blank">Figure 2</a>.</p

<i>Montastraea annularis</i> with and without surrounding algae, and algal mat without sediment.

<p>A) <i>M. annularis</i> ramet bordered by filamentous turf algae, B) <i>M. annularis</i> ramets bordered by crustose coralline algae, C) <i>M. annularis</i> ramet following the removal of filamentous turf algae, D) <i>M. annularis</i> ramet surrounded by filamentous turf algae with sediment trapped in the algal mat, E) ramet from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0054810#pone-0054810-g001" target="_blank">Figure 1D</a> following the removal of sediment from the algal mat using pressured air, and F) magnified view of the periphery of <i>M. annularis</i> being overgrown by filamentous turf algae through projections of prostrated axes. Photo credits: A–E by H Bahena-Basave and F by J Espinoza-Avalos.</p