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Interspecific interactions among species of the coral genus Porites from Okinawa, Japan
Zoology 104 (2001): 91–97 © by Urban & Fischer Verlag http://www.urbanfischer.de/journals/zoology
Interspecific interactions among species of the coral genus Porites from Okinawa, Japan Baruch Rinkevich1 and Kazuhiko Sakai2 1
Minerva Center for Marine Invertebrate Immunology & Developmental Biology, National Institute of Oceanography, Israel Oceanographic & Limnological Research, Tel Shikmona, Haifa, Israel 2 Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, Sesoko, Motobu-cho, Okinawa 905-0227, Japan Received June 7, 2001. Accepted August 13, 2001
Summary Analysis of field established xenogeneic interactions among five Porites species from Sesoko Island, Okinawa, revealed a transitive type of hierarchy as: P. rus > P. cylindrica > P. lobata > P. australiensis > P. lutea. Out of the 111 interspecific encounters studied, in only 5.4% reciprocal interactions were recorded, and in a single case, the opposite directionality of hierarchy was documented. Allogeneic encounters were also observed. A single major effector mechanism, an overgrowth (together with secondary outcomes such as the formation of small points of rejection, bleaching and pink color formation along a narrow peripheral belt of contacting tissues), was the only response in all 10 xenogeneic and 5 allogeneic combinations. In some massive colonies, a long contacting line of up to 50 cm was established. No sign for allelopathy, stand-off or rejection from a distance (i.e., by sweeper tentacles, sweeper polyps) was observed. Results are discussed with the accumulated data on Porites species from different reefs, worldwide, confirming that this genus is commonly lower in the hierarchy of xenogeneic interactions. Key words: allorecognition, Cnidaria, effector mechanism, hierarchy, Japan
Introduction Interspecific competitive networks in sedentary colonial invertebrate assemblages are an important factor in the construction of communities and therefore have been studied in detail in several marine ecosystems, including coral reefs. Neighboring coral colonies which are in close proximity in nature may affect one another through a variety of competitive measures (reviewed in Lang and Chornesky, 1990). However, competitive outcomes are not always visible and even when they are visible, they may depend on both the combination of competing species and the environment (e.g., Cox, 1986; Chornesky, 1989). As a result, the outcomes for
competition were sometimes different when short vs. long-term in situ observations were compared or when laboratory vs. field results were evaluated (Bak et al., 1982; Logan, 1984; Nakaya, 1984; Chornesky, 1989; Romano, 1990). Some slower developing interspecific outcomes were also misinterpreted as “stand-offs” (Connell, 1976) where two coral colonies appeared to stop growing along a common margin, often without obvious damage to their soft tissues. Some followed up stand-offs lasted for at least nine years before one partner eventually overgrew the other (Connell and Keough, 1985). The genus Porites is a worldwide distributed and ecologically important coral taxon (Veron, 1986). Studies
1
Corresponding author: Baruch Rinkevich, Minerva Center for Marine Invertebrate Immunology & Developmental Biology, National Institute of Oceanography, Israel Oceanographic & Limnological Research, Tel Shikmona, P.O.Box 8030, Haifa 31080, Israel, phone: 972-4-8515202; fax: 972-4-8511911; e-mail: [email protected] 0944-2006/01/104/02-091 $ 15.00/0
B. Rinkevich and K .Sakai
were also engaged with interspecific interactions of Porites species against other coral species. These studies were performed in a variety of coral reefs including Enewetak atoll (Stimson, 1985), Chagos atoll (Sheppard, 1979), the Caribbean (Lang, 1973; Logan, 1984; Lang and Chornesky, 1990), the Great Barrier Reef, Australia (Bradbury and Young, 1982; Tanner, 1983), Taiwan (Dai, 1990), Hawaii (Hunter, 1985; Cox, 1986) the Gulf of Thailand (Yamazato and Yeemin, 1986), Gulf of Eilat, Red Sea (Genin and Karp, 1994; Abelson and Loya, 1999) and Okinawa, Japan (Nakaya, 1984). These studies revealed that the Porites species are either intermediate or subordinate (the lower order in ranking) in the competitive hierarchies. In most cases, Porites species were analysed against other coral species. In only a single case (Nakaya, 1984), the aggressive hierarchy between different Porites species was evaluated. The Ryukyu Islands (including Okinawa) possess one of the northernmost distributions of coral reefs (26–27 ºN). The well developed reefs in this area have deteriorated rapidly during the last two decades. About 15 years ago, 143 hermatypic species were still recorded in Sesoko Island, Okinawa, where the Sesoko Marine Station is located, including 11 Porites sp. (Sakai and Yamato, 1987). The rate of decrease in species richness, coral coverage and the number of species was further enhanced following the 1998 coralbleaching event (Loya et al., 2001). In this area, several species of Porites dominate the shallow reef (1–7 m depth) forming massive structures with large colonies that inter- and intraspecifically interact in situ for prolonged periods (Nakaya, 1984). This study reveals the interspecific hierarchy pattern of the five most common Porites species in front of the Sesoko Station.
