Hydrobiologia 260/261: 121-129, 1993.A. R. O. Chapman, M. T. Brown & M. Lahaye (eds), Fourteenth International Seaweed Symposium.© 1993 Kluwer Academic Publishers. Printed in Belgium.

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Vertical distribution of coralline algae in the rocky intertidal ofnorthern Chile

Isabel Meneses C.Departamento de Biologia Marina, Universidad Cat6lica del Norte, Casilla 117, Coquimbo, Chile

Key words: Crustose corallines, vertical distribution, coralline taxa

Abstract

Studies on crustose corallines present in the intertidal region at three localities in northern Chile (30 ° S),show that these algae are well represented in exposed and protected sites, reaching up to 90% cover.Species composition differs between sites with the common occurrence of species or morphologicalvariants of Spongites and a single taxon attributed to Phymatolithon at the most exposed sites, and speciesof Lithophyllum and Titanoderma at more protected localities. The two Lithophyllum taxa recorded aredistinguished by the presence/absence of protuberances, cell size and degree of calcification, whileTitanoderma taxa are segregated by the thickness of the thallus, hypothallic and perithallic cell size andshape. Spongites taxa are distinguished on the basis of external morphology and anatomical features suchas cell size, degree of calcification and percentage of fusions between cells. The variability of thesefeatures within each species is still unknown thus, the taxa remain without specific epithet until furtherstudies. Examination of specific types recorded for nearby regions are also required in order to clarifythe taxonomy of the group in these coasts.

Introduction

Information about crustose coralline taxa forsouthern South America is restricted mainly tothe species records and descriptions based onmaterial collected by expeditions undertaken atthe beginning of the 1900s. These records includethe Antarctic Peninsula, subantarctic islands,Tierra del Fuego and Patagonia, Chilo6 andHuafo islands and the Juan Fernandez Archipel-ago (Foslie 1900, 1907a; Lemoine 1913, 1920).Foslie (1900, 1907) examined material collectedin Tierra del Fuego and Strait of Magellan de-scribing 5 species of Lithothamnion and 2 speciesof Lithophyllum. Lemoine (1913, 1920) describedin detail 4 species from Chiloe Island, one fromthe Juan Fernandez Archipelago and 3 species

from Tierra del Fuego and Patagonia. Lemoine(1920) also included 7 of Foslie's species, chang-ing Lithophyllum discoideum to her newly de-scribed genus Pseudolithophyllum. Foslie's collec-tion was later revised by Adey (1970) whochanged the generic epithet of at least 5 speciesfrom Tierra del Fuego. Finally, new changes atthe generic level have been done by Mendoza(1976a, 1976b) and Mendoza & Cabioch (1984)while working on the distribution of crustose cor-allines from Tierra del Fuego. In addition to thesestudies on material from the southern tip of SouthAmerica and scanty records of crustose corallinetaxa further north (Foslie, 1906, 1907b; Heydrich,1901), no information is available for the rest ofthe Chilean coasts.

The generic concepts in coralline algae have

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been exhaustively reexamined by several authors(for a review see Woelkerling, 1988) based uponthe revision of type specimens (Woelkerling,1983a, 1983b, 1985, 1986; Woelkerling & Irvine,1986; Woelkerling et al. 1985; Penrose, 1991).These taxonomic reassessments resulted in sev-eral changes among the species described by pre-vious authors therefore leading to the necessity ofapplying a new systematical approach to the crus-tose corallines in those regions that have not beenpreviously studied.

Considering the state of the art in crustose cor-alline taxonomy and the lack of information forthese taxa along the Chilean coasts, this studyaims to describe the taxa present at three locali-ties of northern Chile and their distribution at theintertidal region.

