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INFLUENCE OF RHODOLITH‐FORMING SPECIES AND GROWTH‐FORM ON ASSOCIATED FAUNA OF RHODOLITH BEDS IN THE CENTRAL‐WEST GULF OF CALIFORNIA, MÉXICO

GUSTAVO HINOJOSA‐ARANGO AND RAFAEL RIOSMENA‐RODRÍGUEZ

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P.S.Z.N.: Marine Ecology, 25 (2): 109–127 (2004) ! 2004 Blackwell Verlag, Berlin ISSN 0173-9565

Accepted: March 15, 2004

Influence of Rhodolith-Forming Species and Growth-Form on Associated Fauna of Rhodolith Beds in the Central-West Gulf of California, Me´xico Gustavo Hinojosa-Arango* & Rafael Riosmena-Rodrı´guez Programa de Investigacio´n en Bota´nica Marina, Departamento de Biologı´a Marina UABCS, Apartado postal, 19-B, La Paz, Baja California Sur 23080, Me´xico.

With 7 figures and 1 appendix

Keywords: Associated fauna, rhodolith beds, assemblages, growth-form, Gulf of California, Mexico.

Abstract. Rhodoliths provide a stable and three-dimensional habitat to which other seaweeds and invertebrates can attach. Although ecological factors affecting rhodolith beds have been studied, little is known about the effect of rhodolith species and growth-form on associated fauna. Experiments were conducted at three rhodolith beds in the central-west Gulf of California. Faunal abundance differed significantly in relation to rhodolith-forming species, but no significant differences were observed between different growth-forms. Rhodolith structure differs between the species Lithophyllum margaritae and Neogoniolithon trichotomum, and the combination of structure differences and rhodolith abundances may be responsible of the significant differences in faunal abundance and richness. Crustaceans, polychaetes and molluscs were the most important taxa in all three rhodolith beds. The amphipod species Pontogeneia nasa and the cnidarian Aiptasia sp. were dominant in both rhodolith beds, El Requeso´n and Isla Coyote, in Bahı´a Concepcio´n. The Isla Coronados rhodolith bed was dominated by an unidentified harpacticoid copepod (Copepoda sp.1). Rhodolith species is more important than growth-form in determining abundance and richness of the associated fauna. Nevertheless, factors such as wave motion, depth, bioturbation and others should be considered when studying organisms associated with rhodolith beds.

*Author to whom correspondence should be addressed: School of Biology and Biochemistry, Queen’s University of Belfast, Medical Biology Centre, Belfast BT9 7BL, Northern Ireland.

E-mail: g.hinojosa@qub.ac.uk U. S. Copyright Clearance Center Code Statement:

0173-9565/2004/2502–109/$15.00/0

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Problem Rhodolith beds are marine communities dominated by free-living, non-geniculate coralline red algae (Foster, 2001). They are found worldwide and occur from the intertidal zone to depths of over 200 m (Littler et al., 1991). Rhodoliths are considered as !habitat modifiers" or !bioengineers" that, by virtue of their branching and interlocking nature, provide relatively stable and three-dimensional habitats (Bruno & Bertness, 2001). They provide a surface to which other seaweeds (Jacquotte, 1962; Maggs, 1983a, 1983b; Hily et al., 1992; Fazakerley & Guiry, 1998) and animals can attach (Hily et al., 1992; Birkett et al., 1998; Steller et al., 2003). Live rhodolith beds are ecologically important because they may support richer communities than dead rhodoliths, gravel or sand bottoms of equivalent grain size (Cabioch, 1969; Keegan, 1974).

Rhodolith beds in the Gulf of California are composed mainly of six species, which are predominantly fructicose (Riosmena-Rodrı´guez, 2002). Early ecological studies on rhodolith beds in this area focused on how environmental conditions, such as water motion, affected rhodolith morphology (Steller & Foster, 1995). More recent studies have been focused to characterize the community associated with this habitat (ReyesBonilla et al., 1997; Hall-Spencer, 1998; De Grave, 1999; De Grave & Whitaker, 1999; Nunn, 1999; James, 2000; Steller et al., 2003). Another study described the influence of rhodolith branch-density (as an expression of volume) on the associated fauna from beds in the Gulf of California (Steller et al., 2003). That study, however, dealt with only one growth-form (fructicose). Growth-form probably plays an important role in determining faunal abundance and richness, but it would be important to corroborate this based on direct comparisons between the main rhodolith-forming species [Lithophyllum margaritae (Hariot) Heydrich and Neogoniolithon trichotomum (Edrich) Setchell & Mason].

Hypothetically, differences in substratum structure might be reflected in the species composition or relative abundance, but this has never been tested in rhodolith beds.

The aims were therefore to: (i) determine if abundance and richness of associated fauna are influenced by rhodolith growth-form (foliose versus fructicose) and (ii) determine whether associated faunal abundance and richness change depending on the main rhodolith forming species that compose a bed (L. margaritae versus N. trichotomum).

Material and Methods Qualitative and quantitative surveys were carried out in three rhodolith beds from two different localities in the central-west Gulf of California, Me´xico: the Isla Coyote (26"43¢ N, 111"49¢ W) and El Requeso´n (26"39¢ N, 111"49¢ W) rhodolith beds located in Bahı´a Concepcio´n, and the Isla Coronados bed (26"06¢ N, 111"17¢ W) located beside the island of the same name. These localities were described by Foster et al. (1997) and Steller et al. (2003).

At each site, 50-m-long transects were placed randomly inside the bed parallel to the shore and examined using SCUBA techniques. Rhodoliths of 5 cm diameter were randomly selected every 10 m along the transect for associated fauna analysis. The two rhodoliths nearest to the transect at every 10 m mark, which had the required diameter and different growth-form (foliose and fructicose as described in Riosmena-Rodrı´guez et al., 1999, figure 14), were collected from both rhodolith beds, Isla Coyote and El Requeso´n, in Bahı´a Concepcio´n. Two specimens of the rhodolith-forming species L. margaritae and N. trichotomum (as described in Dawson, 1960) were collected following the sampling technique described above from the Isla Coronados" rhodolith bed. All thalli were collected individually in plastic

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bags and sealed underwater when they were retrieved. For each transect a total of 10 rhodoliths were obtained. Samples were fixed in 10% formalin-seawater on the shore and transported to the laboratory.

