Revista Chilena de Historia Natural 73:585-603, 2000

Disjoint geographical distribution of intertidal and nearshore benthic invertebrates in the Southern Hemisphere

Distribuciones geognificas disyuntas de invertebrados bent6nicos intermareales y del submareal somero en el Hemisferio Sur

JUAN C. CASTILLA' & RICARDO GUINEZ

Departamento de Ecologfa. Facultad de Ciencias Biologicas. Pontificia Universidad Catolica de Chile Casilla 114-D, Santiago, C.P. 6513677, Chile, 1 e-mail: [email protected]

ABSTRACT

Biogeographical explanations for the extant and pal eo disjoint geographical distribution in the southern hemisphere of five species of nearshore marine benthic invertebrates: Gaimardia trapesina, Ostrea chilensis, Pyura stolonifera taxonomic complex, Aulacomya ater and Concholepas concholepas, showing distinctive reproductive strategies and early life history characteristics are reviewed and analyzed. Through the use of published and new information we contrasted the following hypotheses: a) vicariance-historical process, b) epiplanktonic larval dispersal, c) juvenile/adult dispersal through rafting and d) planned or accidental anthropogenic dispersal mechanisms. The juvenile/adult transoceanic dispersal hypothesis by rafting was the only one impossible to be rejected for the species analyzed. The implication and future direction for research in this area are discussed.

Key words: paleobiogeography, vicariance, larval dispersal, rafting, anthropogenic dispersal, bivalves, gastropods, tunicates, invertebrates, nearshore, southern hemisphere.

RESUMEN

Se revisa y analiza !as posibles explicaciones para la distribucion geogn'ifica disyunta, presente y pasada, en el hemisferio sur de cinco especies de invertebrados bentonicos marinos litorales: Gaimardia trapesina, Ostrea chilensis, el complejo taxonomico Pyura stolonifera, Aulacomya atery Concholepas concholepas, con estrategias reproductivas y caracterfsticas de historia de vida distintas. Se discute y pone a prueba, usando informacion original o publicada, !as siguientes hipotesis: a) procesos historicos de vicarianza, b) dispersion de larvas epi-planctonicas, c) dispersion de juveniles o adultos por transporte pasivo y d) dispersion antropogenica planificada o accidental. La hipotesis de dispersion transoceanica de juveniles o adultos fue la única imposible de rechazar para !as especies analizadas. Se discute !as direcciones futuras de investigacion en esta área.

Palabras clave: biogeografia, paleobiogeografia, vicarianza, dispersion larvaria, transporte, dispersion antropogenica, bivalvos, gastropodos, tunicados, invertebrados, litoral, hemisferio sur.