Materials and methods

The three study sites are Totoralillo(30 ° 6' S,71 ° 24' W), Lagunillas (30° 6' S,71 ° 24' W) and Guanaquerillos (30° 12' S,71 ° 28' W), and all are located within a distanceof approximately 50 km from each other. Twosites were chosen in each of these localities(Figs 16-18). In each site, sampling was madealong two transects parallel to the shoreline.Cover percentage of taxa was estimated by thepoint interception method with a quadrat of50 cm2. Quadrats were placed every 1 or 2 malong the transects, and the distance betweenconsecutive quadrats depended on the length ofthe intertidal at each locality.

Crustose coralline material was separated inthe field on the basis of external features such ascolor, texture, and thickness. Small thallus pieceswere sampled at each station, labelled and carriedto the laboratory in plastic bags.

Thallus pieces were examined under a Nikon(model SMZ-10) dissecting microscope and frac-tured by hand. Pieces were mounted and glued oncylindrical bronze stubs and double coated withcarbon and gold. Observations and photographswere taken with a scanning electron microscopeJEOL T-300. Photographic film used wasT-MAX 100 ASA.

Results

Description of crustose coralline taxa recorded

Representatives of four genera of crustose coral-line algae Spongites Kiltzing, Lithophyllum Phil-ippi, Titanoderma Nageli and Phymatolithon Fos-lie are present in the rocky intertidal of the threelocalities examined. The genera have been distin-guished on the basis of the classification systemgiven by Woelkerling (1988). Spongites belongs tothe subfamily Mastophoroideae and is character-ized by having uniporate tetrasporangial concep-tacles (Fig. 1), an hypothallus consisting of one ormore cell layers (Fig. 3) parallel to the substratebut not coaxial, and a thallus mainly formed bya perithallus without pit-connections but with fu-sions connecting cells of adjacent filaments(Fig. 4). Either 5 species of Spongites or 5 mor-phological variants of one or two species of thisgenus occur in the region. These five taxa differ infeatures such as presence/absence of protuber-ances, percentage of fusions, cell and degree ofcalcification (Figs 4, 5 & 6) among the perithalliccells. All specimens have a multistratified epith-allus with a subepithallic meristem (Fig. 2).Spongites is the only genus widespread among thestudy sites (Figs 16-18).

The genus Lithophyllum, which together withTitanoderma, belongs to the Lithophylloideae isrepresented by two species occurring only at To-toralillo (Fig. 16). Both species have an hypothal-lus reduced to one single basal layer of cells(Fig. 7), uniporate tetrasporangial conceptaclesand a well-developed perithallus in which no fu-sions are observed. Only secondary pit-connec-tions are detected in transverse sections of thethallus (Figs 8, 9). The two species of Lithophyl-lum not only differ in their external morphology,Lithophyllum sp. 1 has a thin crust with even sur-face and Lithophyllum sp. 2 has a thick thalluswith irregularities and protuberances in its sur-face, but also in their inner features. Perithalliccells of adjacent filaments in Lithophyllum sp. 1appear located at the same vertical level while thisis not evident in Lithophyllum sp. 2 (Figs 8, 9). Onthe other hand, Lithophyllum sp. 2 has larger per-

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Figures 1-6. Spongites taxa. Figures 7-8. Lithophyllum spp.Fig. 1. Uniporate terrasporangial conceptacle. Fig. 2. Thallus section showing round-celled epithallus (e) and subepithallicmeristem (m). Fig. 3. Multistratified hypothallus (h). Fig. 4. Perithallus (p) in Spongites sp. with thin cell walls and fusions(arrowheads). Fig. 5. Perithallus (p) in Spongites sp. 3 with heavily calcified cell walls. Fig. 6. Perithallus (p) of vertically elon-gated cells in Spongites sp. 2. Fig. 7. Hypothallic (h) basal layer in Lithophyllum sp. 2. Fig. 8. Banded perithallus (p) with sec-ondary pit-connections (arrowheads).Fig. 1 scale = 50 Im, Figs. 2-4, 7, 8 scale = 10 pm, Figs. 5, 6 scale = 5 Jm.