Rhodoliths" branch density was estimated as the mean number of apical tips counted in five quadrants of 1 cm2 as described by Steller & Foster (1995). All rhodolith-forming species were identified using Riosmena-Rodrı´guez (2002) and the resulting collection has been deposited in the Herbario Ficolo´gico of the Universidad Autonoma de Baja California Sur (UABCS). Rhodolith thalli were crushed with forceps.

Epibenthic and cryptic organisms larger than 0.5 mm were removed with the aid of a stereoscopic microscope (40·) and identified following Smith & Carlton (1975), Sieg & Winn (1978, 1981), Brusca (1980), Salazar-Vallejo et al. (1989), Bastida-Zavala (1991), Keen (1992), and Wicksten (1984). The organisms were preserved in 70% ethanol and have been held by the second author for eventual transfer to the Museo de Historia Natural in La Paz, Baja California Sur, Me´xico (UABCS).

At the two rhodolith beds in Bahia Concepcio´n, El Requeso´n and Isla Coyote, samples were collected specifically to examine the effects of growth-form on faunal richness and abundance. Lithophyllum margaritae rhodoliths were obtained (40 foliose and 40 fructicose morphologies as in RiosmenaRodrı´guez et al., 1999) from eight transects. The effect of rhodolith species on faunal abundance and richness was evaluated at Isla Coronados. At this locality, two rhodolith species, N. trichotomum and L. margaritae, are found growing adjacent to each other in relative high abundance. A total of 40 rhodoliths were obtained from four transects as described previously (20 N. trichotomum and 20 L. margaritae).

Data of species abundance and richness were tested using Cochran and Kolmogorov-Smirnov for normality and homogeneity of variance, respectively (a ¼ 0.05). Unidentified organisms were not considered in richness analyses, and only species which composed 90% of the variance were included in statistical analyses. Mean and standard error (SE) were calculated for abundance and richness, and a oneway ANOVA (model 1) was applied. A Tukey test was used when significant differences were present (Zar, 1996).

Results A total of 120 rhodoliths were analyzed and 8199 associated faunal organisms obtained, of which only 6806 (83%) could be identified. The number of animals identified to species level was 6007, another 782 to genus and 17 only to family. A total of 104 species (52 determined to species and 52 to genus level) were found (see Appendix). Crustaceans, polychaetes and molluscs were the most important groups in all three rhodolith beds. Cnidarians, echinoderms, bryozoans and sponges presented low abundance and richness when present.

General faunal abundance was greater in foliose forms in Isla Coyote and in fructicose forms in El Requeso´n (Fig. 1). In El Requeso´n and Isla Coyote, foliose form richness tended to be greater than in fructicose, but the differences were not significant (Fig. 1). ANOVA showed no significant differences (P > 0.10) in faunal abundance, and no clear relationship between faunal abundance and rhodolith growth-form was found.

Analyses using the most important taxa showed that crustaceans had a higher richness than the other taxa in both Isla Coyote and El Requeso´n localities. Cnidarians, molluscs and polychaetes showed lower species number (Fig. 2). However, the differences were not significant (P > 0.10) and, as in the case of abundance, the relation between rhodolith growth-form was not clear.

In analyzing the fauna of the two growth-forms at El Requeso´n and Isla Coyote, the simple dominance coefficient showed that nine species represented 90% of the total abundance. Pontogeneia nasa (amphipod) was the dominant species with 23 indiv.Ærhodolith)1 (35.9% of total abundance) in both growth-forms. It was followed by the cnidarian Aiptasia sp. and the ostracod Cylindroleberis sp. with 11

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Fig. 1. Abundance and richness of cryptofauna: comparison of two different rhodolith growth-forms in Bahı´a Concepcio´n beds. Means ± standard error (SE).

indiv.Ærhodolith)1 (17.5%), the amphipods Ianiropsis montereyensis, Bemlos macromanus and Microdeutopus sp. and Copepoda sp.1 with 5 indiv.Ærhodolith)1 (6% each species). The amphipod Elasmopus rapax and the ophiuran Ophiactis savignyi, both 2 indiv.Ærhodolith)1, made up 1% of the total abundance. The associated species did not show significant differences (P > 0.10) between the two rhodolith growth-forms at El Requeso´n and Isla Coyote beds (Fig. 3). Comparisons between two rhodolith species at the Isla Coronados bed showed that N. trichotomum had greater faunal abundance (49 organisms) than L. margaritae (32 organisms) (Fig. 4). Differences in abundance between species were statistically significant (P < 0.05). Species richness followed a similar pattern for the most important groups, the crustaceans, molluscs and polychaetes. All taxa, except molluscs, had higher richness in N. trichotomum, but these differences were not significant (Fig. 5).

Crustaceans were the most abundant group in both rhodolith species, being significantly greater in N. trichotomum (P < 0.01) than in L. margaritae. This group was followed in importance by molluscs and polychaetes, with abundance below 5 indiv.Ærhodolith)1. Neither group presented significant differences (P > 0.10) between rhodolith species (Fig. 6).

A total of seven species represented 85% of the faunal abundance in the two rhodolith species. The analysis of associated species in N. trichotomum and L. margaritae showed a similar pattern. An unidentified species of harpacticoidean copepod (Copepoda sp.1) was dominant in both rhodolith species with an average of 32 indiv.Ærhodolith)1 (78% total abundance). The other species, Copepoda sp.5, Micropanope nitida, P. nasa, B. macromanus, Califanthura squamosissima and Copepoda sp.3 represented less than 3% of the total abundance, respectively (Fig. 7).

