Coral Reefs (2004) 23: 578–583 DOI 10.1007/s00338-004-0419-5
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J. A. Sa´nchez Æ Maria F. Gil Æ Luis H. Chasqui Elvira M. Alvarado
Grazing dynamics on a Caribbean reef-building coral
Received: 21 February 2003 / Accepted: 12 July 2004 / Published online: 9 September 2004 Springer-Verlag 2004
Abstract Corals in certain Caribbean coral reef habitats are constantly grazed-on due to the territorial marking behavior of the stoplight parrotfish Sparisoma viride. We studied the grazing dynamics on the Caribbean reefbuilding coral Montastraea annularis. We transplanted colonies to algae-dominated reefs (Rosario Islands, Cartagena, Colombia), where they encountered higher grazing pressure. We counted grazed polyps every month throughout a year. Over the course of a year, 4,101 different grazed polyps were counted on lobe-like M. annularis transplants (n =23). Grazing was evaluated on a monthly basis as the probabilities of all the possible transitions among four grazing categories (0%, >0–1%, >1–5%, >5% grazed tissue), uncovering a dynamic process. Higher transition probabilities were always between 0 and 1% (coral tissue grazed) grazing states, indicating that grazing did not usually exceed 1% per coral per month. The probability of remaining uninjured in a month was 0.19, 0.17 of a change from 0–1% grazing state, 0.31 of remaining at 1%, and of full recovery from 1% grazing was 0.16. More than one month was usually required for complete recovery (P 1) probably due to both steady grazing pressure and slow regeneration rates. Since the marking behavior of the parrotfish was not as common on other zones of the reef no comparison on the grazing among environments was possible. In spite of this, it is possible to have stable transplanted populations of corals such as M. annularis on algae-dominated Caribbean reef environments due to their tolerance to the natural grazing pressure. Communicated by: K. S. Sealey J. A. Sa´nchez (&) Æ M. F. Gil Æ L. H. Chasqui Æ E. M. Alvarado Centro de Investigaciones Cientı´ ficas (Museo del Mar), Universidad de Bogota´ Jorge Tadeo Lozano, Calle 22-3-30 Bogota´, Colombia E-mail:
[email protected] Present address: J. A. Sa´nchez Departamento de Biologı´ a, Universidad de los Andes, PO Box 4976, Carrera 1E-18A-10 Bogota´, Colombia
Keywords Grazing Æ Montastraea annularis Æ Reef-building coral Æ Regeneration
Introduction A fundamental question in the study of colonial organisms is how the modular, repetitive units are functioning in response to environmental challenges (e.g., Huang and Robinson 1992). Modules of sessile invertebrate colonies such as reef-building corals (Scleractinia: Cnidaria) have a high degree of colony integration because the polyps (modules) are physically connected, and thereby share physiological functions (e.g., Cartwright et al. 1999). This integration contributes to the way in which many physiological functions are dealt with, particularly regeneration and growth (Rinkevich 1996; Oren et al. 2001), both of which are functions of module replication (Hughes 1983, 1989). This is of great relevance to the colony fitness, because survivorship and fecundity increase with size (see review in Hughes et al. 1992). Nonetheless, environmental cues such as grazing constantly affect the organism’s growth and shape (Karlson et al. 1996; Grunbaum 1997). Therefore, growth and regeneration is a highly dynamic process where colonies do not only respond by following a developmental program but by adapting to their changing external (e.g., grazing: Lasker 1985) and internal environments (e.g., branching self-organization: Sa´nchez et al. 2004; colony development: Cartwright et al. 1999). However, there is little documentation on the dynamics of processes such as grazing and regeneration through time or evaluating natural scenarios of grazing on reef-building corals. Algae-dominated coral reef habitats in the Caribbean Sea provide a good scenario to examine grazing on reefbuilding corals. A synergism between the die-off of the sea urchin Diadema antillarum and nutrient enrichment, along with increases in global sea surface temperatures and coral reef diseases seems to be causing adverse
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effects on Caribbean coral populations (e.g., Hughes 1994). Seaweed dominated areas such as the extensive dead Acropora cervicornis stands in the Caribbean (e.g., Knowlton et al. 1990; Sa´nchez 1995) provide excellent scenarios to study grazing effects on corals. For instance, although the stoplight parrot fish Sparisoma viride does not properly feed on living corals (e.g., Lewis 1986), it creates conspicuous ‘‘white spots’’ on coral colonies, especially Montastraea annularis (Ellis and Solander) located near territory boundaries (e.g., Bruggemann et al. 1994; Van Rooij et al. 1995). Males of S. viride, in deeper parts of the reef (>3.5 m), actively defend territories due to their haremic behavior and/or an increase in the availability of resources (Bruggemann et al. 1994). We observed that dead Acropora cervicornis stands in a Colombian coral reef where colonies were studied, comprise a habitat where the few reef-building corals still present in this habitat were continually stressed due to use as territorial markers (e.g., Fig. 1). Using this opportunity we transplanted colonies of the Caribbean
Fig. 1 Colonies of Montastraea annularis at Isla Grande, Rosario archipelago, Colombia. A Transplanted colony the day of transplant (February 1997). B Large M. annularis genet showing several ramets. C Colony with recent grazing bites. D Colony with a grazed area colonized by filamentous algae. E – F Colonies showing numerous regenerating polyps and nearly closed algae colonized injuries
dominant species Montastraea annularis of similar characteristics and followed the natural grazing dynamics on a monthly basis. The study described and estimated the natural dynamic process of grazing and survivorship using a population approach. We developed a stagestructured model to predict the fate at varied degrees of natural grazing on transplanted colonies.