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Figures 9, 10. Lithophyllum spp. Figures 11-13. Titanoderma sp. Figures 14, 15. Phymatolithon sp.Fig. 9. Banded perithallus (p) showing abundant secondary pit-connections (arrowheads). Fig. 10. Thin cell-walled perithallus(p) and epithallus (e). Fig. 11. Palisade-like cells of hypothallus (h), with secondary pit-connections (arrowheads) in

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TOTORALILLO

Titanodrrnma sp

Spongites sp3100 _ _ Lithophyllum spl

_ _ Lithophyllum sp 2

Crustose corallines

-11 48CORALLINA SP

HILDENBRANDIA SP

PROFILE

0 2 4 6 8 10 12 14 16mSEA4-

0 2 4 6 8 io 12m

Fig. 16. Vertical distribution and abundance (expressed as cover percentage) of crustose coralline taxa in the locality of Totoralillo.Lower section shows non-crustose coralline taxa and total crustose coralline taxa, upper section shows crustose corallines sep-arated into taxa.

ithallic cells, less calcified cell walls and second-ary pit-connections are less frequent than in Li-thophyllum sp. 1 (Fig. 10).

The only species of Titanoderma was collectedat Totoralillo (Fig. 16), and is distinctive by anhypothallus of elongate, obliquely oriented, pali-sade-like cells (Fig. 11), perithallic cells of adja-cent filaments at the same vertical level (Fig. 12)joined by secondary pit-connections (Fig. 11) andan unistratified epithallus (Fig. 13).

The last taxon recorded is a species attributedto the genus Phymatolithon although further infor-mation is required to be certain of this identifica-tion. This species has multiporate tetrasporangialconceptacles (Fig. 14), a non-coaxial hypothallus(Fig. 15) and only occasional fusions present(Fig. 15) between cells of adjacent filaments.

Distribution and abundance of crustose corallinetaxa in each the localities studied

Totorallillo is the most protected amongst thesites studied and consists of a long and extendedintertidal region. Crustose corallines are presentall along the 16 and 13 m of the transects sampled(Fig. 16) at the two sites. In general, geniculatecorallines and Hildenbrandia sp. are the mostabundant taxa at this locality. Crustose corallinesnever reach abundances higher than 40% in thequadrats closest to the ocean, and include twospecies of Lithophyllum, one of Titanoderma andone of Spongites. These taxa occur in both siteswith Lithophyllum sp. 2 restricted to the high in-tertidal in site A and Spongites sp. 3 restricted tothe low intertidal in site B (Fig. 16).

O- 0-

GELIDIUM SP

perithallus (p). Fig. 12. Banded perithallus (p). Fig. 13. Unstratified epithallus (e). Fig. 14. Multiporate tetrasporangial concep-tacle (pores = p). Fig. 15. Multistratified hypothallus (h) with fusions (arrowheads).Figs 9-13 scale = 10 #m, Fig. 14 scale = 50 pm, Fig. 15 scale = 20 pm.

_ _

v T

____ �__ I I

- - -

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Lagunillas can be characterized as beingsemiexposed to wave action. Here, the intertidalregion is shorter extending for no longer than13 m. Different sites within the same locality arevariable in the distribution and composition ofcrustose corallines (Fig. 17). Only Spongites isrepresented in this locality. Crustose corallines asa group are more abundant here than in Totora-lillo, reaching up to 90% cover in site A. Twospecies of Spongites alternate between the sites.

Finally Guanaquerillos is an exposed localityin which the intertidal region is highly reduced(10 m in site A and 5 m in site B). Three taxa ofSpongites and one of Phymatolithon are the rep-resentatives of crustose corallines at this locality,where they reach up to 80% in cover. Phymatoli-thon sp. is restricted to a low percentage in coverin site B (Fig. 18).