The dominant species, Copepoda sp.1, was the only one significantly more abundant in N. trichotomum (P < 0.01).

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Fig. 2. Richness of dominant cryptofaunal taxa depending on rhodolith growth-form in Bahı´a Concepcio´n beds. Means ± SE.

Discussion A total of 104 species (52 determined to species and 52 to genus level) were associated with rhodolith beds in the central-western Gulf of California, numbers similar to those reported by Steller et al. (2003). This number of species is also similar to that observed in other marine systems like corals, maerl and kelp beds (Jacquotte, 1962; Cabioch, 1969; Keegan, 1974; Bosence, 1979; Austin et al., 1980; Tsuchiya et al., 1986, 1989; Hily, 1989; Hily et al., 1992; Tsuchiya & Yanaha, 1992; Patton, 1994), although sampling size in most of these studies was bigger. Comparing a similar area or volume between rhodoliths and other habitats reveals a higher abundance and richness in the former. Rhodoliths present higher stability to physical and animal disturbance than other non-calcareous macroalgae. However, the species richness observed in the present study was lower than that reported by Dearn (1987) for the calcareous algae Calliarthon sp.: that macroalga presented an additional 43 associated species.

Rhodolith density may be another important factor for associated fauna because it provides stability, and such beds are less easily disturbed by wave and current action.

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Fig. 3. Abundance of dominant cryptofaunal species depending on rhodolith growth-form in Bahı´a Concepcio´n beds. Means ± SE.

Low density and spheroid shape will favor perturbations by physical factors, as has been observed in cobbles (Lieberman et al., 1979; Davis & Wilce, 1987). One factor which contributes to the abundant associated fauna in rhodoliths is probably the lack of secretion of antigrazing substances, as observed in other macroalgae (Norton & Benson, 1983; Hay et al., 1988; Williams & Seed, 1992).

The main disadvantage for organisms associated with ephemeral algae is that substrate availability depends on algal life cycle. Coyer (1984) observed that organisms associated with kelps can only live there for a short time because kelp grows at a fast rate. Rhodoliths are always available as substrate, and faunal abundance and richness are therefore greater than described for brown algae holdfasts (Ojeda & Santelices, 1984; Villouta & Santelices, 1984), and some corals (Tsuchiya et al., 1986, 1989; Tsuchiya & Yanaha, 1992). Brusca et al. (2004) observed significant variations in crustacean community with seasonal temperature changes, which coincided with Sargassum sinicola Setchell & Gardner death and habitat disappearance. In contrast, rhodoliths are stable and permanent structures due to calcification, supporting greater faunal abundance and richness.

Statistical analyses showed no significant growth-form-related differences in faunal abundance and richness. Both rhodolith forms presented 5 cm average diameter and 5 branchesÆcm)2 . This structural similarity provides approximately the same number of available spaces and, as a consequence, the rhodoliths" functionality as a habitat for associated species may not change. This would explain the similar abundance and

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Fig. 4. Abundance (* indicates statistically significant, P < 0.05) and richness of cryptofauna: comparison of two rhodolith species in the Isla Coronados bed. Means Âą SE.

richness values. Certain species showed similar patterns of general abundance and richness. For example, the amphipods P. nasa (35%) and B. macromanus (11%) were dominant and showed no differences between foliose and fructicose forms. Rhodoliths are physically in contact with one another, and mobile organisms â&#x20AC;&#x201C; amphipods, copepods, polychaetes, etc. â&#x20AC;&#x201C; can disperse freely among them. This would further explain the homogeneous abundance and richness in the two growth-forms. Various studies on colonization and succession have demonstrated that, within hours, new substrata can be occupied by the above-mentioned taxa (Atilla & Fleeger, 2000; Chapman, 2002). The similar faunal abundance and richness associated with different rhodolith growth-forms suggests that thalli are highly stable against physical disturbance due to rhodolith density in the beds, independent of growth-form.

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Fig. 5. Richness of the dominant cryptofaunal taxa: comparison of two rhodolith species in the Isla Coronados bed. Means ± SE.

Associated fauna abundance did differ significantly between rhodolith species, while richness did not. Openly branched forms, such as N. trichotomum, interlock with each other more readily than densely branched plants. They present less surface area to water movement than more densely branched forms. Densely branched plants, such as L. margaritae, are likely to roll more easily and to be more resistant to breakage caused by movement than openly branched plants due to intercalary growth (Fazakerley & Guiry, 1998). Plant shape, studied by Fazakerley & Guiry (1998) in Kingstown Bay and Mannin Bay, is clearly a function of size; smaller plants are more spherical than their larger counterparts. Lithophyllum fasciculatum (Lamarck) Foslie has a more uniformly spheroidal growth form than Lithothamnion corallioides (P. L. Crouan &

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Fig. 6. Abundance of the dominant cryptofaunal taxa: comparison of two rhodolith species in the Isla Coronados bed. Means Âą SE. Crustacea were significantly more abundant (* indicates P < 0.01).

H. M. Crouan) P. L. Crouan & H. M. Crouan at both exposed and sheltered locations in Kingstown Bay (Fazakerley & Guiry, 1998). The branching patterns of L. fasciculatum radiate out from the center of the plant, with few irregular lateral branches.

Lithothamnion corallioides has a more eccentric branching habit, with many side branches and more irregular-shaped branches. The difference in branching habit has implications for the ecology of the two species because L. corallioides could be expected to interlock more readily with its nearest neighbors than L. fasciculatum, which will roll more readily (Fazakerley & Guiry, 1998). Similarly, L. margaritae is more likely to roll than N. trichotomum and this movement could prevent settlement of a higher number of species (Basso & Tomaselli, 1994). As a consequence, N. trichotomum presented a higher associated faunal abundance.