Materials and methods Observations were conducted in situ by SCUBA diving at a depth of 1–7 m in front of the marine station at Sesoko Island. Five species of Porites are commonly found in this area: the hemispherical P. australiensis Vaughan 1918, P. lutea Edwards and Haime 1860, P. lobata Dana 1846; P. rus Forskäl 1775, with laminar or contorted anastomosing branches and column colonies, and the branching species P. cylindrica Dana 1846. In many cases, colonies of two or more of the above species grew near or attached to each other. We surveyed the area for all Porites vs. Porites interspecific (xenogeneic) interactions, and when applicable, also for intraspecific (allogeneic) encounters. This field study documented the interactions found in situ (June-August 2000; interactions between Porites species and other coral species were not studied) and did not involve long term followed up observations. Interactions between colonies of the above five species were documented underwater in detailed writing and by photography. Each colony was labeled with a plastic tag and in the case of the three hemispherical species (P. australiensis, P. lutea, P. lobata), colony samples were taken by hammer and chisel. Each sample, containing at least 50 polyps, was separately put into a marked plastic bag. Samples were taken to the laboratory and the tissues were removed by Clorox solution overnight. All samples were checked under a compound microscope to verify species identity. This thorough examination revealed few interactions of the above Porites species with two additional species, P. solida and P. okinawensis, which could not be identified as such in situ. We documented any outcome that was clear from visual inspections. Some interactions were carefully isolated
Table 1. Summary of interspecific interactions between five Porites species from Sesoko Island, Okinawa. Type of combination A vs. B
n
A wins (%)
B wins (%)
P. rus vs. P. cylindrica
16
100.0
0.0
0.0
P. rus vs. P. lobata P. rus vs. P. australiensis P. rus vs. P. lutea P. cylindrica vs. P. lobata
11 7 8 13
100.0 100.0 100.0 84.6
0.0 0.0 0.0 0.0
0.0 0.0 0.0 15.4
P. cylindrica vs. P. australiensis P. cylindrica vs. P. lutea P. lobata vs. P. australiensis
9 6 21
88.9 100.0 85.7
11.1 0.0 0.0
0.0 0.0 14.3
P. lobata vs. P. lutea P. australiensis vs. P. lutea
7 13
85.7 100.0
0.0 0.0
14.3 0.0
92
Reciprocal (%)
Major interactions Overgrowth, small and few necrotic areas, limited bleaching as above as above as above Points of rejections on recessive species tissues followed by overgrowth in areas of contact as above as above Wide front of overgrowth, small and few necrotic areas, limited bleaching bands along the frontiers, pink colors and in many cases, turf algae settlement as above as above Zoology 104 (2001) 2
Porites interspecific interactions
by chisel and hammer from the colonies, brought to the laboratory and inspected under a binocular stereomicroscope. There were cases in the field where no decision on the type of interaction could be made. These cases typically involved reciprocal interactions that were partially covered with encrusting organisms and algae that settled onto interacting zones. These cases were eliminated from the analysis to reduce artifacts and errors for hierarchy determination resulting from interactions with other organisms, or caused by environmental factors (partial predation, sedimentation effects, algae interference, etc.).
Results General hierarchy
The 5 Porites species formed 10 interspecific combinations, of which we observed a total of 111 interspecific encounters. The outcome of these interactions revealed a linear type of hierarchy, with Porites rus as the most dominant species and P. lutea at the bottom as the subordinate (Fig. 1, Table 1). The linear hierarchy was clearly evident although in 6 cases (5.4%), reciprocal interactions were recorded, and in a single case (0.9%), the opposite directionality of hierarchy was documented (Fig. 1, Table 1). P. cylindrica colonies were recorded in 4 cases encountering P. okinawensis colonies, with two winners for each partner species. Two cases of P. solida > P. lobata were also recorded. Many of the interactions detailed below are probably long-term encounters that developed through years of tissue-to-tissue contacts reducing the variations recorded during short-term observations (i.e., Chornesky, 1989).
tions between the other four species which, in many cases, developed along a wide front of tissue-to-tissue contacts, interactions of P. cylindrica against the other Porites species were developed through one or multiple points of contact, resulting from the branching structure of P. cylindrica colonies (Fig. 2b). Tissue-to-tissue contacts formed limited necrotic areas on inferior Porites colonies (starting with points of pink-red color on contacting tissue zones of subordinates; Fig. 2b) which were followed by restricted overgrowth of P. cylindrica tissue and skeleton (Fig. 2c). In a few cases, interspecific interactions revealed reciprocal overgrowths on both partners’ tissue (15.4% of interactions with P. lobata) or an opposite directionality of overgrowth (11.1% of interactions with P. australiensis; Fig. 2d, Table 1). In the case illustrated in Figure 2c, P. lobata was first overgrowing above P. cylindrica and then, overgrowth directionality changed, resulting in a rimlike structured area along a wide frontier area between the partners. The overgrowing area of P. australiensis above a P. cylindrica branch (Fig. 2d) did not reveal any point of rejection. P. lobata This is the 3rd species ranked in the studied hierarchy, recessive to P. rus and P. cylindrica (22 out of 24 interactions) and dominant to P. australiensis and P. lutea
P. rus P. rus was recorded as the clear winner in all 42 interspecific interactions with the other four Porites species (Table 1, Fig. 1). In these encounters, P. rus was always found overgrowing the other Porites colonies (Fig. 2a) with both, tissue and skeleton. In most cases, necrotic zones did not demarcate the borderline between both colonies. Points of rejection (or points of tissue necrosis) were found but were restricted to a few places on the subordinate partner tissue. From time to time, a limited (2–3 mm width) bleached area was found near the overgrowing front, on the inferior tissue only. In some cases, a very narrow (1–2 mm) peripheral light pink color was observed along the overgrowing front line of P. rus tissue. P. cylindrica P. cylindrica is competitively dominant to 3 species (25 out of 28 cases) and inferior only to P. rus (16 out of 16 interactions; Table 1, Fig. 1). In contrast to the interacZoology 104 (2001) 2
Fig. 1. A panel of transitive xenogeneic interactions between five species of the coral genus Porites from Sesoko Island, Okinawa. Arrows point from the dominant to the subordinate. The number of encounters for each pairwise combination and directionality are marked along the arrows.