Discussion

Clearly the crustose coralline entity until now re-ferred to as 'Lithothamnia' for the coasts of Chile

(Guiler, 1959; Stephenson & Stephenson, 1972,Alveal & Romo, 1977) is a complex assemblageof taxa with a high variability in its compositiondepending on the characteristics of each locality.Although representatives of this group occur inthe three sites studied, their patterns of distribu-tion and relative abundance vary between sites.Exposure to wave action seems to be a factorinfluencing the taxa composition and abundance.The Lithophylloideae (Lithophyllum and Titano-derma) are found in protected and flat areas suchas the intertidal of Totoralillo, while specimens ofSpongites and Phymatolithon appear in higherabundance and frequency in exposed or semi-exposed areas like Lagunillas and Guanaqueril-los. This taxa partitioning of the habitats has alsobeen observed in calcareous crustose algae fromTierra del Fuego (Mendoza, 1988). Mendoza(1988) points out that Clathromorphum obtectulum(Foslie) Adey and Hydrolithon falcklandicum(Foslie) Mendoza appear mainly in the low in-tertidal while Clathromorphum lemoineanum Men-doza et Cabioch and Hydrolithon consociatum(Foslie) Mendoza occur in the low subtidal.

LAGUNILLASJuveniles

Spongites sp3

_ -4 Spongites sp2Spongites spl

Crustose corallines

-W LESSONIA

4 CODIUM

MONTEMARIA

PROFILE

12 10 8 6 4 2 Om 12 1 8 6 4 2 Om-SEA

Fig. 17. Vertical distribution and abundance (expressed as cover percentage) of crustose coralline taxa in the locality of Lagunillas.Lower section shows non-crustose coralline taxa and total crustose coralline taxa, upper section shows corallines separated intotaxa.

01%

__

L --0000Il

ANIft

GUANAQUERILLOSPhymatolithon sp

Spongites sp 5

Spongites sp4

Spongites spl

Crustose corallines

GELIDIUM

14 _,

8 6 4 2 Om 4 3 2 1 Om

HI LDENBRANDIA

PROFILE

e SEA

Fig. 18. Vertical distribution and abundance (expressed as cover percentage of crustose coralline taxa in the locality of guanaque-rillos). Lower section shows non-crustose coralline taxa and total crustose coralline taxa, upper section shows crustose corallinesseparated into taxa.

Furthermore, crustose coralline taxa at Totora-lillo seem to have a relatively uniform distributionand similar abundances along the entire length ofthe transects. This could reflect the homogeneityof the habitat, a flat zone of small boulders withscattered areas of coarse sand along approxi-mately 20 m.

The genus Spongites is taxonomically complex,recently Hydrolithon Foslie (1909), PorolithonFoslie (1909) and Pseudolithophyllum sensu Adey(1970) were included under its circumscription(Penrose & Woelkerling, 1988). This resolutionwas taken considering that trichocyte arrange-ment and occurrence, hypothallus structure (un-istratified versus multistratified) and cell size arecharacters too variable to distinguish among thesegenera. However, observations based on the tet-rasporangial conceptacle development of the typespecies of Hydrolithon, Porolithon and Spongites(Penrose & Woelkerling, 1992) indicate that thefirst two genera share the presence at the porecanal of a ring of elongate cells oriented more orless perpendicularly to the roof surface, these cellsarise from filaments interspersed amongst spo-rangial initials and do not protrude into the canal.

In Spongites the ring of cells is oriented more orless parallel to the roof surface, protrudes into thecanal and arises from peripheral roof filaments(Penrose & Woelkerling, 1992). These two pat-terns are considered to provide a basis for genericsegregation therefore, further observations basedon different developmental stages of tetrasporan-gial conceptacles are required to assign, with cer-tainty, the taxa observed in this study to Spong-ites.

Since the variability of characters such as ex-ternal morphology, cell size, degree of calcifica-tion and others is unknown in crustose corallinesfrom the coasts of Chile, the taxa attributed toSpongites in this study will remain unidentifieduntil further information is available. In the mean-time, five taxa are recognized within this genusbut these could be either different species or mor-phological variants of one or two species. Mor-phological variability is well documented in crus-tose corallines, external morphology changes inLithophyllum congestum (Steneck & Adey, 1976)depending on the exposure to water movementand this could be the case for the different taxaattributed to Spongites in this study. Differences

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128

between Spongites sp. 5 and the rest of the taxacould represent a morphological variability due tomicrohabitat conditions. However, the presenceat the same tidal level and locality of Spongitessp. 5 and other two taxa of Spongites suggests thisis not the case.