Methods The study system, Montastraea annularis (Ellis and Solander) is currently one of the most important and abundant reef-building corals of the Caribbean region (Fig. 1). This species has been validated as separate species from the M. annularis complex (Weil and Knowlton 1994), although some authors have questioned the separation. They consider it as part of a larger polymorphic species complex (Van Veghel and Bak
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1993; Van Veghel 1994) together with M. faveolata (Ellis and Solander) and M. franksi (Gregory). Nevertheless, differences among these species have included several life history characteristics (see review in Szmant et al. 1997). For example, colony architecture and size frequency distributions are different among these species. While M. faveolata and M. franksi produce mostly massive or plate-like colonies with few asexual ramet colonies, M. annularis grows producing hundreds of asexual ramets connected from a base in a tree-like structure (Lasker and Sa´nchez 2002). This suggests that profound differences may govern the module replication, and response to partial mortality, among the M. annularis complex. In fact, differences in regeneration efficacy (or injury recovery) have been observed among the three species (e.g., Weil and Knowlton 1994). Therefore, we decided to study M. annularis sensu stricto to avoid confounding variation within the species complex. Additionally, this coral has the technical advantage of having small (10–30 cm in diameter), discrete ramet colonies of hemispheric shapes as well as discrete modules (polyps) of medium size (11 polyps cm–2), which are identifiable even after grazing. Thus, M. annularis colonies can be accurately measured and polyps easily counted, providing an ideal system to examine regeneration dynamics. The particular scars we assessed on coral transplants (e.g. Fig. 1) were congruent with the scars made by Sparisoma viride (5.8±0.174: Brueggemann et al. 1994) although larger injures were also observed due to cumulative grazing. Individuals of S. viride were also observed throughout the area of the transplant experiment year-wide. The study of grazing dynamics in Montastraea annularis, was carried out at the Isla Grande coral reef, Rosario Islands off the Caribbean coast of Colombia (see area description in Sa´nchez et al. 1999). We chose to observe transplants in order to have similar colonies as opposed to the diverse size ranges of the few colonies still present in the dead Acropora cervinornis habitat. In addition, colonies from the Montastraea spp. area were usually less stressed as territorial markings than in the A. cevirconis zone. Colonies chosen for transplantation were harvested from El Varadero (22 km NE from Isla Grande off Cartagena Bay), a leeward reef with a forereef terrace comprised of mixed coral growth between 4 and 15 m in water depth. El Varadero Island, between Tierra Bomba and Baru islands, has dynamic surface waters, including constant runoff from Cartagena Bay (see also Sa´nchez 1999), which has freshwater effluents. As Cartagena Bay is being developed, coral reefs at El Varadero run the risk of disappearing due to dredging and sediment suffocation. Isla Grande (Rosario Islands) Reef, on the other hand, has been protected as part of a National Natural Park since 1978. The reef portion chosen for transplants is part of an 11-km fringing reef complex along Isla Grande. The area is windward on a sinuous fore-reef terrace (50–200 m width) with extensive dead Acropora palmata or A. cervicornis stands (see more details in Sa´nchez et al. 1999). A. cervicornis stands,
where transplants were relocated, were primarily covered with the fleshy algae Dictyota spp. and calcareous algae such as Halimeda spp. and Peyssionella spp. Despite the differences between Isla Grande and El Varadero, forereef terrace habitats below 10 m are very similar in terms of community structure (unpublished data). Transplanted corals were transported by boat for no more than two hours and were kept under shade in plastic trays and regularly sprayed with seawater. Transplants were settled down in four 20-m transects placed at 30, 50, 300, and 700 m apart and an average of 8, 11, 12, and 10 m in water depth, respectively, in order to capture the habitat heterogeneity. They were placed on degraded Acropora cervicornis stands (occasionally dead Agaricia tenuifolia and/or Porites furcata) colonized by algae. Colonies had at least a 10-cm conic base of old calcium carbonate, which was used to cement them. We used a construction-type cement mixed with sand (1:2) and a special additive for under-water conditions (ca. 1 L in 3 gal of blend, SIKATM), which attached corals to substrate in 2–4 h. Portions of dead coral structures were broken from necessity in some cases to create a bed for the transplants, but normal reef topography was conserved. The grazing on Montastraea annularis was studied on 23 transplanted colonies (15–30 cm in diameter) of the typical hemispheric form of M. annularis that were lacking injuries, recent grazing, and/or deformations (e.g., Fig. 1 B). This facilitated area estimations. Every month for 13 months the number of grazed polyps and dead calyces (often algae colonized) were counted for each colony. Grazing was analyzed on a monthly basis according to the percentage of net grazing effects (e.g., recently grazed plus old dead tissue from previous grazing) tissue per colony in four categories (0%, >0–1%, >1–5%, >5%). The grazed and dead tissue categories per colony each month were estimated by counting the number of affected polyps that were converted to area—using a mean of 11.04 polyps cm–2, ±2.15 SD, n =33 different central ramets (4·4 cm sampled in each colony), 95% of confidence interval = 0.76—and finally transformed in percentage respect to the initial colony area. The initial area was calculated as half of an oblate ellipsoid. Given a as the maximum radius and b the minimum (measured underwater, February 1997), we estimated coral area (Ac) with the following expression modified from Eshbach (1952): pb2 1þe ð1Þ ln 2Ac ¼ 2pa2 þ 1e e when pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi a2 b2 e¼ : a
