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

Abstract

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.

Fig 1. Experimental design used for Orbicella annularis ramets, with four treatments.

The experiment included O. annularis 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 O. annularis 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).

Fig 2. Orbicella annularis gametogenesis.

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.

Fig 3. Mean percentage values of gamete stages of Orbicella annularis during gametogenesis.

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.

Fig 4. Mean values ± SD of the maximum diameter of eggs of Orbicella annularis during gametogenesis.

A) Egg size at the beginning (May) of gametogenesis, and B) egg size at the end (August) of gametogenesis. 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) above pair of bars indicate treatments that were significantly different (P = 0.000). n = 7 collected ramets per treatment on each date.