Norton & Benson (1983) found that some corals release chemical substances that prevent settlement of epiphytes and epifauna. Lithophyllum margaritae perhaps uses the same kind of mechanisms, although more studies are necessary. On the other hand,

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Fig. 7. Abundance of the dominant cryptofaunal species: comparison of two rhodolith species in the Isla Coronados bed. Means ± SE. Copepoda sp.1 was significantly more abundant (* indicates P < 0.01) in Neogoniolithon trichotomum.

N. trichotomum may release substances which facilitate invertebrate settlement, as is known in other coralline red algae (Barnes & Gonor, 1973; Morse & Morse, 1984; Pearce & Scheibling, 1990).

Kelp and coral studies showed crustaceans and molluscs to be the dominant groups, while polychaetes were less abundant (Patton, 1974; Austin et al., 1980; Tsuchiya et al., 1989; Patton, 1994). The rhodolith-associated fauna coincided with this description; however, polychaetes exhibited an important richness and abundance, possibly because rhodoliths do not secrete inhibitory substances as do corals (Norton & Benson, 1983; Hay et al., 1988). Polychaete abundance in rhodolith beds reflected the fact that these habitats are mixed with sandy bottoms, boasting polychaete abundance and richness. Steller et al. (2003) reported that echinoderms and polychaetes were the dominant group in Bahı´a Concepcio´n, contrasting with the present results. Our observations are from data collected almost 8 years after a previous study by Steller et al. (2003), suggesting that severe inter-annual changes may occur in these beds. These patterns might be pluriannual or seasonal, but more studies are required.

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Conclusions Rhodoliths provide a three-dimensional substrate in sandy bottoms and their accumulation increases habitat complexity and available colonization areas. The associated fauna community in rhodolith beds is primarily determined by the stability provided by these algae and by their branch density, and secondarily by rhodolith density. In this habitat, as in others, abiotic factors such as stochastic (wave) and periodic (tidal currents) perturbations directly affect associated macroalgae and invertebrate richness and abundance. Our analysis suggests that these factors affect both rhodolith growth-forms in the same proportion, but that the high rhodolith density here increases stability inside beds. Rhodolith species is more important than their growth-form in determining abundance and richness of the associated fauna.

Nevertheless, factors such as wave motion, depth, bioturbation and others should be considered when studying organisms associated with rhodolith beds.

Acknowledgements We would like to thank K. Cisneros, M. Lo´pez and M. Medina for help in the field. Prof. C. Maggs, Dr. M.S. Foster, M. Melia and C. Blake gave valuable comments on earlier drafts of this manuscript. Dr. Gambi and two anonymous referees made valuable comments to the final manuscript. We also thank Conabio S074 to R. Riosmena-Rodrı´quez for funding this research. G. Hinojosa wants to thank CONACYT’s scholarship (162307).

References Atilla, N. & J. W. Fleeger, 2000: Meiofaunal colonization of artificial substrates in an estuarine embayment. P.S.Z.N.: Marine Ecology, 21(1): 69–83.

Austin, A. D., S. A. Austin & P. F. Sale, 1980: Community structure of the fauna associated with the coral Pocillopora damicornis (L.) on the Great Barrier Reef, Australia. J. Mar. Freshwater Res., 31: 163– 174.

Barnes, J. R. & J. J. Gonor, 1973: The larval settling responses of the lined chiton Tonicella lineata. Mar. Biol., 20: 259–264.

Basso, D. & V. Tomaselli, 1994: Paleontological potentiality of rhodoliths: a Mediterranean case history.

In: R. Matteucci (Ed.), Studies on Ecology and Paleoecology of the Benthic Communities. Boll. Soc. Paleontol. Ital. Spec. Vol. 2: 17–27.

Bastida-Zavala, J. R., 1991: Poliquetos (Annelida: Polychaeta) del Suroeste de la Bahı´a de La Paz, B.C.S., Me´xico: Taxonomı´a y aspectos biogeogra´ficos. B.Sc. thesis, UABCS, Mexico; 145 pp.

Birkett, D. A., C. Maggs & M. J. Dring, 1998: Maerl: an overview of dynamic and sensitivity characteristics for conservation management of marine SACs. Scott. Assoc. Mar. Sci. (SAMS), 5: 1–90.

Bosence, D. W. J., 1979: Live and dead faunas from coralline algal graves, Co. Galway. Palaeontology, 22(2): 449–478.

Bruno, J. F. & M. D. Bertness, 2001: Habitat modifications and facilitation in benthic marine communities.

In: M. D. Bertness, S. D. Gaines & M. E. Hay (Eds.), Marine Community Ecology. Sinauer, Sunderland, MA: 201–218.

Brusca, R. C., 1980: Common Intertidal Invertebrates of the Gulf of California. University of Arizona Press, Tuscan, AZ; 513 pp.

120

Hinojosa-Arango & Riosmena-Rodrı´guez

Brusca, R. C., D. Perry & R. Zimmeeran, 2004: Seasonality and population dynamic of the motile invertebrates community associated with Sargassum in the Gulf of California, Mexico: the isopod crustaceans. J. Crust. Biol., in press.

Cabioch, J., 1969: Les fonds de maerls de la baie de Morlaix et leur peuplement vegetal. Cah. Biol. Mar., 10: 139–161.

Chapman, M. G., 2002: Early colonization of shallow subtidal boulders in two habitats. J. Exp. Mar. Biol.

Ecol., 275: 95–116.

Coyer, J., 1984: The invertebrate assemblage associated with the giant kelp Macrocystis pyrifera, at Santa Carolina Island, California: a general description with emphasis on amphipods, copepods, mysids, and shrimps. Fish. Bull., 82(1): 55–66.

Davis, A. N. & R. T. Wilce, 1987: Floristic, phenology, and ecology of the sublittoral marine algae in an unstable cobble habitat (Plum Cove, Cape Ann, Massachusetts, USA). Phycologia, 26(1): 23–34.