INTRODUCTION environments of less than ea. 100 m of depth). The hypotheses for the southern hemispheric A taxon's geographical distribution is the result geographical distribution of benthic nearshore from a combination of historic, regional and local invertebrates fall into 4 main categories: (H 1) the processes, ecological interactions and accidental vicariance-historical hypothesis, contenting that or planned introductions (Knox 1980, Ruiz et al. the disjoint geographical distributions of NSBI 1997, Lindberg 1991, Castilla et al. in press). The may be the result of ancient continuous deep ocean that separates South America from distributions following the break-up of South Africa, New Zealand and Australia Gondwanaland (late Mesozoic) and posterior, but represents a major barrier for the dispersal of concurrent, paleoceanographic changes (Knox sessile or slow mobile nearshore marine benthic 1980, Zinsmeister 1982, Kott 1985); (H2) the invertebrates (NSBI= those found in rocky oceanic epiplanktonic larval dispersal hypothesis, intertidal and/or shallow subtidal inshore contenting that larval dispersal had occurred via 586 CASTILLA & GUINEZ the southern hemisphere oceanic circulation of Pyura stolonifera (Helier, 1878) taxonomic com- water masses generated by Coriolis forces, and plex (see Kott 1997, 1998), showing external the west-wind-drift and moving oceanic water fertilization and a larvae with a short free-swim- masses predominantly westward (Fell 1962, ming planktonic period (few hours); ( 4) the ribbed Orensanz 1990, 6 Foighil et al. 1999); (H3) the mussel Aulacomya ater (Molina, 1872), showing oceanic dispersal of juveniles or adults hypothesis, external fertilization and larvae with long free- contending that the dispersal of individuals swimming planktonic period (several weeks), and occurred via rafting; e.g., the transport of sessile (5) the gastropod muricid "loco" Concholepas or sedentary juvenile or adult stages of an organism concholepas (Bruguiere, 1789), showing internal on a drifting object or transporting agents, such as fertilization (copulation) and a larvae with a long kelps, logs, seagrasses or pumice (Scheltema 1977, free-swimming planktonic period (several J okiel1984, 1989, High smith 1985, J ackson 1986, months). For each of them we discuss the most 6 Foighil 1989, Worcester1994); and (H4) the plausible hypotheses to explain their extant and planned or accidental anthropogenic dispersal paleo geographical distribution. hypothesis, such of those occurring via aquaculture, ship fouling (Monniot & Monniot 1994) or ballast sea water (Car!ton & Geller 1993 ). MATERIAL AND METHODS Five elements, independent or combined, have been used in the hypotheses testing of NSBI dis- The geographical distribution of the species joint paleo and/or extant biogeographic distribu- analyzed and suggestions for the routes and tion of this part of the world: (1) evidence of plate mechanisms of dispersal are based on published tectonic and paleoceanographic changes occurred information. For the brooding bivalve, G. over time in the southern hemisphere; (2) trapesina, we used information from Ojeda & paleobiological reconstruction; (3) phylogenetic Santelices (1984 ), Zinsmeister (1984 ), Cas till a relationship of the taxa investigated; ( 4) the (1985) and the work ofHelmuth et al. (1994) for knowledge on the life history of the species in- evidences on long distance dispersal kelp-rafting. volved, particularly the extension of larval stages; For the Chilean oyster, 0. chilensis, we followed and (5) the genetic structure (particularly mo- papers referring to characteristics of the larvae lecular genetics) of local populations, which may (Chanley & Dinamani 1980, DiSalvo et al. 1983 ), provide independent evidence for genetic bounda- genetic work (Buroker et al. 1983, 6 Foighil et al. ries, temporal frameworks for species divergence, 1999), and particularly the work of Foighil et al. phylogenetic reconstruction and information on ( 1999) that uses paleobiological, phylogenetic geography of allelic variants within species analyses and archaeological information to (Palumbi 1996). address the contenting hypotheses. For the In this paper we analyzed the biogeographical southern hemisphere P. stolonifera taxonomic quest presented by a