ð2Þ
The raw data consisted of a record of 13 monthly estimates per colony. In the initial month, all the colonies were in the 0% category. The grazing state per
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colony was then transformed as the number of colonies per each of the possible transitions among the four categories (e.g., number of cases when a colony with 0% changed to 0%, 0 to >0–1%, >0–1% to >0–1%, >0– 1% to 0, >0–1% to >1–5%, ..., >5–>5%). Then, we calculated transition frequencies accumulated during the 12 months presenting transitions with respect to the total number of transitions in all states during the same period (23 colonies per 12 months, n =276), which is also the percentage and the probability of the particular transition. For instance, if there were colonies with transitions from 0 to >0–1% 46 times, that particular transition (0 to >0–1%) had a probability of 0.16. Using the transition probabilities, we assembled an empiric grazing category-structured model predicting the most likely fate for a transplanted colony for the oncoming month if starting from 0%, >0–1%, >1–5%, or >5% and all the possible transitions among those categories as it is usually presented in stage-structured population models (e.g., Caswell, 1989). This model is also a rough descriptor of the regeneration capability of the species because it indicates the probabilities for full recovery from particular percentages of grazed tissue or if it is not possible in just a month. For example, if the probability of fully recovering from >5% to 0 in a month is less than 0 (e.g., not presented in the model) but from >5% to >0–1% is 0.1 and from >0–1% to 0 is 0.2, it is possible that a colony at >5% category might recover completely after 2 months because there is some chance (0.1) to move to state >0–1% after 1 month and an even higher chance (0.2) from >0–1% to 0 in the following month. Nonetheless, the fate of a colony greatly depends on the random event of grazing per se and it is important to understand the model as merely probabilistic.
Results Grazed polyps on Montastraea annularis were easily distinguished from those remaining due to loss of tissue and calcium carbonate and, usually, a bright white appearance or slightly darker coloration (Fig. 1 C). Algae colonized polyps when the grazing area was extensive (e.g., >5% Fig. 1 C and F), were also easily differentiated. Restored polyps were variable in appearance ranging from transparent to bleached polyps, perhaps due to lateral or inner regeneration of polyps (Fig. 1 E and F). It is important to note that bleaching was infrequent in these colonies during 1997 and 1998 (only one colony). Cases of ca. 250 polyps per injury were recorded as an estimated area of an ellipsoid or the geometric two-dimensional structure of the total injury. However, these cases were very unusual—6 in total, just one colony >15% of total colony area (80%). Transplanted corals were found grazed after the first month of observations (Fig. 2). A total of 4,101 different grazed polyps were counted over the 13 months (during the first month all the colonies were intact) on the 23
Fig. 2 Monthly variation in the percentage of colonies of Montastraea annularis per stage of grazed tissue (%) during March 1997 to March 1998 (t0 = February 1997)
reef-building coral transplants. During the first fourmonth period (March to June), including the very first months after transplant, grazing was highly variable (Fig. 2). Total number of grazed polyps during that period (2009) doubles the numbers recorded in the following periods (July to October = 1,119 and November to February, 973). After a year, the 23 transplanted colonies had between 9 and 963 grazed polyps y1 (mean SD 226.2±50.8). In terms of net grazing effects on colonies, the proportion of different stages of grazing varied considerably during the first half-year and stabilized in the second half (Fig. 2). Although every transplant accumulated grazing injures at the end of the year, nearly 50% of the colonies were completely recovered. Nevertheless, along the year of observation most of the colonies fluctuated from one stage of injury to another repeatedly, suggesting constant shifts in the marking behavior of the parrotfish. The most likely fate of transplanted reef-building colonies under grazing pressure due to marking behavior in an algae-dominated coral reef habitat is in Fig. 3 and represented as transition probabilities among the grazing categories. Higher transition probabilities were always between the 0 and 1% stages (Fig. 3), indicating that marks on corals by Sparisoma viride usually did not
Fig. 3 Loop diagram with transition probabilities of the Montastraea annularis monthly regeneration dynamic. Circles indicate the coral stage in terms of percent of grazed tissue per colony (0, >0–1%, >1–5%, >5%)
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exceed 1% of the total number of polyps per colony in a month. The highest probability (0.31) was to remain in the 1% grazing state. The probability of remaining uninjured (0) in a month was 0.19 and of full recovery from 1% grazing was 0.16. More than one month was usually required for complete recovery (P 1) and even more from higher grazing stages (e.g., 5 and >5% categories not linked with 0%; Fig. 3). A good portion of the grazed colonies had a great chance to remain in a regenerative dynamic, probably due to both cumulative grazing pressure and slow regeneration rates for higher categories.