93
94
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Porites interspecific interactions
(24 out of 28 interactions; Table 1, Fig. 1). Interactions between P. lobata and P. lutea or P. australiensis were usually developed through a wide front line of overgrowing tissue and skeleton (in cases of very large colonies, up to 50 cm in length). Soft tissue lesions were few and were restricted to contact areas. Limited bleaching of inferior species tissue (most of the cases) was seen at 1–2 mm width along contact zones, as well as the appearance of pink color which was developed by all massive species in some of the interacting areas. Some old interactions between different pairwise combinations were partly covered by turf algae and other sedentary organisms, blurring the directionality of hierarchy (Figs. 2e, f). Some reciprocal cases in P. lobata vs. P. australiensis or vs. P. lutea (Table 1, Figs. 1, 2f) were also observed. Xenogeneic interactions looked the same among different species combinations and only careful examination of coral samples under the binocular stereomicroscope revealed colony identity as belonging to a specific species. P. australiensis The 4th species in the rank of hierarchy. This species dominated only P. lutea colonies and was inferior in most (33/37) interactions with the other three Porites species (Table 1, Figs. 1, 2b, e, g). The interactions developed in a similar manner in all three massive Porites species. In only one case (11.1%) P. australiensis overgrew P. cylindrica (Fig. 2d) and in 3 cases (14.3%), reciprocal interactions were developed with P. lobata colonies. P. lutea The inferior species, overgrown in 33/34 cases documented with the other four Porites species. Only in a single case, a reciprocal overgrowth was recorded in a P. lobata vs. P. lutea interaction. As above, interactions against the other massive species developed usually through a wide frontier line of contacts. Intraspecific interactions
We also recorded a high number of intraspecific combinations, mainly in the massive species P. australiensis
(14 cases; Fig. 2h), P. lobata (13 cases) and P. lutea (8 cases). The structure of contacting areas (long frontiers), the type of interactions (overgrowths, restricted pink color and bleaching areas, settlement of turf algae and other organisms in old contacting areas, limited and a few necrotic areas) and reciprocal events of intraspecific interactions were morphologically and structurally the same as recorded in the interspecific encounters. We found no signs of allelopathy in either encounter nor any rejection from a distance (i.e., by sweeper tentacles).
Discussion This field study on interspecific interactions between 5 common Porites species from Sesoko Island, Okinawa, suggests a transitive type of hierarchy. The three massive species (P. lobata, P. australiensis and P. lutea) are ranked lower in this hierarchy (51/54 interactions) while the encrusting species P. rus emerged as the dominant species. Out of the variety of intraspecific defence mechanisms recorded in scleractinian corals (such as allelopathy, sweeper tentacles, sweeper polyps, standoffs, fillings and more; Lang and Chornesky, 1990; Peach and Hoegh-Guldberg, 1999), only the single effector mechanism of overgrowing responses (together with associated secondary outcomes such as the formation of small points of rejection, bleaching of contacting areas, the pink color formation, etc.) dominated the 10 different interspecific and the 5 intraspecific combinations studied here. This outcome differs from the diversity of effector mechanisms found in other coral species where specific genotypes reacted differently (with variable expression of effector mechanisms) to unlike xenogeneic and allogeneic challenges (Rinkevich, 1996; Rinkevich et al., 1993). Interspecific as well as intraspecific interactions between Porites colonies are genetically controlled phenomena (Rinkevich, 1996) that are probably developed slowly with minimal tissue destruction to the inferior partner. Fast developing and acute inflicting effector mechanisms such as digestion by mesenterial filaments (Lang, 1973), sweeper tentacles (Lang and Chornesky, 1990) or
Fig. 2. Xenogeneic and allogeneic interactions between Porites species; (a) P. rus, overgrowing P. cylindrica branches. Few, limited necrotic zones on P. cylindrica tissue (arrowheads). (b) P. cylindrica vs. P. australiensis (right). Two points of contact (arrowheads) with pink-color on P. australiensis areas and restricted overgrowth (lower arrowhead). (c) P. cylindrica (right colony) vs. P. lobata. The rim-like structure area is marked by an arrowhead. (d) P. australiensis (right) overgrowing P. cylindrica branch. (e) P. lobata (up) overgrowing P. australiensis, with sedentary organisms that settled along the frontier line (arrowhead). The contacting P. australiensis tissue is partly bleached. (f) P. australiensis (up) overgrowing P. lobata. The contacting P. lobata tissue is partly bleached (arrowheads). A thin (1–2 mm) pink line along the edge of the peripheral tissue of P. australiensis. (g) P. australiensis (left) overgrowing P. lutea. The contacting P. lutea tissue is bleached along the frontier line (arrowheads). (h) P. australiensis allogeneic interaction. The inferior (lower) partner has a bleached tissue along the contact line. Zoology 104 (2001) 2