selected group of southern complex we followed Kott' s (1997, 1998) hemisphere NSBI invertebrate species that show interpretation. Additionally, we discussed their transoceanic geographical distributions and dis- larval life history (Clarke et al. 1999), tinctive reproductive strategies and early life his- phylogenetic analysis of DNA sequences and tory characteristics, and argue about dispersal/ derived PAU trees for the South African, transport mechanisms. As it has been suggested Australian and Chilean populations (Castilla et by several authors, it is expected a positive rela- al. unpublished data). Summaries for the specific tionships between the length of planktonic larval methods used (i.e. tunicate DNA sequencing) are time and geographic distribution; thus, a species included within the species analysis. For the ribbed with short, or no planktonic stage, is supposed to mussel, A. ater, we followed Osorio & Bahamonde have a small geographic range, while a long plank- (1968), Cancino & Becerra (1978), Ojeda & tonic phase may promote a wider distribution Santelices (1984 ), Zinsmeister (1984 ), Cas till a range (Mileikovsky 1971, Scheltema 1978, 1986a, (1985), Suchanek (1986), Erkon Schuring & Crisp 1978, Jablonski 1986; but see Johannesson Griffiths ( 1990) and Crame ( 1999). For the muricid 1988). C. concholepas we incorporated recent published We selected the following species: (1) information about their paleogeographical Gaimardia trapesina (Lamarck, 1819), a small distribution (De Vries 1995, Vermeij 1998). For bivalve showing internal fertilization and brood- extant populations of C. concholepas we discuss ing strategy; (2) the Chilean oyster Ostrea the characteristics of its reproduction and chilensis (Philippi, 1845), showing external ferti- planktonic larvae (DiSalvo 1988, DiSalvo & lization and retention of the larvae inside the Carriker 1994), growth, ecology, genetic mantle cavity of the adult; (3) ascidians of the differentiation of populations in central and DISJOINT GEOGRAPHICAL DISTRIBUTION OF MARINE INVERTEBRATES 587 northern Chile and archaeological findings and the later approximately 2,000 km west from (Castilla & Jerez 1986, Jerardino et al. 1992, Cape Horn. Additionally, the Kerguelen Islands Guifiez efal. 1992, Castilla 1999). are approximately 3,500 km from the nearest continental landmass, making it one of the most isolated places on Earth (Blott et al. 1988). Also, RESULTS AND DISCUSSION other species with direct development has been found in isolated islands (e.g., Easter Island, the Gaimardia trapesina (Lamarck, 1819): a brooder Juan Fernandez Islands, and Kerguelen Island) at species with no free-living larval stage higher proportion than usual (McDowall 1968) Vicariance (H1) and epiplanktonic larval dis- Present disjoint biogeographical distribution: G. persal (H2) hypotheses: G. trapesina lacks a free- trapesina exhibits a wide geographic distribution living larval stage, therefore the epiplanktonic (Fig. 1) throughout the Scotia Arc, including larval dispersal hypothesis could be discarded. Cape Horn, Falkland Islands, South Georgia, However, it is possible that founding of isolated South Sandwich Islands, Crozet Island, Marion island populations may have occurred through Island and the Kerguelen Islands (Fell 1962, Dell dispersal of larvae with an extended plankto- 1964, Ralph & Maxwell1977, Blankey & Grindley trophic phase (pelagic development) from the 1985, Thiriot-Quievreux et al. 1988, Helmuth et original populations, provided that this develop- at. 1994, Linse 1999). The species broods its mental mode was loss afterwards in both young and has no free-living larval stage (Thiriot- populations. Prior to 1984 the oldest record for Quievreux et al. 1988). Therefore, according to Gaimardia was from the late Pleistocene of New the larval dispersal hypothesis it is no expected to Zealand. Nevertheless, Zinsmeister (1984) re- find Gaimardia populations with so wide· and ported the presence of Gaimardia flemingi, that disjoint distribution: i.e. the Falkland Islands resembles G. trapesina, in the upper Eocene at La which are located approximately 1,300 km east- Meseta Formation, Seymour Island from the Ant- northwest of the Antarctic island South Georgia, arctic Peninsula. He suggested that Gaimardia

