The short-term aggressive behavior of scleractinian corals from La Blanquilla Reef, Veracruz Reef System, Gulf of Mexico was determined. Unilateral aggression, bilateral aggression and indifference were observed through experimental interspecific encounters in situ, in aquarium conditions and through direct observation of natural encounters on the reef. Species were characterized as highly aggressive, moderately aggressive and not very aggressive establishing a hierarchy with two competitive rings representing similar aggressive abilities among some species. Most observations of aggression were of extracoelenteric digestion. Mussa angulosa was the most aggressive species and Oculina diffusa the least. Apparently there is a direct relationship among aggressiveness and relative coverage as three of the most abundant corals at dephts of  4-9 m Montastraea cavernosa, Colpophyllia natans and Montastraea annularis, are all highly aggressive, have massive growth and have a high relative coverage. Siderastrea siderea is the only dominant species that was not ranked as highly aggressive; its high coverage is due to other reasons. ]]> Key words:  Scleractinian, coral, aggression, behavior, Veracruz.
 
 
The available space in a coral reef is a limited resource (Bak 1975, Connell, 1976). As a result, the scleractinian corals have developed diverse mechanisms that allow them to gain and maintain the space that they occupy (Lang and Chornesky 1990). Corals may directly cause tissue damage in some neighboring organisms and possibly cause their death, mainly through aggression (Porter 1974, Lang and Chornesky 1990, Genin et al.  1994). Aggression is carried out by means of specialized structures called sweeper tentacles (Den Hartog 1977, Richardson et al.  1979, Wellington 1980, Chornesky 1983, Ates 1989), or through extracoelenteric digestion, using the mesenteric filaments of the gastrovascular cavity (Lang 1970, 1973, Logan 1984, Sheppard 1979, Cope 1981, Yamazato and Yeemin 1986). Field studies have been carried out in scleractinian corals, facing species against each other, to determine which species are more aggressive and therefore dominant (Lang 1970, 1973, Logan 1984, Sheppard 1979, Cope 1981, Yamazato and Yeemin 1986). These studies have allowed researchers to classify and to rank coral species as highly aggressive, moderately aggressive and not very aggressive. Complex and not always linear patterns of aggressive dominance have been established (Logan 1984). Active aggression by scleractinian corals contributes to the determination of reef coral community structure (Lang 1970, 1973; Sheppard 1980a, b, Bak et al.  1982, Lang and Chornesky 1990). Additionally some experiments in ahermatypic corals have demonstrated that a competitive dominant may influence the abundance and population structure of a subordinate by reducing its sexual reproductive output, increasing larval mortality and altering recruitment patterns (Chadwick 1991). Aggressive behavior has also been used as a taxonomic character to differentiate species of the same genus, as in Scolymia (Lang 1971), Acropora (Potts 1978) and Montastraea (Weil and Knowlton 1994).

Like other attributes (e.g. color, shape) the patterns of aggressive behavior can slightly vary for the same species in different localities. Lang (1971, 1973) proposed a linear hierarchy in the extra-coelenteric digestive dominance pattern of corals from Jamaica, while Logan (1984) found that there might not be a clear dominance among some species. These results suggest regional differences that should be assessed. The objective of the present study was to determine the pattern of short-term of aggressive dominance in scleractinian corals from La Blanquilla reef, Veracruz Reef System (VRS), based on observations of corals in aquarium conditions and in the field. The VRS is located at the western limit of the coral reef distribution in the Atlantic (Horta-Puga et al.  1997), which confers to it particular characteristics that make it different from the other reef areas previously studied in the Caribbean biogeographic area.
 
Materials and methods
 
The study was carried out between February 1987 and August 1988, on the Blanquilla reef (19° 13´ 35” N, 96° 05´ 54” W) in the VRS. The experimental design consisted of establishing interspecific encounters, in situ and in aquarium conditions, as much as possible, between each of the readily-available scleractinian species. Experimental pairs were formed by tying two colonies of different species together with plastic wire, in such a way that the living tissue of each coral were in direct contact. Care was take in order to not damage the soft tissues while tying corals each other. We replicated, when possible, each experimental pair at least once. After a variable lapse of time, we recorded the results of the interaction in each pair as:  (1) unilateral aggression, when just one species showed signs of tissue necrosis, having a dominant (winner) and a subordinate species, (2) bilateral aggression, when both organisms presented significant damage in the contact area, implying that both species were aggressive, but neither dominated, and (3) indifference, determined when no specimen showed tissue damage, also indicating that neither was dominant. Our results for the Montastraea annularis complex (Weil and Knowlton 1994) were recorded without any distinction among the species involved, for obviously reasons.