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sweeper polyps (Peach and Hoegh-Guldberg, 1999) were never observed during this study nor reported for other studies on Porites interspecific/intraspecific interactions (Lang, 1973; Sheppard, 1979; Bradbury and Young, 1982; Tanner, 1983; Logan, 1984; Nakaya, 1984; Hunter, 1985; Stimson, 1985; Cox, 1986; Dai, 1990; Lang and Chornesky, 1990; Genin and Karp, 1994; Abelson and Loya, 1999). It is also clear that the expressed type of the effector mechanism is not related to the general architectural morphology of the colony (i.e., a branching form vs. massive). For example, xenogeneic and allogeneic interactions of Goniopora (belongs to the same family Poritidae) are characterized by rapid tissue destruction through the production of sweeper polyps (Sheppard, 1982; Peach and Hoegh-Guldberg, 1999). These special structures exude biologically active substances that adversely affect conspecific and xenospecific colonies (Gunthorpe and Cameron, 1990). Another point for consideration is the time course of interactions. Nakaya (1984) explored interspecific and intraspecific interactions in five Porites species in front of Sesoko Island. Three of Nakaya’s species are included in the present study: P. lutea, P. cylindrica (there called P. eridani) and P. rus (called P. iwayamaensis). Studies were performed on long-term field established interactions (as in the present study) and field experiments were conducted for 6 months. The results of the short-term experiments (P. lutea > P. rus > P. cylindrica) differ significantly from the long-term observations (P. rus > P. lutea > P. cylindrica). These contradicting results resemble the interspecific outcomes between Cyphastrea ocellina and Pocillopora damicornis from Hawaii (Romano, 1990), where long-term results of interactions (11 months duration) were quite different from the short-term results (2–11 days duration). Nakaya’s (1984) results also differed from the present research outcomes which indicate that P. lutea is the ultimate subordinate species. Furthermore, our results confirmed previous outcomes (Dai, 1990) demonstrating that P. lutea is a subordinate species to other Porites species, including P. cylindrica, P. australiensis and P. rus. In Chagos Archipelago, P. lutea was also recorded as the most subordinate species out of the 35 xenogeneic combinations assayed with it, also killed by P. andrewsi (Sheppard, 1979 ). Colonies of the 5 tested species interact in the field not only in pairwise combinations but also, simultaneously, in a multi-combination pattern of 3 or more species (data not shown). In these cases, hierarchy developed as expected from the pairwise combination analysis, further emphasizing that hierarchy is genetically controlled (but see Chornesky, 1989), irrespective of the general health of the colony or physiological parameters, although different environmental and biological factors (such as water flow, Genin and Karp, 1994; or 96
epifauna interference, Bak et al., 1982) may affect some of the results. There were also no standoffs, i.e., interactions without a clearly observable outcome such as winner or loser (with the exception of cases where the interacting areas were covered by other organisms). It is known that the expression of different effector mechanisms within a xenogeneic panel of interactions (such as allelopathy, overgrowth, sweeper tentacles, sweeper polyps, etc.) can cause major departures from transitive types of hierarchy (Tanner, 1993). Colonies of the above Porites species interact in the field with other hard and soft coral species (unpublished). A more complete panel of xenogeneic interactions may change the linear hierarchy recorded here to a circular type of hierarchy as recorded in other studies (Chronesky, 1989; Rinkevich et al., 1993; Abelson and Loya, 1999). This could prove to be an important mechanism in maintaining high species diversity in the coral reef.
Acknowledgements This study is part of the research carried out in the Minerva Center for Marine Invertebrate Immunology and Developmental Biology and was also supported by a fellowship to BR from the Japanese Ministry of Science, Education, Culture and Sports to a Foreign Visiting Professor of the Tropical Biosphere Research Center, University of the Ryukyus. We thank A. Takemura, S. Nakamura, C. Uchima and Y. Nakano for hospitality and assistance during the study and to R. van Woesik for help in identifying Porites species.
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Dai, C.F. 1990. Interspecific competition in Taiwanese corals with special reference to interactions between alcyonaceans and scleractinians. Mar. Ecol. Prog. Ser. 60: 291–297. Genin, A. and L. Karp. 1994. Effects of flow on competitive superiority in scleractinian corals. Limnol. Oceanogr. 39: 913–924. Gunthorpe, L. and A.M. Cameron. 1990. Toxic exudate from the hard coral Goniopora tenuidens. Toxicon 28: 1347–1350. Hunter, C.L. 1985. Assessment of clonal diversity and population structure of Porites compressa (Cnidaria, Scleractinia). Proceeding of the 5th International Coral Reef Congress, Tahiti 1985, 6: 69–74. Lang, J. 1973. Interspecific aggression by scleractinian corals. 2. Why the race is not only to the swift. Bull. Mar. Sci. 23: 260–279. Lang, J. and E.A. Chornesky. 1990. Competition between scleractinian reef corals – A review of mechanisms and effects. In: Ecosystems of the world (Z. Dubinsky, ed.). Coral Reefs 25: 209–252. Logan, A. 1984. Interspecific aggression in hermatypic coral from Bermuda. Coral Reefs 3: 131–138. Loya, Y, K. Sakai, K. Yamazato, Y. Nakano, H. Sambali and R. van Woesik. 2001. Coral bleaching: The winners and the losers. Ecol. Lett. 4: 122–131. Nakaya, S. 1984. Intra- and interspecific interactions in Porites (Scleractinia). M.Sc. thesis, The Univ. Ryukyus, 102 pp. Peach, B. and O. Hoegh-Guldberg. 1999. Sweeper polyps of the coral Goniopora tenuidens (Scleractina: Poritidae). Invertebrate Biol. 118: 1–7. Rinkevich, B. 1996. Links between alloimmune and their genetic background in colonial urochordates and cnidarians: Evidence for the recognition of “nonself” as opposed to “self”. In: Modulators of Immune Responses: the Evolutionary Trail (J.S.