Gaimardia trapesina

• • Fig. 1. Southern hemisphere extant disjoint geographical distribution of the bivalve Gaimardia trapesina (see stippled areas). Distribuci6n geografica disyunta de !as poblaciones actuales del bivalvo Gaimardia trapesina en el hemisferio sur (ver areas achuradas). 588 CASTILLA & GUINEZ

originated in the southern hemisphere around (1976) suggested that 0. lutaria [according to Antarctica during the Paleogene (Paleocene- Buroker et al. (1983) was wrongly referred as 0. Oligocene). Further, it has been argued that dur- angasi (Sowerby, 1871)] and 0. chilensis were ing the late Miocene, at the beginning of mark- closely related species. Chanley & Dinamani edly cooler conditions, species moved northward ( 1980) compared the larval characters of ostreid into lower latitudes (Zinsmeister & Feldman species around the world and found that 0. 1984 ). Thus the vicariance hypothesis and/or the chilensis and 0. lutaria differed from all other independent evolution of a common development ostreids and proposed the creation of a new genus, mode may explain the present pattern of geo- Tiostrea, including two species: Tiostrea chilensis graphic distribution exhibited by Gaimardia and Tiostrea lutaria. However, Buroker et al. trapesina. (1983) using protein-gel electrophoresis found The juvenile/adult dispersal (H3) and anthro- that both taxa were different geographical pogenic dispersal (H4) hypotheses: Helmuth et populations of a single species. Harry (1985) al. ( 1994) presented evidence of long-distance extended the classification of the living species (approximately 1,300 to 2,000 km) dispersal for of oysters beyond that proposed by Stenzel ( 1979) this brooding bivalve in the Southern Ocean: and divided the genus Ostrea (Ostreidae, Cape Horn, the Falkland Islands, and South Geor- Ostreinae, Tribe Ostreini) into two subgenera: gia. G. trapesina is a common component of kelp- Ostrea s.s. and Eostrea Ihering, 1907. He proposed bed communities (Dell 1964, Ralph & Maxwell that Eostrea have a single species: Ostrea 1977, Ojeda & Santelices 1984, Castilla 1985). (Eostrea) puelchana Orbigny, 1841, including as Therefore, it is possible that the species might be junior synonyms the following: Tiostrea Chanley transported offshore via kelp-rafting. In fact, and Dinamani, 1980, Ostrea lutaria Hutton, 1873, Helmuth et al. (1994 ), on a cruise between South Ostrea chilensis Philippi, 1845, Ostrea angasi Georgia and Punta Arenas, Chile, made observa- Sowerby, 1871 and Ostrea algoe.nsis Sowerby, tions and collections of 43 kelps from three rafts. 1871. Harry (1985) suggested that 0. puelchana The rafts were made almost entirely of individual is a circumglobal species, extending between 35o plants of Macrocystis pyrifera and the relative and 50°S latitude, including coasts of South abundance of G. trapesina on kelp stipe was America, southern New Zealand, southern Aus- highly variable, showing no significant trend with tralia, and South Africa. Additionally, Carriker et distance from South America. The authors also al. (1994) proposed 0. puelchana as a synonym found that G. trapesina bivalves were able to for 0. chilensis. According to Toro (1995) the survive transport across distances between South taxonomic status of these oysters is still obscure, Georgia and South America, maintaining brooded particularly because neither the proposition of young during this time. The authors suggested Harry (1985) nor that of Carriker et al. (1994) that dispersal by rafting can occur over geologi- have considered the presence of significant cal and ecological time scales and could poten- differences in the reproductive biology among tially serve as a significant way of genetic ex- them (Fernandez Castro 1988, Toro & Chaparro changes between populations. The adult dispersal 1990, Pascual et al. 1992, Toro 1995). hypothesis (H3) and the vicariance hypothesis Consequently, in this paper we follow Toro ( 1995) (H 1) cannot be discarded even when the Scotia and continue referring to the Chilean oyster as Arc, the Falkland Islands, South Georgia, Marion Ostrea chilensis: a species showing a disjoint Island and the Kerguelen Islands were probably distribution spanning New Zealand and Chile (Fig. completely covered by ice between the late 2). Miocene and the Early Pliocene (Knox 1980, In New Zealand, 0. chilensis is found through- Graft I 994). out the nearshore including the Chathman Is- lands, between 34° and 47°S of latitude (Buroker et al. 1983, Jeffs & Creese 1996). The main popu- Ostrea chilensis: a brooding species with short- lation of 0. chilensis in New Zealand is present in lived planktonic larvae Foveaux Strait, in the South Island, and supports a valuable dredge fishery (Cranfield & Michael Present disjoint biogeographical distribution: The 1989). In Chile, the distribution of the species classification of the New Zealand dredge oyster shows a restricted geographical range between, Ostrea lutaria (Hutton, 1873) and the Chilean 41 o and 4 7° S of latitude, but is found mainly oyster Ostrea chilensis (Philippi, 1845) is between 41 o to 42°, from shallow waters down to controversial. Wakamatsu (1975) described 0. depths of approximately llm (Buroker et al. 1983, chilensis as occurring along the West Coast of Winter et al. 1984, Guifiez & Galleguillos 1985, South America and around New Zealand. Korringa Toro 1995). The main beds are located in Gulf of DISJOINT GEOGRAPHICAL DISTRIBUTION OF MARINE INVERTEBRATES 589