Dawson, E. Y., 1960: Symposium: the biogeography of Baja California and adjacent seas. Part II. Marine biotas. A review of ecology, distribution and affinities of benthic flora. Syst. Zool., 9: 93–100.

De Grave, S., 1999: The influence of sedimentary heterogeneity on within maerl beds differences in infaunal crustacean community. Estuarine Coastal Shelf Sci., 49: 153–163.

De Grave, S. & A. Whitaker, 1999: Benthic community re-adjustment following dredging of a muddymaerl matrix. Mar. Pollut. Bull., 38(2): 102–108.

Dearn, S. L., 1987: The faunal subtidal articulated coralline mats: composition, dynamics, and effects of spatial heterogeneity. M.Sc. thesis, SJSU, USA; 134 pp.

Fazakerley, H. & M. D. Guiry, 1998: The distributions of maerl beds around Ireland and their potential for sustainable extraction: phycology section. Report to the Marine Institute, NUI, Galway, Dublin; 34 pp.

Foster, M. S., 2001: Rhodoliths: between rocks and soft places. J. Phycol., 37: 659–667.

Foster, M. S, R. Riosmena-Rodrı´guez, D. L. Steller & W. J. Woelkerling, 1997: Living rhodolith beds in the Gulf of California and their implications for paleoenvironmental interpretation. Geol. Soc. Am. Spec. Pap., 318: 127–139.

Hall-Spencer, J. M., 1998: Conservation issues relating to maerl beds as habitats for molluscs. J. Conchol.

Spec. Publ., 2: 271–286.

Hay, M. E., P. E. Renauol & W. Fenical, 1988: Large mobile versus small sedentary herbivores and their resistance to seaweeds chemical defences. Oecologia, 75: 246–252.

Hily, C., 1989: Le me´gafaune benthique des fonds meubles de la Rade de Brest: pre´-e´chantillonnage per video sous-marine. Cah. Biol. Mar., 30: 433–454.

Hily, C., P. Potin & J. Y. Floc’h, 1992: Structure of subtidal algal assemblages on soft bottom sediments: fauna/flora interactions and role of disturbances in the Bay of Brest, France. Mar. Ecol. Prog. Ser., 85: 115–130.

Jacquotte, R., 1962: Etude des fonds des mae¨r de Me´diterrane´e. Recl Trav. Stn Mar. Endoume., 26: 141– 235.

James, D. W., 2000: Diet, movement, and covering behavior of the sea urchin Toxopneustes roseus in rhodolith beds in the Gulf of California, Me´xico. Mar. Biol., 137: 913–923.

Keegan, B. F., 1974: The macrofauna of maerl substrates on the west coast of Ireland. Cah. Biol. Mar., 15: 513–530.

Keen, B. F., 1992: Sea Shell of Tropical West America. Marine Molluscs from Baja California to Peru.

Stanford Univ. Press, Stanford, Palo Alto, CA; 1064 pp.

Lieberman, M., D. M. John & D. Lieberman, 1979: Ecology of subtidal algae on seasonally devastated cobble substrates off Ghana. Ecology, 60(6): 1151–1161.

Littler, M. M., D. S. Littler & M. D. Hanisak, 1991: Deep-water rhodolith distribution, productivity, and growth history at sites of formation and subsequent degradation. J. Exp. Mar. Biol. Ecol., 150: 163– 182.

Maggs, C. A., 1983a: A phenological study on two maerl beds in Galway Bay, Ireland. Ph.D. thesis, NUI, Galway; 346 pp.

Maggs, C. A., 1983b: A seasonal study of seaweed communities on subtidal maerl (unattached coralline algae). Prog. Underwater Sci., 9: 27–40.

Morse, A. N. C. & D. E. Morse, 1984: Recruitment and metamorphosis of Haliotis larvae induced by molecules uniquely available at the surfaces of crustose red algae. J. Exp. Mar. Biol. Ecol., 75: 191– 215.

Norton, T. A. & M. R. Benson, 1983: Ecological interactions between the brown seaweed Sargassum muticum and its associated fauna. Mar. Biol., 7: 167–177.

Nunn, J. D., 1999: The marine mollusca of Strangford Lough, Co. Down. Porcupine Newsletter, 3: 18–33.

Ojeda, F. B. & B. Santelices, 1984: Invertebrate communities in holdfast of the kelp Macrocystis pyrifera from Southern Chile. Mar. Ecol. Prog. Ser., 16: 65–73.

Rhodolith species and associated fauna

121

Patton, W. K., 1974: Community structure among the animals inhabiting the coral Pocillopora damicornis at Heron Island, Australia. Bull. Mar. Sci., 14(2): 212–243.

Patton, W. K., 1994: Distribution and ecology of animals associated with branching corals Acropora spp. from the Great Barrier Reef, Australia. Bull. Mar. Sci., 55(1): 193–211.

Pearce, C. M. & R. E. Scheibling, 1990: Induction of metamorphosis of larvae of the green sea urchin, Strongylocentrotus droebachiensis, by coralline red algae. Biol. Bull., 179: 304–311.

Reyes-Bonilla, H., R. Riosmena-Rodrı´guez & M. S. Foster, 1997: Hermatipyc corals associated to rhodolith beds in the Gulf of California, Me´xico. Pac. Sci., 157: 328–337.

Riosmena-Rodrı´guez, R., 2002: Taxonomy of the Order Corallinales (Rhodophyta) from the Gulf of California, Me´xico. La Trobe University, Melbourne; 200 pp.

Riosmena-Rodrı´guez, R., W. J. Woelkerling & M. S. Foster, 1999: Taxonomic reassessment of rhodolithforming species of Lithophyllum (Corallinales, Rhodophyta) in the Gulf of California, Mexico.

Phycologia, 38(5): 401–417.

Salazar-Vallejo, S. J., J. A. De Leo´n-Gonza´lez & H. Salice-Polaco, 1989: Poliquetos (Annelida: Polychaeta) de Me´xico. Libros Universitarios UABCS, Me´xico; 212 pp.