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Stolen, T.C. Fletcher, C.J. Bayne, C.J. Secombes, J.T. Zelikoff, L. Twerdok and D.P. Anderson, eds.). SOS Publications, pp. 1–13 Rinkevich, B., N. Shashar and T. Liberman. 1993. Nontransitive xenogeneic interactions between four common Red Sea sessile invertebrates. Proceedings of the 7th International Coral Reef Symposium, pp. 833–839. Romano, S.L. 1990. Long-term effects of interspecific aggression on growth of the reef-building corals Cyphastrea ocellina (Dana) and Pocillopora damicornis (Linnaeus). J. Exp. Mar. Biol. Ecol. 140: 135–146. Sakai, K. and K. Yamazato. 1987. Preliminary list of hermatypic corals around Sesoko Island, Okinawa with a note on the decrease of the species richness from 1980 to 1986. Galaxea 6: 43–51. Sheppard, C.R.C. 1979. Interspecific aggression between reef corals with reference to their distribution. Mar. Ecol. Prog. Ser. 1: 237–247. Sheppard, C.R.C. 1982. “Reach” of aggressively interacting corals and relative importance of interactions at different depths. Proceedings of the 4th International Coral Reef Symposium, Manila, 2: 363–368. Stimson, J. 1985. The effect of shading by the table coral Acropora hyacinthus on understory corals. Ecology 66: 40–53. Tanner, J.E. 1993. Experimental analysis of digestive hierarchies in coral assemblages. Proceedings of the 7th International Coral Reef Symposium, Guam, 1: 569–574. Veron, J.E.N. 1986. Corals of Australia and the Indo Pacific. Univ. Hawaii Press, Honolulu, 644 pp. Yamazato, K. and T. Yeemin. 1986. Preliminary study on the inter- and intra-specific interactions among coral of Khang Khao Island, The Sichang Islands, Gulf of Thailand. Galaxea 5: 163–174.
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Interspecific interactions among species of the coral genus Porites from Okinawa, Japan Baruch Rinkevich1 and Kazuhiko Sakai2 1
Minerva Center for Marine Invertebrate Immunology & Developmental Biology, National Institute of Oceanography, Israel Oceanographic & Limnological Research, Tel Shikmona, Haifa, Israel 2 Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, Sesoko, Motobu-cho, Okinawa 905-0227, Japan Received June 7, 2001. Accepted August 13, 2001
Summary Analysis of field established xenogeneic interactions among five Porites species from Sesoko Island, Okinawa, revealed a transitive type of hierarchy as: P. rus > P. cylindrica > P. lobata > P. australiensis > P. lutea. Out of the 111 interspecific encounters studied, in only 5.4% reciprocal interactions were recorded, and in a single case, the opposite directionality of hierarchy was documented. Allogeneic encounters were also observed. A single major effector mechanism, an overgrowth (together with secondary outcomes such as the formation of small points of rejection, bleaching and pink color formation along a narrow peripheral belt of contacting tissues), was the only response in all 10 xenogeneic and 5 allogeneic combinations. In some massive colonies, a long contacting line of up to 50 cm was established. No sign for allelopathy, stand-off or rejection from a distance (i.e., by sweeper tentacles, sweeper polyps) was observed. Results are discussed with the accumulated data on Porites species from different reefs, worldwide, confirming that this genus is commonly lower in the hierarchy of xenogeneic interactions. Key words: allorecognition, Cnidaria, effector mechanism, hierarchy, Japan
Introduction Interspecific competitive networks in sedentary colonial invertebrate assemblages are an important factor in the construction of communities and therefore have been studied in detail in several marine ecosystems, including coral reefs. Neighboring coral colonies which are in close proximity in nature may affect one another through a variety of competitive measures (reviewed in Lang and Chornesky, 1990). However, competitive outcomes are not always visible and even when they are visible, they may depend on both the combination of competing species and the environment (e.g., Cox, 1986; Chornesky, 1989). As a result, the outcomes for
competition were sometimes different when short vs. long-term in situ observations were compared or when laboratory vs. field results were evaluated (Bak et al., 1982; Logan, 1984; Nakaya, 1984; Chornesky, 1989; Romano, 1990). Some slower developing interspecific outcomes were also misinterpreted as “stand-offs” (Connell, 1976) where two coral colonies appeared to stop growing along a common margin, often without obvious damage to their soft tissues. Some followed up stand-offs lasted for at least nine years before one partner eventually overgrew the other (Connell and Keough, 1985). The genus Porites is a worldwide distributed and ecologically important coral taxon (Veron, 1986). Studies
1
Corresponding author: Baruch Rinkevich, Minerva Center for Marine Invertebrate Immunology & Developmental Biology, National Institute of Oceanography, Israel Oceanographic & Limnological Research, Tel Shikmona, P.O.Box 8030, Haifa 31080, Israel, phone: 972-4-8515202; fax: 972-4-8511911; e-mail: [email protected] 0944-2006/01/104/02-091 $ 15.00/0
B. Rinkevich and K .Sakai
were also engaged with interspecific interactions of Porites species against other coral species. These studies were performed in a variety of coral reefs including Enewetak atoll (Stimson, 1985), Chagos atoll (Sheppard, 1979), the Caribbean (Lang, 1973; Logan, 1984; Lang and Chornesky, 1990), the Great Barrier Reef, Australia (Bradbury and Young, 1982; Tanner, 1983), Taiwan (Dai, 1990), Hawaii (Hunter, 1985; Cox, 1986) the Gulf of Thailand (Yamazato and Yeemin, 1986), Gulf of Eilat, Red Sea (Genin and Karp, 1994; Abelson and Loya, 1999) and Okinawa, Japan (Nakaya, 1984). These studies revealed that the Porites species are either intermediate or subordinate (the lower order in ranking) in the competitive hierarchies. In most cases, Porites species were analysed against other coral species. In only a single case (Nakaya, 1984), the aggressive hierarchy between different Porites species was evaluated. The Ryukyu Islands (including Okinawa) possess one of the northernmost distributions of coral reefs (26–27 ºN). The well developed reefs in this area have deteriorated rapidly during the last two decades. About 15 years ago, 143 hermatypic species were still recorded in Sesoko Island, Okinawa, where the Sesoko Marine Station is located, including 11 Porites sp. (Sakai and Yamato, 1987). The rate of decrease in species richness, coral coverage and the number of species was further enhanced following the 1998 coralbleaching event (Loya et al., 2001). In this area, several species of Porites dominate the shallow reef (1–7 m depth) forming massive structures with large colonies that inter- and intraspecifically interact in situ for prolonged periods (Nakaya, 1984). This study reveals the interspecific hierarchy pattern of the five most common Porites species in front of the Sesoko Station.