Experimental determination of aggression under aquarium conditions:  To carry out this part of the study, we manually gathered numerous healthy colonies, 10 cm apart from other corals,  and with a diameter of >7 cm in the  N, S and W slopes of the reef at depths of 4-10 m. We placed the colonies in polyethylene bags with sea water from the collection site, stirring the water occasionally and avoiding direct sunlight. The corals were  taken to the lab in mainland within 30 min of  collection, where they were placed in 40 l glass aquariums, each with a continuous flow of recirculated water, obtained from reef. The aquariums were located outdoors, indirectly exposed to the sun. The following day after collection, we formed experimental pairs, always keeping one colony of each species alone as control in order to detect if the aquarium environmental conditions were not the cause of tissue damage. In order to determine the behavior pattern of each species every 3 hours we checked the schedule of activity and the mechanism being used for aggression, if any, during a period of up to 192 hrs. According to Lang (1970) this is enough time to determine the extracoelenteric digestion responses of corals. ]]> Experimental determination of the aggression on the reef:  The field study was carried out at 4-9 m on the same N, E and W slopes of La Blanquilla reef. We collected numerous specimens and tied them underwater, forming experimental pairs, that were positioned as close as possible to the places at which they have been collected. We checked each of the 300 experimental pairs after 192 hrs to look for signs of aggressive behavior. As experimental controls, we placed healthy colonies in the same area, to verify that transplantion was not the reason for any observed responses.

Natural interactions observed in the reef:  During the numerous dives carried out to collect the specimens for the study, we made direct observations of the natural interactions among corals in the reef. Each interaction was carefully observed and data such as:  participating species and type of interaction were recorded.

Results

Aggressive behavior under aquarium conditions:  We obtained results for 345 experimental pairs that implied interactions among 16 species, of which 280 gave conclusive results (Fig. 1). In the remaining pairs the corals died during the course of the experiment. Extracoelenteric digestion by the extrusion of the mesenteric filaments was the only observed mechanism used by the dominant colony to attack the subordinate species, causing tissue necrosis to the latter. In Agaricia agaricites, A. lamarcki, Leptoseris cucullata and Oculina diffusa, we did not see mesenteric filaments, even when they were dominant in different interspecific encounters. Chornesky (1983) recorded sweeper tentacles in Agaricia, but they were not observed here, possibly due to the fact that they only develop after several weeks of tissue contact. However, the damage inflicted by these species on the subordinate species was similar to  that of the filament extruding species. Bak et al.  (1982) reported that in Agaricia agaricites the filaments are very small and their observation is only possible under a microscope. Almost all the species extruded their mesenteric filaments during the night, generally 6-9 hrs after the beginning of the contact. Montastraea cavernosa and Colpophyllia natans were the only ones that extruded their filaments during the day. We observed three or four extruded filaments per polyp in most of the aggressive colonies. However, in some colonies of Montastraea cavernosa, there were as many as approximately 30 extruded filaments per polyp. The time for the manifestation of a clear aggressive dominance was variable for each species. Thus, while Montastraea cavernosa was dominant over Stephanocoenia intersepta in 24 hrs, Colpophyllia natans took up to 120 hrs to dominate this same species.
 

Aggressive behavior in field conditions:  Conclusive results were obtained in 219 of  300 experimental pairs in the field (Fig. 1). Acropora cervicornis, A. palmata and Siderastrea radians were included in these studies. Some experimental pairs were separated by the action of surf, currents or fishes or other reef organisms. Contrary to our results for the aquarium conditions, it was not always possible to observe the aggression mechanism(s) used by every species. The resulting classification as highly aggressive, moderately aggressive and not very aggressive species is similar to that determined under aquarium conditions. There are slight differences on the arrangement of species within the “competitive rings” (Fig. 4). Acropora cervicornis, A. palmata and Siderastrea radians, although they are not show in the hierarchy, were considered not very aggressive since they were subordinate to the highly aggressive species, although due to the small number of experimental pairs for these species, it is not possible to draw conclusive results about their behavior.

Records of natural interactions:  We recorded 88 natural interactions among corals of 11 different species in La Blanquilla reef (Fig. 2). We only observed two interaction types, unilateral aggression or indifference. The hierarchy of natural aggresssive dominance using these observations (Fig. 5) closely resembles those obtained experimentally.

There were no important differences among the dominance patterns found in this study, and those previously noted in Jamaica (Lang 1970, 1973) and Bermuda (Logan 1984), and the more recent study in Curacao (Van Veghel et al.  1996), where the scleractinian fauna is similar. Lang (1973) ranked M. cavernosa lower in the hierarchy than Diploria spp. and M. annularis, and Logan (1984) ranked this sames species higher. This can be considered an evidence for our suggestion of the existence of a group of higher rank of similar aggressive capacities, in addition of that proposed for the weakly-aggressive species. Unfortunately, the absence of some species for each studied geographic area, could not permit a thorough comparison of the hierarchies. The small differences in the aggressive capacity registered for each species in each area, could be explained by:  (1) the state of health of the used colonies, (2) physical, chemical, seasonal and/or geographical variations as was suggested by Logan (1984, 1986), and (3) the use of more than one mechanisms of aggression (Lang and Chornesky 1990). ]]> The coral community structure in the reef slopes of La Blanquilla reef is well known (Bravo et al.  1989). The most abundant species on the reef slopes between 4-9 m depth in order of importance are:  Montastraea cavernosa (28%), Colpophyllia natans (20%), Siderastrea siderea (20%) and Montastraea annularis (13%). Each of this species, except Siderastrea siderea, is characterized as highly aggressive. The aggressive character of these species could explain in part their high coverage in the reef, as was pointed out for Montastraea annularis complex by Van Veghel et al.  (1996). All are also massive colonies that grow slower than ramose and leafy colonies, like Acropora and Agaricia respectivelly. Our results constitute an additional evidence that some corals use aggressive behavior to compete against the fast-growing species and each other, in order to gain and maintain the space in the reef (Lang 1970, 1973, Sheppard 1980a, b, Bak et al.  1982, Genin et al.  1994).