Sieg, J. & R. Winn, 1978: Key to suborders and families of Tanaidacea (Crustacea). Proc. Biol. Soc. Wash., 4(91): 840–846.

Sieg, J. & R. Winn, 1981: The Tanaidae (Crustacea: Tanaidacea) of California with a key to the world genera. Proc. Biol. Soc. Wash., 2(94): 315–343.

Smith, R. & J. Carlton, 1975: Light’s Manual: Intertidal Invertebrates on the Central California Coast.

University of California Press, Berkeley; 721 pp.

Steller, D. L. & M. S. Foster, 1995: Environmental factors influencing distribution and morphology of rhodoliths in Bahia Concepcion, B.C.S., Mexico. J. Exp. Mar. Biol. Ecol., 194: 201–212.

Steller, D. L., R. Riosmena-Rodrı´guez, M. S. Foster & C. Roberts, 2003: Rhodolith bed diversity in the Gulf of California: the importance of rhodolith structure and consequences of anthropogenic disturbances. Aquat. Conserv. Mar. Freshwater Ecosyst., 13: S5–S20.

Tsuchiya, M., Y. Nakasone & M. Nishihira, 1986: Community structure of coral associated invertebrates of the hermatypic coral, Pavona frondifera, in the Gulf of Thailand. Galaxea, 5: 120–140.

Tsuchiya, M., Y. Nakasone & M. Nishihira, 1989: Species composition of small animals associated with the coral Pocillopora damicornis at Sichang Islands, the Gulf of Thailand: size effect of coral colony.

Galaxea, 8: 257–269.

Tsuchiya, M. & C. Yanaha, 1992: Community organisation of associates of the scleractinian coral Pocillopora damicornis, effects of colony size and interactions among obligate symbionts. Galaxea, 11: 29–56.

Villouta, E. & B. Santelices, 1984: Estructura de la comunidad submareal de Lessonia (Phaeophyta, Laminariales) en Chile norte y central. Rev. Chil. Hist. Nat., 57: 111–122.

Wicksten, M. R., 1984: Distribution of some common decapod crustaceans and a pycnogonid from the continental-shelf of Northern California. Calif. Fish Game, 70(3): 132–139.

Williams, G. A. & R. Seed, 1992: Interaction between macrofaunal epiphytes and their host algae. In: D. M. John, S. J. Hawkins & J. H. Price (Eds.), Plant–Animal Interactions in the Marine Benthos.

Systematic Association. Claredon Press, Oxford, Special Vol. 46: 189–211.

Zar, J. H., 1996: Biostatistical Analysis. Prentice Hall, New Jersey; 121 pp.

Appendix Fauna associated with rhodolith beds in the Gulf of California.

M ¼ mean SE ¼ standard error N. t. ¼ Neogonoilithon trichotomum L. m. ¼ Lithophyllum margaritae

Family

Family

Family

PHYLUM Family

Family

PHYLUM Class Family

PHYLUM Class

Class Family

PHYLUM Class Family

PORIFERA Desmospongiae Haliclonidae Haliclona sp.

Calcarea Leucascidae Leucetta sp.1 Leucetta sp.2 CNIDARIA Anthozoa Aiptasia sp.

PLATYHELMINTHES Turbellaria Leptoplanidae Stylochoplana longipennis (Hyman, 1953) Cryptocelidae Phaenocelis mexicana (Hyman, 1953) ANNELIDA Amphinomidae Eurythoe sp.

Spionidae Polydora armata (Langerhans, 1880) Cirratulidae Caulleriella hamata (Hartman, 1948) Cirriformia sp. ¨ rsted, 1843) Dodecaceria concharum (O Phyllodocidae Eulalia bilineata (Johnston, 1840) ¨ rsted, 1843) Eumida sanguinea (O 0.05 (0.22) –

– 0.10 (0.45) 0.05 (0.22)

–

0.45 (1.10)

–

0.85 (0.93)

13.7 (11.6)

0.05 (0.22) 0.05 (0.22)

– –

0.35 (0.99) 0.05 (0.22) –

0.05 (0.22)

0.70 (1.87)

–

0.60 (1.43)

15.9 (10.6)

0.05 (0.22) 0.05 (0.22)

–

M (SE)

M (SE)

–

fructicose (n ¼ 20)

foliose (n ¼ 20)

El Requeso´n

0.05 (0.22) –

0.05 (0.22) – –

–

0.30 (0.57)

0.10 (0.45)

0.55 (0.94)

12 (13.9)

0.05 (0.22) –

0.05 (0.22)

M (SE)

foliose (n ¼ 20)

– 0.05 (0.23)

0.11 (0.46) – 0.05 (0.23)

–

–

–

0.47 (0.96)

9.84 (10.4)

– 0.05 (0.23)

–

M (SE)

fructicose (n ¼ 20)

Isla Coyote

– –

0.25 (1.12) – –

–

–

–

0.05 (0.22)

0.05 (0.22)

– 0.05 (0.22)

–

M (SE)

N. t. (n ¼ 20)

– –

– – –

–

–

–

–

–

– –

–

M (SE)

L. m. (n ¼ 20)

Isla Coronados

122 Hinojosa-Arango & Riosmena-Rodrı´guez

Family

Family

Family

Family

Family

Family

Family

Family

Polynoidae Thormora johnstoni (Kinberg, 1855) Chrysopetalidae Bhawania goodei (Webster, 1884) Syllidae Odontosyllis sp.

Exogone sp.

Branchiosyllis exilis (Gravier, 1900) Branchiosyllis sp.

Trypanosyllis (Tripanodentata) taeniaeformis (Haswell, 1866) Typosyllis sp.

Syllis sp.

Pseudosyllis sp.

Nereididae Ceratonereis singularis Treadwell, 1929 Nereis sp.

Eunicidae Eunice sp.

Eunice vittatopsis Fauchald, 1970 Lysidice ninetta Audouin & Milne-Edwards, 1833 Marphysa sp.