Quetalmahue and Guaitecas Islands (Solfs 1967, isoenzymes and mitochondrial DNA does not sup- Winter et al. 1984, Guifiez & Galleguillos 1985, port the vicariance hypothesis. Buroker et al. Toro & Chaparro 1990). The Chilean oyster popu- (1983) compared the genetic structure of oysters lation within its northern range has sustained an from New Zealand and Chile and concluded, on important fishery, but has also suffered st(ong the basis on 29 structural loci, that both taxa were declines due to overfishing (i.e. Pullinque bed: almost indistinguishable. They suggested that the Toro & Chaparro 1990). Presently the Chilean Chilean and New Zealand oysters represent oyster production is sustained mainly through disjoint geographical populations of the same oysterculture (Lepez 1984, Toro & Chaparro species. The same conclusion was reached by 6 1990). Foighil et al. (1999), using 609 nucleotide frag- The prevailing hypotheses accounting for the ment of the cytochrome oxidase I (COl) mtDNA 0. chilensis disjoint biogeographical distribution gen. They found a difference of four nucleotide have been recently discussed and scrutinized by substitutions between samples from the North 6 Foighil et al. (1999) and encompass the four Island (New Zealand) and Chiloe island (Chile), types of hypotheses defined by us in the Introduc- implying a 0.6% sequence divergence. tion. In conclusion, fossil and genetic information The vicariance-historical hypothesis (H1): It allows concluding that the hypothesis of may be expected that both Chilean and New Zea- vicariance through a Gondwanaland connection land oyster populations are Gondwanaland rel- does not explain the trans-Pacific disjoint distri- icts. The species has been documented for the bution of the Chilean and New Zealand oysters. New Zealand Pliocene (Beu & Maxwe111990) but The evidence suggests that the New Zealand oys- fossil oysters from pre-Holocene Chilean strata ter population is the ancestral one (6 Foighil et al. are unknown (Herm 1969, 6 Foighil et al. 1999). 1999). Other hypotheses must be used to explain Therefore, it is possible that the species does not the present geographical distribution. belong to the Gondwanaland fragmentation The oceanic epiplanktonic larval dispersal hy- (Weissel & Hayes 1977). The fossil and genetic pothesis (H2): The Chilean oyster broods its lar- evidence information obtained through vae within the mantle cavity for approximately 8

Ostrea chilensis

..

Fig. 2. Southern hemisphere extant disjoint geographical distribution of the bivalve Ostrea chilensis (see stippled areas). The arrow indicates the Chiloe island, Chile. Distribuci6n geognifica disyunta de las poblaciones actuales del bivalvo Ostrea chilensis en el hemisferio sur (ver areas achuradas). La flecha indica la isla de Chiloe, Chile. 590 CASTILLA & GUINEZ