There are five species that could be attributedto Lithophyllum according to the genus diagnos-tic characters reported for the Chilean coasts.One of them is Lithophyllum (Dermatolithon) con-spectum Foslie which belongs to the genus Titan-oderma according to Lemoine's description (1913)and to the revision of the generic concepts doneby Woelkerling et al. (1985). This species alsocited by Mendoza (1988) for Tierra del Fuegoprobably corresponds to our material. Among theother four species, Lithophyllum skottsbergii Lem-oine, L. fetum Foslie, L. fernandezianum Lemoineand L. almanense Lemoine, the two latter havea poorly developed hypothallus consisting ofa single basal layer of cells not clearly distin-guished from the epithallial cells according toLemoine (1920) and may correspond to materialrecorded in this study. Nevertheless, no assump-tions can be made before examining type speci-mens.

The recognition of a taxon belonging to thegenus Phymatolithon has to be regarded with cau-tion. The type species Phymatolithon calcareum(Pallas) Adey & McKibbin (1970) has been re-corded from Tierra del Fuego (Hariot 1895) asLithothamnion (See Woelkerling, 1988), althoughthis record requires verification. Phymatolithon issimilar to Clathromorphum Foslie but differs in theposition of cell elongation (behind or within veg-etative initials) and the adventitious or subepith-allic origin of conceptacle primordia which arenot known for the Chilean material.

Acknowledgements

I would like to give my special thanks to PedroToledo for his technical assistance with the SEMwork, to Alonso Vega for his assistance in thefield, and to Erika Fonck for her support andgrant of the facilities used during this study. Funds

were provided by the Direcci6n General de In-vestigaci6n of the Universidad Cat6lica del Norte.

References

Adey, W. H., 1970. A revision of the Foslie crustose corallineherbarium. K. norske Vidensk. Selsk. Skr. 1970: 1-46.

Adey, W. H. & D. McKibbin, 1970. Studies on the maerlspecies Phymatolithon calcareum (Pallas) nov. comb. andLithothamnion corallioides Crouan in the Ria de Vigo. Bot.Mar. 13: 100-106.

Alveal, K. & H. Romo, 1977. Consideraciones sobre la dis-tribucion vertical de la biota costera. Fundamentos para unnuevo esquema de zonaci6n. Bol. Soc. Biol. Concepci6n51: 25-39.

Foslie, M. 1900. Calcareous algae from Fuegia. Wissensch.Ergebn. Schwed. Exped. Magell., 1895-1897. Botanik, 3:65-75.

Foslie, M. 1906. Algologiske Notiser II. K. norske Vidensk.Selsk. Skr. 1906: 1-28.

Foslie, M. 1907a. Antarctic and Subantarctic Corallinaceae.Wissensch. Ergebn. Schwed. S1dpolar Exped. 1901-1903Bd. IV.: 1-16.

Foslie, M., 1907b. Algologiske Notiser III. K. norske Vidensk.Selsk. Skr. 1907: 1-26.

Foslie, M. 1909. Algologiske Notiser VI. K. norske Vidensk.Selsk. Skr. 1909: 1-63.

Guiler, E. R. 1959. Intertidal belt-forming species on the rockycoasts of Northern Chile. Pap. Proc. Roy. Soc. Tasmania93: 165-183.

Hariot, P., 1895. Nouvelle contribution a l'tude des algues dela region magellanique. J. Bot., Paris 9: 95-99.

Heydrich, F. 1901. Die Lithothamnien des Museum d'HistoireNaturelle in Paris. Bot. Jb. 28: 529-545.