In the case of  Siderastrea siderea, its high bottom coverage could be explained by its high reproductive potential (Szmant 1986) and its capacity to adapt to variable environmental conditions (Bak and Elgershuizen 1976, Loya, 1976). Mussa angulosa constitutes an exceptional case, although it is the most aggressive coral species, it is not abundant in La Blanquilla reef (relative coverage <<1%), thus, its aggressive capacity either play a secondary role in the determination of its coverage and/or distribution,and due that grows and reproduces slowly, without its high digestive dominance and ability to tolerate some shade, it might no longer exist at all.

The VRS is a marginal reef environment, that has lower faunal diversity (e.g. corals, fish, annelids, mollusks) than other Caribbean reef areas, indicating an impoverished ecosystem that has developed at the limit of tolerable environmental conditions possibly mediated by low winter temperatures and high sedimentation rates (Gutiérrez et al.  1993, Carricart-Ganivet and Horta-Puga 1993, Vargas-Hernández et al.  1993). These reefs have also been imperiled for centuries, from the arrival of the Spaniards at the beginning of the 16th century, to the present. The anthropogenic impacts on these reefs include chemical pollution, over-fishing, accidental oil spills, unrestricted tourism, ship groundings, discharges of sewage effluents, dredging, boat anchoring, and the extraction of coral for building purposes (Horta-Puga et al.  1997). In spite of this severe environmental framework for the VRS, the coral species exhibit the same aggressive capacities as in other reef areas of the Western Atlantic.
 
Acknowledgments

Many thanks to Judy Lang for her thoroughly review and her suggestions that notably improved the manuscript. We also thank Leonardo Alcantar, Juan Pablo Carricart, Ricardo Saenz, Joel Reyes, Jaime Camacho, Juan Bravo, Hugo Castro and Miguel Fuentes for their help in the experimental design and sampling. Thanks to Guillermina Sedas for her support during the field work.
 
Resumen
 
Se determinó el comportamiento agresivo a corto plazo de los corales escleractinios del arrecife La Blanquilla, Sistema Arrecifal Veracruzano, en el Golfo de México por medio de pares experimentales interespecíficos en condiciones de acuario y campo, así como de la observación directa de encuentros interespecíficos naturales. Las especies de coral fueron caracterizadas como altamente agresivas, moderadamente agresivas y no muy agresivas, estableciéndose una jerarquía en la que se incluyen dos anillos competitivos en los cuales las especies tienen una capacidad agresiva similar. La digestión extracelentérica fue el mecanismo de agresión más frecuentemente observado. La especie más agresiva fue Mussa angulosa y la menos agresiva Oculina diffusa. Aparentemente existe una relación directa entre la capacidad agresiva y la cobertura relativa de las tres especies más abundantes a profundidades entre 4-9 m Montastraea cavernosa, Colpophyllia natans y M. annularis, ya que todas fueron clasificadas como altamente agresivas, tienen un crecimiento masivo y una cobertura relativa alta. Siderastrea siderea es la única especie dominante que no fue clasificada como altamente agresiva, por lo que su cobertura alta es debida a otros factores. ]]>  
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1 Pronatura Península de Yucatán, A.C. Calle No. 1-D 254-A. Col. Campestre. Mérida, Yucatán 97120, México; ppy@pibil.finred.com.mx

2 INVEMAR, UBIPRO, ENEP Iztacala, Universidad Nacional Autónoma de México. Av. de los Barrios s/n, Los Reyes Iztacala, Tlalnepantla, México 54090. Fax:  +(52) 56231225; horta@servidor.unam.mx ]]> 1989 12 181-190 1975 45 181-190 1976 69 215-222 1982 69 215-222 1989 México, D.F México, D.F 1993 1976 1981 Manila 357-362 1991 70 39-48 1983 165 569-581 1977 Miami Florida 463-469 1994 39 913-924 1993 1997 México D.F México D.F 015 1970 80 1971 21 952-959 1973 23 260-279 1990 25 1984 3 131-138 1986 32 347-351 1976 26 450-466 1974 18 6 543-545 1978 220 55-74 1979 55 181-186 1979 1 237-247 1980 6 57-60 1980 6 57-60 1986 5 43-54 1992 1996 58 792-803 1993 1994 55 ^s151-175 ^s151-175 151-175 1980 65 516-525 1986 5 163-174