Discussion The reef-building coral Montastraea annularis tolerated with minor net effects the grazing pressure from the marking behavior of the parrot fish Sparisoma viride in algae-dominated Caribbean reef environments. It can be inferred from the results that this species responded to partial mortality by actively restoring lost polyps and likely producing new ones. It was also clear that grazing and regeneration are highly dynamic processes, which can also be approached using tools such as stage transition models (see also Ruesink 1997). These tools can show the net effects at the population level whereas giving an idea of the individual colony response. Some of those transplanted corals were also observed spawning during the 1997 and 1998 reproductive seasons (Sa´nchez et al. 1999), suggesting maintenance of their fitness after transplantation. Regeneration of lost parts in reef-building corals, sometime as much as half of the colony, seems to be a physiological priority, as it has been observed in the Red Sea coral Stylopora pistillata (Loya 1976; Rinkevich and Loya 1985; Rinkevich 2002). The reef-building coral case resembles the tolerance to partial mortality observed in some species of plants that respond to mortality with vigorous regrowth and reproductive performance (e.g., Huhta et al. 2000). Similarly, in Caribbean gorgonian octocorals, it has been observed that after partial mortality the colonies exceed normal branching rates (Sa´nchez and Lasker 2004). Recovering from partial mortality is considered a fixed characteristic of modular growth (Hughes 1983) and with likely adaptive value (Meesters et al. 1996). Adverse environmental effects such as bleaching have shown to decrease the regenerating capability of Montastraea annularis (e.g., Mascarelli and BunkleyWilliams 1999). Since the marking behavior of the parrotfish was not as common on other zones of the reefs no comparison on the grazing among environments was possible. In spite of this, it is possible to have stable transplanted populations of corals such as M. annularis on algae-dominated Caribbean reef environments due to their tolerance to the natural grazing pressure. Several species of reef-building corals have been transplanted using a number of different techniques (e.g., Oren and Benayahu 1997; Van Treeck and Schu-
hmacher 1997; Yap et al. 1998). The positive outcome of those transplant experiments suggests that reef-building corals can resist drastic changes in the environment such as transplantation. Therefore, transplantation of reef-building corals may help to rehabilitate degraded algae-dominated reef areas and/or conserve endangered species (see review in Edwards and Clark 1998). This can maintain local diversity in places unsuitable for coral recruits to settle such as seaweed-dominated Acropora cervicornis stands. Transplantation of corals, from reefs that may be destroyed by development, to degraded coral areas in natural reserves, as in this study on dead A. cervicornis stands, may provide a worthwhile compensation in terms of conservation of coral genotypes at intervened reefs. Acknowledgments This work was funded by COLCIENCIAS (1202-09-221-96) and the Jorge Tadeo Lozano University. Special thanks to O. L. Arenas, H. Charry, C. Gomez (Ministerio del Medio Ambiente, Seccio´n de Parques Nacionales), C. Sareztki, N. Schonwald, M. Morelos ‘‘Man˜e’’, R. Garcia, Ecobuzos (Cartagena), and Sport Baru´ (Senzato family, Cie´naga de Cholo´n) for their help and collaboration in the field. Comments and discussion from A. R. Acosta-de-Sa´nchez, H.R. Lasker, H. Guzman, S. Santos, and two anonymous reviewers improved the paper. J.A. Sa´nchez acknowledges a Smithsonian Institution postdoctoral scholarship. Contribution No. 9 of ‘‘Centro the Investigaciones Cientı´ ficas’’, Jorge Tadeo Lozano University.
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