Nematonereis unicornis Schmarda, 1861, Palola siciliensis (Grube, 1840) Dorvilleidae Dorvillea cerasina (Ehlers, 1901) Dorvillea moniloceras (Moore, 1909) Oenonidae Oenone sp.

Terebellidae Amphitrite sp.

Eupolymnia crescentis Chamberlin, 1919 Lanice sp.

Pista sp.

Polycirrus sp.

(0.22) (0.99)

(0.22)

(0.22)

0.50 – 0.05 0.20 0.05

(0.22) (0.70) (0.22)

(0.89)

0.10 (0.31)

0.05 (0.22) 0.25 (0.70)

– – 0.05 (0.22) – 0.05 (0.22) –

0.35 (0.81) –

0.05 – – – 0.05 – 0.05 0.60

0.05 (0.22)

–

(0.82)

(0.22) (0.45)

(0.22)

0.15 (0.37) 0.05 (0.22) 0.45 (1.23) – –

–

0.05 (0.22) 0.05 (0.22)

– – 0.05 (0.22) – – –

0.30 (0.98) –

0.05 – – – 0.05 0.10 – 0.40

–

0.10 (0.45)

– – 0.10 (0.31) 0.05 (0.22) 0.05 (0.22)

0.10 (0.31)

0.10 (0.45) 0.15 (0.37)

– – – – – –

0.35 (0.88) –

– 0.05 0.22 – – – 0.10 (0.31) – 0.20 (0.52)

0.05 (0.22)

–

0.47 0.05 0.16 0.11 0.05

– (0.84) (0.23) (0.50) (0.46) (0.23)

0.11 (0.46) –

– – – 0.05 (0.23) 0.05 (0.23) 0.16 (0.50)

0.37 (0.68) 0.05 (0.23)

– – – – – 0.05 (0.23) 0.11 (0.32) 0.16 (0.50)

0.16 (0.37)

0.05 (0.23)

0.10 (0.31) – – 0.10 (0.31) –

0.15 (0.37)

– 0.15 (0.49)

0.10 (0.31) – – – – 0.05 (0.22)

0.25 (0.55) –

– – 0.15 (0.49) 0.15 (0.37) – – – 0.25 (0.72)

–

–

– – – – –

–

– –

– – – – – –

– –

–

– – – – – –

–

–

Rhodolith species and associated fauna

123

Family

Family

Class Order Family

Class Family

Order

PHYLUM Class Order

Family

Family

Sabellidae Branchiomma sp.

Potamilla reniformis (Leuckart, 1849) Serpulidae Janua sp.

Pseudovermilia occidentalis (Mclntosh, 1885) ARTHROPODA Maxillopoda Harpacticoida Copepoda sp.1 Copepoda sp.2 Copepoda sp.3 Copepoda sp.4 Copepoda sp.5 Sessilia Tetraclita sp.

Ostracoda Cylindroleberididae Cylindroleberis sp.

Malacostraca Isopoda Limnoriidae Limnoria sp.

Sphaeromatidae Paracerceis sp.

Joeropsididae Joeropsis dubia dubia (Menzies, 1951) 0.45 (1.05)

0.05 (0.22)

–

0.30 (0.92)

–

1.75 (2.61) – – – –

– –

0.10 (0.31)

–

0.05 (0.22)

–

–

– 0.05 (0.22) 2.70 (3.33) – 0.05 (0.22)

– –

– 0.10 (0.31)

M (SE)

M (SE) 0.05 (0.22) 0.15 (0.67)

fructicose (n ¼ 20)

foliose (n ¼ 20)

El Requeso´n

0.10 (0.31)

0.05 (0.22)

0.30 (0.92)

11 (11)

–

3.75 (4.09) 0.2 (0.70) 0.05 (0.22) – –

0.10 (0.31) 0.05 (0.22)

– –

M (SE)

foliose (n ¼ 20)

– –

– –

M (SE)

N. t. (n ¼ 20)

– –

– –

M (SE)

L. m. (n ¼ 20)

Isla Coronados

–

0.21 (0.54)

0.47 (1.43)

13.9 (12.8)

–

0.05 (0.22)

–

0.10 (0.45)

–

0.25 (0.43)

0.05 (0.22)

–

0.05 (0.20)

–

–

4.74 (6.92) 31.9 (26.5) 17.4 (13.2) – – 0.05 (0.22) – 0.10 (0.31) 0.60 (1.64) – 0.35 (0.67) 0.25 (0.64) – 1.45 (2.26) 0.25 (0.55)

– –

– –

M (SE)

fructicose (n ¼ 20)

Isla Coyote

124 Hinojosa-Arango & Riosmena-Rodrı´guez

Family

Family

Order Family

Suborder Family

Family

Family

Family

Family

Family

Order Suborder Family

Order

Family

Family

Family

Janiridae Ianiropsis montereyensis (Menzies, 1952) Munnidae Munna ubiquita (Menzies, 1952) Paranthuridae Califanthura squamosissima (Menzies, 1951) Tanaidacea Leptochelia dubia (Kroyer, 1842) Amphipoda Gammaridea Anamixidae Anamixis lindsleyi (Barnard, 1955) Gammaridae Elasmopus rapax Costa, 1853 Eusiridae Pontogeneia nasa Barnard, 1969 Pontogeneia sp.

Iphimediidae Iphimedia sp.1 Iphimedia sp.2 Aoridae Microdeutopus sp.

Corophiidae Bemlos macromanus Shoemaker, 1925 Caprellidea Protellidae Tritella sp.