Lemoine, P. 1913. Melobesiees. In: Deuxieme Expedition Ant-arctique Francaise (1908-1910). (eds. Masson et Cie.),Paris, 67 pp.

Lemoine, P., 1920. Les Melobesiees. In: Botanische Ergeb-nisse der Schwedischen Expedition nach Patagonien undder Feuerlande 1907-1909. Kungl. Svensk. Vetenskapa-kad. Hand. Bd. 4: 1-17.

Mendoza, M. L. 1976a. Antarcticophyllum, nuevo gnero paralas Corallinaceae. Bol. Soc. Argentina Bot. 17: 252-261.

Mendoza, M. L. 1976b. Presencia del gnero Pseudolithophyl-lum (Corallinaceae) en Argentina. Centro de Investigaci6nde Biologia Marina, Contr. 140: 1-9.

Mendoza, M. L. 1988a. Consideraciones biol6gicas y bio-geograficas de las Corallinaceae (Rhodophyta) de las costasde la Isla Grande de Tierra del Fuego. Gayana, Bot. 45:163-171.

Mendoza, M. L. & J. Cabioch, 1984. Redefinition comparede deux especes de corallinac6es d'Argentine: Pseudolitho-phyllum fuegianum (Heydrich) comb. nov. et Hydrolithon

129

discoideum (Foslie) comb. nov. Cryptogamie: Algologie 4:141-154.

Penrose, D., 1991. Spongites fruticulosus (Corallinaceae,Rhodophyta), the type species of Spongites, in southernAustralia. Phycologia 30: 438-448.

Penrose, D. & Wm. J. Woelkerling, 1988. A taxonomic reas-sessment of Hydrolithon Foslie, Porolithon Foslie andPseudolithophyllum Lemoine (Corallinaceae, Rhodophyta)and their relationships to Spongites Kiltzing. Phycologia 27:159-176.

Penrose, D. & Wm. J. Woelkerling, 1992. A reappraisal ofHydrolithon and its relationship to Spongites (Corallinaceae,Rhodophyta). Phycologia 31: 81-88.

Steneck, R. S. & W. H. Adey, 1976. The role of environmentin control of morphology in Lithophyllum congestum, a Car-ibbean algal ridge builder. Bot. Mar. 19: 197-215.

Stephenson, T. A. & A. Stephenson, 1972. Life between tidemarks on rocky shores. Freeman, W. H. & Comp., SanFrancisco, 425 pp.

Woelkerling, Wm. J. 1983a. A taxonomic reassessment ofLithothamnium (Corallinaceae, Rhodophyta) based onstudies of R. A. Philippi's original collection. Br. Phycol. J.18: 165-197.

Woelkerling, Wm. J., 1983b. A taxonomic reassessment ofLithophyllum (Corallinaceae, Rhodophyta) based on studiesof R. A. Philippi's original collection. Br. Phycol. J. 18:299-328.

Woelkerling, Wm. J., 1985. A taxonomic reassessment ofSpongites (Corallinaceae, Rhodophyta) based on studies ofKiltzing's original collection Br. Phycol. J. 20: 123-153.

Woelkerling, Wm. J., 1986. The genus Litholepis (Corallinace-ae, Rhodophyta): taxonomic status and disposition. Phy-cologia 25: 253-261.

Woelkerling, Wm. J. 1988. The Coralline Red Algae: An anal-ysis of the Genera and Subfamilies of Non-geniculate Cor-allinaceae. Oxford University Press, Oxford and BritishMuseum (Natural History), London, xi + 268 pp.

Woelkerling, Wm. J. & L. M. Irvine, 1986. The typificationand status of Phymatolithon (Corallinaceae, Rhodophyta).Br. phycol. J. 21: 55-80.

Woelkerling, Wm. J., Chamberlain, 1. M. & P. C. Silva, 1985.A taxonomic and nomenclatural reassessment of Tenarea,Titanoderma and Dermatolithon (Corallinaceae, Rhodo-phyta) based on studies of type and other critical speci-mens. Phycologia 24: 317-337.