Materials and methods Observations were conducted in situ by SCUBA diving at a depth of 1–7 m in front of the marine station at Sesoko Island. Five species of Porites are commonly found in this area: the hemispherical P. australiensis Vaughan 1918, P. lutea Edwards and Haime 1860, P. lobata Dana 1846; P. rus Forskäl 1775, with laminar or contorted anastomosing branches and column colonies, and the branching species P. cylindrica Dana 1846. In many cases, colonies of two or more of the above species grew near or attached to each other. We surveyed the area for all Porites vs. Porites interspecific (xenogeneic) interactions, and when applicable, also for intraspecific (allogeneic) encounters. This field study documented the interactions found in situ (June-August 2000; interactions between Porites species and other coral species were not studied) and did not involve long term followed up observations. Interactions between colonies of the above five species were documented underwater in detailed writing and by photography. Each colony was labeled with a plastic tag and in the case of the three hemispherical species (P. australiensis, P. lutea, P. lobata), colony samples were taken by hammer and chisel. Each sample, containing at least 50 polyps, was separately put into a marked plastic bag. Samples were taken to the laboratory and the tissues were removed by Clorox solution overnight. All samples were checked under a compound microscope to verify species identity. This thorough examination revealed few interactions of the above Porites species with two additional species, P. solida and P. okinawensis, which could not be identified as such in situ. We documented any outcome that was clear from visual inspections. Some interactions were carefully isolated
Table 1. Summary of interspecific interactions between five Porites species from Sesoko Island, Okinawa. Type of combination A vs. B
n
A wins (%)
B wins (%)
P. rus vs. P. cylindrica
16
100.0
0.0
0.0
P. rus vs. P. lobata P. rus vs. P. australiensis P. rus vs. P. lutea P. cylindrica vs. P. lobata
11 7 8 13
100.0 100.0 100.0 84.6
0.0 0.0 0.0 0.0
0.0 0.0 0.0 15.4
P. cylindrica vs. P. australiensis P. cylindrica vs. P. lutea P. lobata vs. P. australiensis
9 6 21
88.9 100.0 85.7
11.1 0.0 0.0
0.0 0.0 14.3
P. lobata vs. P. lutea P. australiensis vs. P. lutea
7 13
85.7 100.0
0.0 0.0
14.3 0.0
92
Reciprocal (%)
Major interactions Overgrowth, small and few necrotic areas, limited bleaching as above as above as above Points of rejections on recessive species tissues followed by overgrowth in areas of contact as above as above Wide front of overgrowth, small and few necrotic areas, limited bleaching bands along the frontiers, pink colors and in many cases, turf algae settlement as above as above Zoology 104 (2001) 2
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by chisel and hammer from the colonies, brought to the laboratory and inspected under a binocular stereomicroscope. There were cases in the field where no decision on the type of interaction could be made. These cases typically involved reciprocal interactions that were partially covered with encrusting organisms and algae that settled onto interacting zones. These cases were eliminated from the analysis to reduce artifacts and errors for hierarchy determination resulting from interactions with other organisms, or caused by environmental factors (partial predation, sedimentation effects, algae interference, etc.).
Results General hierarchy
The 5 Porites species formed 10 interspecific combinations, of which we observed a total of 111 interspecific encounters. The outcome of these interactions revealed a linear type of hierarchy, with Porites rus as the most dominant species and P. lutea at the bottom as the subordinate (Fig. 1, Table 1). The linear hierarchy was clearly evident although in 6 cases (5.4%), reciprocal interactions were recorded, and in a single case (0.9%), the opposite directionality of hierarchy was documented (Fig. 1, Table 1). P. cylindrica colonies were recorded in 4 cases encountering P. okinawensis colonies, with two winners for each partner species. Two cases of P. solida > P. lobata were also recorded. Many of the interactions detailed below are probably long-term encounters that developed through years of tissue-to-tissue contacts reducing the variations recorded during short-term observations (i.e., Chornesky, 1989).