Decapoda Xanthidae Micropanope nitida (Rathbun, 1898) Pilumnidae Pilumnus townsendi Rathbun, 1923 Diogenidae Paguristes sanguinimanus Benedict, 1901 –

0.05 (0.22)

0.60 (0.82)

0.05 (0.22)

4 (4.13)

2.70 (8.05)

0.25 (0.79) 0.4 (0.68)

22.8 (20.5) –

2.15 (5.85)

–

0.05 (0.22)

–

0.35 (1.14)

4.90 (6.13)

0.05 (0.22)

–

0.70 (0.80)

–

2.45 (2.82)

2.50 (5.39)

0.30 (0.73) 0.70 (1.59)

17.2 (13.3) –

1.30 (3.66)

–

0.05 (0.22)

0.65 (1.84)

6.55 (9.65)

–

–

0.65 (0.67)

–

13.5 (16.7)

1.95 (3.73)

0.40 (1.57) 0.25 (0.55)

– –

0.70 (1.95)

0.40 (1.27)

–

0.05 (0.22)

1 (1.56)

3.7 (4.43)

–

–

0.32 (0.58)

–

11.2 (17)

1.84 (3.40)

0.26 (0.81) 0.32 (0.95)

28.8 (36.1) –

0.63 (1.61)

0.05 (0.23)

–

0.05 (0.23)

0.32 (0.82)

2.53 (2.91)

–

–

0.55 (0.83)

–

0.35 (0.93)

0.35 (1.35)

– 0.05 (0.22)

0.60 (1.39) 0.10 (0.31)

0.05 (0.22)

–

0.15 (0.67)

0.75 (1.02)

0.15 (0.67)

0.35 (1.57)

–

–

0.75 (0.85)

–

0.75 (1.89)

0.20 (0.62)

– –

0.55 (0.83) –

0.10 (0.45)

–

–

0.10 (0.31)

–

0.05 (0.22)

Rhodolith species and associated fauna

125

Order

Order

Order

Order

Order

PHYLUM Class Order

MOLLUSCA Gastropoda Archaeogastropoda Calliostoma sp.

Tegula sp.

Arene fricki Crosse, 1865 Arene sp.

Olivia sp.

Neogastropoda Mitra sp.

Mitrella sp.

Microdaphne trichodes (Dall, 1919) Conus (Conus) nux (Broderip, 1833) Neotaenioglossa Modulus cerodes (Adams, 1851) Cerithiopsis sp.

Epitonium (Asperiscala) emydonensus (Dall, 1917) Opalia sp.

Bittium sp.

Ptenoglossa Alora gouldii (Adams, 1857) Alora sp.

Cephalaspidea Atys castus Carpenter, 1864 Retusa xystrum (Dall, 1919) Bulla sp.

Heterostropha Odostomia sp.

0.25 (0.55)

–

–

– –

0.15 (0.37) – – 0.05 (0.22) –

– – – –

0.10 (0.31)

– – –

–

0.15 (0.37) – – – –

– –

–

– –

– –

M (SE)

M (SE)

– – – – 0.05 (0.22)

fructicose (n ¼ 20)

foliose (n ¼ 20)

El Requeso´n

(0.37) (0.22) (0.37) (0.22)

0.60 (1.19)

– – 0.25 (0.72)

0.25 0.91 –

– 0.05 (0.22) – 0.10 (0.31) –

0.05 (0.22) – – –

– 0.15 0.05 0.15 0.05

M (SE)

foliose (n ¼ 20)

0.32 (1)

0.16 (0.37)

–

– 0.21 (0.92)

– 0.32 (0.82) 0.05 (0.23) – 0.05 (0.23)

– – – –

– 0.16 (0.37) – 0.05 (0.23) –

M (SE)

fructicose (n ¼ 20)

Isla Coyote

–

0.10 (0.31) 0.10 (0.31) –

–

–

–

– 0.35 (0.59)

– –

– – – 0.40 (0.68)

0.15 (0.37) –

0.05 (0.22) – – –

– 0.25 (0.55) 0.10 (0.45) – –

M (SE)

L. m. (n ¼ 20)

0.50 (0.69) –

0.15 (0.37) 0.15 (0.49) 0.05 (0.22) –

– 0.10 (0.31) – – –

M (SE)

N. t. (n ¼ 20)

Isla Coronados

126 Hinojosa-Arango & Riosmena-Rodrı´guez

PHYLUM Class

PHYLUM Class

Class

PHYLUM Class

Family

Class Family

Order

Order

Class Order

Bivalvia Mytiloida Mytella sp.

Septifer zeteki (Hertlein & Strong, 1946) Ostreoida Argopecten ventricosus (Sowerby, 1842) Veneroida Pitar sp.

Tellina sp.

Polyplacophora Ischnochitonidae Stenoplax mariposa Bartsch & Dall, 1919 Acanthochitonidae Acanthochitona avicula (Carpenter, 1864) ECHINODERMATA Stelleroidea Ophiothrix spiculata Le Conte, 1851 Ophiactis savignyi (Mu¨ller & Troschel, 1842) Echinoidea Arbacia incisa (Blainville & Gmelin) Eucidaris thouarsii (Valeciennes, 1846) CHORDATA Ascidiacea Ascidia interrupta Heller, 1878 ECTOPROCTA Gymnolaemata Bugula neritina (Linnaeus, 1758) Anexechona ancorata (Osburn, 1950) Arthropoma sp.

– – –

–

0.05 (0.22) –

0.50 (1.05) 2.90 (3.95)

0.05 (0.22)

–

– –

0.10 (0.45)

– –

– – –

0.20 (0.89)

– –

0.1 (0.45) 3.35 (4.06)

–

–

– –

–

– –

– – 0.15 (0.25)

–

– –

34.9 (39.9) 0.2 (0.4)1

–

–

0.05 (0.22) 0.20 (0.41)

–

– –

0.11 (0.32) 0.11 (0.42) –

–

– –

– 0.05 (0.23)

–

–

– 0.11 (0.46)

0.05 (0.23)

– –

– – –

–

– 0.05 (0.22)

– –

–

–

– –

–

0.85 (1.26) –

– – –

–

– –

– –

–

0.10 (0.31)

– 0.05 (0.22)

–

– –

Rhodolith species and associated fauna

127