weeks, longer than any other oyster species. The Rafting has been suggested as the most probable veligers are not lecitothrophic, but remove in- explanation for the present disjoint trans-Pacific gested particles suspended in the mantle cavity of distribution of the Chilean oyster (Buroker et al. the mother. The larvae are released at a very 1983, 6 Foighil et al. 1999). In fact, given that advanced stage of development (approximately hypotheses H1, H2 and H4 have been rejected as >450 IJlll diameter) and settle within a few hours plausible explanations for the disjoint present (DiSalvo et al. 1983, Winter et al. 1984, Toro & distribution of the Chilean oyster, the conclusion Chaparro 1990, Chaparro et al. 1993). Therefore, of 6 Foighil et al. ( 1999), is that dispersal by the oceanic larval dispersal hypothesis cannot be rafting is by far the most likely explanation. They called for. However, 6 Foighil et al. (1999) dis- suggested that pumice may have served as the cussed a possible variant of this hypothesis: the subscase for transport. It is known that pumice Chilean population may have been established have been released by repeated eruptions of the from New Zealand via the transoceanic dispersal New Zealand North Island Taupo Volcanic Zone of larvae with extended planktotrophic pelagic since the Pliocene (Wilson et al. 1986, 6 Foighil development, with a posterior and independent et al. 1999). loss of this developmental mode in both populations. 6 Foighil et al. (1999) examined a juvenile fossil folding from New Zealand (late Pyura stolonifera taxonomic complex of species: Pliocene strata, 1.6-2.0 mya) through scanning larvae with a short free-swimming planktonic electron micrographs ofprodissoconch and found period that their structure is identical to that of modern specimens. This suggests that the species had Present disjoint biogeographical distribution: fully evolved the present day larval development Large barrel-shaped filter-feeding tunicates, such prior to the Pleistocene. In Chile, there is no as Pyura species, are found as dominant rocky fossil evidence of this species from the Pliocene/ intertidal and shallow water organisms exclusively Pleistocene (Herm 1969, 6 Foighil et al. 1999). along the shores of South Africa, Australia and Radiocarbon techniques giving an age estimates Chile (Fig 3). So far, the taxonomic nomenclature (95 % confidence intervals) of 953-1,238 and of these taxa is confounded and the phylogeny is 2,998-3,383 years before the present (y BP) have not well understood (but see below). According dated the first subfossils found in Chile. The to Kott (1997) the following subspecies may be juvenile fossils preserved had the present larval distinguished: (1) P. stolonifera stolonifera (=P. development (6 Foighil et al. 1999). The stolonifera Helier, 1878) (see Day 1974, Fielding phylogenetic parsimony search of COl including et al. 1994), known inS. Africa as "red bait" and the South and North Islands of New Zealand and present in the lower intertidal rocky shore fringe Chiloe island (Chile) indicated that the New Zea- and shallow subtidal, along several1,000's of km land North Island and Chilean samples belong to of coastline, from Cape Town to Natal; (2) P. sister lineages with the New Zealand South Island stolonifera praeputialis (= P. praeputialis Helier, branching off earlier. This implies an additional 1878) (see Fairweather 1991 ), known in Australia restriction to the variant hypothesis of loss of the as "cunjevoy" and present in the mid and low extended pelagic larval period, since it would intertidal rocky shore fringes and shallow subtidal require three independent homoplasies after the along several 1,000's of km of coastline, in New respective branching of the N. Zealand South South Wales, Victoria and Tasmania; (3) P. Island, North Island and (pre-Pleistocene and post- stolonifera bradleyi (= P. bradleyi Van Name, trans-Pacific colonization) Chilean lineages (6 1931) ( =P. praeputialis Hell er, 1878; see Paine & Foighil et al. 1999). The evidence and arguments Suchanek 1983, Castilla 1997a, Clarke et al. 1999), discussed preclude the oceanic larval dispersal known in Chile as "piure de Antofagasta" and hypothesis (H2). present in the mid and low rocky intertidal fringes Oceanic dispersal of juvenile or adult (H3) and and shallow subtidal exclusively inside the Bay anthropogenic dispersal (H4) hypotheses: The of Antofagasta Chile, along approximately 70 km evidence discussed above suggests that the founder of coast (Clarke et al. 1999, Castilla et al. 2000). oyster population in Chile occurred at least 2,000 P. bradleyi (Van Name, 1931) was collected only y BP and originated from N. Zealand North Is- once, in 1931, in Zorritos, northern Peru. Since land. It is known that the first human settlement then, the species has not been collected. Two in New Zealand occurred unequivocally about expeditions to Peru aiming specifically to 950 y BP (McGlone et al. 1994 ). Then, the anthro- Zorritos' site, have not succeeded to locate the pogenic oyster introduction or dispersal hypoth- species (see Clarke et al. 1999). Recently, Kott esis can be discarded (6 Foighil et al. 1999). (1998) has suggested that species in the Pyura DISJOINT GEOGRAPHICAL DISTRIBUTION OF MARINE INVERTEBRATES 591 stolonifera complex from South Africa, Australia (MacDonald 1859) (Molgulidae) andAsterocarpa and Chile are conspecific, returning to her previous humilis (Helier 1878) (Styelidae) (Clarke & opinion (Kott 1985). Castilla 2000) all collected in Antofagasta (Chile). The vicariance (H 1) hypothesis: Tunicates, in J.C. Castilla did field collections in all sites with spite of the hard tunicin protein-like of their the exception of Cape Town, where Prof. G. tunic, do not fossilize well. In the case of this Branch collected tunicates. complex of subspecies there is not known fossil A summary of the methodology used for the record. The prevailing hypothesis accounting for tunicate's sequence of COl mitochondrial genes their disjoint biogeographical distribution, spe- is the following: double-stranded products for the cially between the Australian and Chilean pyurid COl mitochondrial gene were amplified via PCR populations, was suggested by Kott (1985). The using primers from Folmer et al. (1994). They author proposed that the Chilean Pyura were cycle-sequenced using the Thermo populations may be a Gondwanaland species rel- Sequenase Dye Terminator Cycle Sequencing Pre- ict, remaining since the late Mesozoic, when the mix Kit (Amersham). Sequences were generated Australian and South African Pyura populations from electrophenograms using ABI Prism RRR diverged (Kott 1985). In order to test the taxa 377 software and analyzed with Sequence Navi- status and phylogenetic relationships between the gator RRR (ABI). Each amplified mtDNA prod- southern hemisphere Pyura stolonifera complex uct was sequenced in both directions and com- (Castilla et al., unpublished data), DNA was pared by overlap to assure accuracy. COl were extracted from either gill-sac or siphon tissue of translated to aminoacids, based on the mitochon- P. stolonifera collected from Botany Bay (Sydney, drial code for invertebrates, with ascidians ex- Australia), from the Bay of Antofagasta (Chile) ceptions (Yokobori et al.1993 ), via Mac Vector and from Cape Town (South Africa). As outgroup, RRR (IBI) and aligned by eye. Additionally, the the authors analyzed subtidal individuals of Pyura COl sequence of a pyurid species Halocynthia chilensis (Molina 1872) (Pyuridae), Molgulaficus roretzi was available from Gen Bank (ace. N°