tions between the other four species which, in many cases, developed along a wide front of tissue-to-tissue contacts, interactions of P. cylindrica against the other Porites species were developed through one or multiple points of contact, resulting from the branching structure of P. cylindrica colonies (Fig. 2b). Tissue-to-tissue contacts formed limited necrotic areas on inferior Porites colonies (starting with points of pink-red color on contacting tissue zones of subordinates; Fig. 2b) which were followed by restricted overgrowth of P. cylindrica tissue and skeleton (Fig. 2c). In a few cases, interspecific interactions revealed reciprocal overgrowths on both partners’ tissue (15.4% of interactions with P. lobata) or an opposite directionality of overgrowth (11.1% of interactions with P. australiensis; Fig. 2d, Table 1). In the case illustrated in Figure 2c, P. lobata was first overgrowing above P. cylindrica and then, overgrowth directionality changed, resulting in a rimlike structured area along a wide frontier area between the partners. The overgrowing area of P. australiensis above a P. cylindrica branch (Fig. 2d) did not reveal any point of rejection. P. lobata This is the 3rd species ranked in the studied hierarchy, recessive to P. rus and P. cylindrica (22 out of 24 interactions) and dominant to P. australiensis and P. lutea
P. rus P. rus was recorded as the clear winner in all 42 interspecific interactions with the other four Porites species (Table 1, Fig. 1). In these encounters, P. rus was always found overgrowing the other Porites colonies (Fig. 2a) with both, tissue and skeleton. In most cases, necrotic zones did not demarcate the borderline between both colonies. Points of rejection (or points of tissue necrosis) were found but were restricted to a few places on the subordinate partner tissue. From time to time, a limited (2–3 mm width) bleached area was found near the overgrowing front, on the inferior tissue only. In some cases, a very narrow (1–2 mm) peripheral light pink color was observed along the overgrowing front line of P. rus tissue. P. cylindrica P. cylindrica is competitively dominant to 3 species (25 out of 28 cases) and inferior only to P. rus (16 out of 16 interactions; Table 1, Fig. 1). In contrast to the interacZoology 104 (2001) 2
Fig. 1. A panel of transitive xenogeneic interactions between five species of the coral genus Porites from Sesoko Island, Okinawa. Arrows point from the dominant to the subordinate. The number of encounters for each pairwise combination and directionality are marked along the arrows.
93
94
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(24 out of 28 interactions; Table 1, Fig. 1). Interactions between P. lobata and P. lutea or P. australiensis were usually developed through a wide front line of overgrowing tissue and skeleton (in cases of very large colonies, up to 50 cm in length). Soft tissue lesions were few and were restricted to contact areas. Limited bleaching of inferior species tissue (most of the cases) was seen at 1–2 mm width along contact zones, as well as the appearance of pink color which was developed by all massive species in some of the interacting areas. Some old interactions between different pairwise combinations were partly covered by turf algae and other sedentary organisms, blurring the directionality of hierarchy (Figs. 2e, f). Some reciprocal cases in P. lobata vs. P. australiensis or vs. P. lutea (Table 1, Figs. 1, 2f) were also observed. Xenogeneic interactions looked the same among different species combinations and only careful examination of coral samples under the binocular stereomicroscope revealed colony identity as belonging to a specific species. P. australiensis The 4th species in the rank of hierarchy. This species dominated only P. lutea colonies and was inferior in most (33/37) interactions with the other three Porites species (Table 1, Figs. 1, 2b, e, g). The interactions developed in a similar manner in all three massive Porites species. In only one case (11.1%) P. australiensis overgrew P. cylindrica (Fig. 2d) and in 3 cases (14.3%), reciprocal interactions were developed with P. lobata colonies. P. lutea The inferior species, overgrown in 33/34 cases documented with the other four Porites species. Only in a single case, a reciprocal overgrowth was recorded in a P. lobata vs. P. lutea interaction. As above, interactions against the other massive species developed usually through a wide frontier line of contacts. Intraspecific interactions
We also recorded a high number of intraspecific combinations, mainly in the massive species P. australiensis
(14 cases; Fig. 2h), P. lobata (13 cases) and P. lutea (8 cases). The structure of contacting areas (long frontiers), the type of interactions (overgrowths, restricted pink color and bleaching areas, settlement of turf algae and other organisms in old contacting areas, limited and a few necrotic areas) and reciprocal events of intraspecific interactions were morphologically and structurally the same as recorded in the interspecific encounters. We found no signs of allelopathy in either encounter nor any rejection from a distance (i.e., by sweeper tentacles).
Discussion This field study on interspecific interactions between 5 common Porites species from Sesoko Island, Okinawa, suggests a transitive type of hierarchy. The three massive species (P. lobata, P. australiensis and P. lutea) are ranked lower in this hierarchy (51/54 interactions) while the encrusting species P. rus emerged as the dominant species. Out of the variety of intraspecific defence mechanisms recorded in scleractinian corals (such as allelopathy, sweeper tentacles, sweeper polyps, standoffs, fillings and more; Lang and Chornesky, 1990; Peach and Hoegh-Guldberg, 1999), only the single effector mechanism of overgrowing responses (together with associated secondary outcomes such as the formation of small points of rejection, bleaching of contacting areas, the pink color formation, etc.) dominated the 10 different interspecific and the 5 intraspecific combinations studied here. This outcome differs from the diversity of effector mechanisms found in other coral species where specific genotypes reacted differently (with variable expression of effector mechanisms) to unlike xenogeneic and allogeneic challenges (Rinkevich, 1996; Rinkevich et al., 1993). Interspecific as well as intraspecific interactions between Porites colonies are genetically controlled phenomena (Rinkevich, 1996) that are probably developed slowly with minimal tissue destruction to the inferior partner. Fast developing and acute inflicting effector mechanisms such as digestion by mesenterial filaments (Lang, 1973), sweeper tentacles (Lang and Chornesky, 1990) or
Fig. 2. Xenogeneic and allogeneic interactions between Porites species; (a) P. rus, overgrowing P. cylindrica branches. Few, limited necrotic zones on P. cylindrica tissue (arrowheads). (b) P. cylindrica vs. P. australiensis (right). Two points of contact (arrowheads) with pink-color on P. australiensis areas and restricted overgrowth (lower arrowhead). (c) P. cylindrica (right colony) vs. P. lobata. The rim-like structure area is marked by an arrowhead. (d) P. australiensis (right) overgrowing P. cylindrica branch. (e) P. lobata (up) overgrowing P. australiensis, with sedentary organisms that settled along the frontier line (arrowhead). The contacting P. australiensis tissue is partly bleached. (f) P. australiensis (up) overgrowing P. lobata. The contacting P. lobata tissue is partly bleached (arrowheads). A thin (1–2 mm) pink line along the edge of the peripheral tissue of P. australiensis. (g) P. australiensis (left) overgrowing P. lutea. The contacting P. lutea tissue is bleached along the frontier line (arrowheads). (h) P. australiensis allogeneic interaction. The inferior (lower) partner has a bleached tissue along the contact line. Zoology 104 (2001) 2
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sweeper polyps (Peach and Hoegh-Guldberg, 1999) were never observed during this study nor reported for other studies on Porites interspecific/intraspecific interactions (Lang, 1973; Sheppard, 1979; Bradbury and Young, 1982; Tanner, 1983; Logan, 1984; Nakaya, 1984; Hunter, 1985; Stimson, 1985; Cox, 1986; Dai, 1990; Lang and Chornesky, 1990; Genin and Karp, 1994; Abelson and Loya, 1999). It is also clear that the expressed type of the effector mechanism is not related to the general architectural morphology of the colony (i.e., a branching form vs. massive). For example, xenogeneic and allogeneic interactions of Goniopora (belongs to the same family Poritidae) are characterized by rapid tissue destruction through the production of sweeper polyps (Sheppard, 1982; Peach and Hoegh-Guldberg, 1999). These special structures exude biologically active substances that adversely affect conspecific and xenospecific colonies (Gunthorpe and Cameron, 1990). Another point for consideration is the time course of interactions. Nakaya (1984) explored interspecific and intraspecific interactions in five Porites species in front of Sesoko Island. Three of Nakaya’s species are included in the present study: P. lutea, P. cylindrica (there called P. eridani) and P. rus (called P. iwayamaensis). Studies were performed on long-term field established interactions (as in the present study) and field experiments were conducted for 6 months. The results of the short-term experiments (P. lutea > P. rus > P. cylindrica) differ significantly from the long-term observations (P. rus > P. lutea > P. cylindrica). These contradicting results resemble the interspecific outcomes between Cyphastrea ocellina and Pocillopora damicornis from Hawaii (Romano, 1990), where long-term results of interactions (11 months duration) were quite different from the short-term results (2–11 days duration). Nakaya’s (1984) results also differed from the present research outcomes which indicate that P. lutea is the ultimate subordinate species. Furthermore, our results confirmed previous outcomes (Dai, 1990) demonstrating that P. lutea is a subordinate species to other Porites species, including P. cylindrica, P. australiensis and P. rus. In Chagos Archipelago, P. lutea was also recorded as the most subordinate species out of the 35 xenogeneic combinations assayed with it, also killed by P. andrewsi (Sheppard, 1979 ). Colonies of the 5 tested species interact in the field not only in pairwise combinations but also, simultaneously, in a multi-combination pattern of 3 or more species (data not shown). In these cases, hierarchy developed as expected from the pairwise combination analysis, further emphasizing that hierarchy is genetically controlled (but see Chornesky, 1989), irrespective of the general health of the colony or physiological parameters, although different environmental and biological factors (such as water flow, Genin and Karp, 1994; or 96
epifauna interference, Bak et al., 1982) may affect some of the results. There were also no standoffs, i.e., interactions without a clearly observable outcome such as winner or loser (with the exception of cases where the interacting areas were covered by other organisms). It is known that the expression of different effector mechanisms within a xenogeneic panel of interactions (such as allelopathy, overgrowth, sweeper tentacles, sweeper polyps, etc.) can cause major departures from transitive types of hierarchy (Tanner, 1993). Colonies of the above Porites species interact in the field with other hard and soft coral species (unpublished). A more complete panel of xenogeneic interactions may change the linear hierarchy recorded here to a circular type of hierarchy as recorded in other studies (Chronesky, 1989; Rinkevich et al., 1993; Abelson and Loya, 1999). This could prove to be an important mechanism in maintaining high species diversity in the coral reef.
Acknowledgements This study is part of the research carried out in the Minerva Center for Marine Invertebrate Immunology and Developmental Biology and was also supported by a fellowship to BR from the Japanese Ministry of Science, Education, Culture and Sports to a Foreign Visiting Professor of the Tropical Biosphere Research Center, University of the Ryukyus. We thank A. Takemura, S. Nakamura, C. Uchima and Y. Nakano for hospitality and assistance during the study and to R. van Woesik for help in identifying Porites species.
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