Pyura stolonifera taxonomic complex

Fig. 3. Southern hemisphere extant disjoint geographical distribution of the tunicate Pyura stolonifera taxonomic complex (see stippled areas and taxonomical discussion in the text). The arrow indicates the Bay of Antofagasta, Chile. Distribuci6n geognifica disyunta de !as poblaciones actuales del complejo de especies del tunicado Pyura stolonifera en el hemisferio sur (ver areas achuradas y discusi6n taxon6mica en el texto). La flecha indica la Bahfa de Antofagasta, Chile. 592 CASTILLA & GUINEZ

S54796). The resulting data matrix for analyses that given the extensive range of geographical totaled a length of 588 bases for 11 individuals/ distribution of P. praeputialis in Australia and taxa. The data were analyzed using PAUP* 4.0 the extremely restricted one in Chile, the (Swofford 1998). Tree searches were conducted Australian population is more likely to be the with optimality criteria of parsimony, maximum ancestral stock. It appears plausible that the "piure likelihood, and minimum evolution(= 1,000 rep- of Antofagasta" represents a population of Pyura licates). The degree of transition: transversion praeputialis, introduced from Australia and not a bias was estimated using maximum likelihood. Gondwanaland relict. Parsimony searches were done with and without The larval dispersal hypothesis (H2): Clarke et transversion bias corrections by differential al. ( 1999) published information on the reproduc- weighing. Maximum likelihood searching, with tion, early embryology, larval development and 10 replicates, for optimal trees with simultaneous metamorphosis for P. stolonifera from estimation of the T-ratio (= 3.01), gamma shape Antofagasta. In the laboratory the mean active parameter ( = 0,305), the shape of the distribution free-swimming period for the tadpole larvae (rang- of substitution rates across the COl sequences ing from 1080 to 1380 mm) was of 2:35 h (SD= were done. A Bremer's node (Bremer 1988, 1994) 0:59 h). This period was similar to what Anderson on the consensus ten most parsimonious et al. (1975) reported for the active free-swim- phylogenetic trees was applied. ming tadpole larvae of P. stolonifera from Aus- For the phylogenetic analysis, we calculated, tralia: 1:00-2:00. Griffiths ( 1976) reported that (Castilla et al., unpublished data) a distance for P. stolonifera from South Africa the tadpole matrix for the COl sequence data yielded the free-swimming period lasted "few hours". The following results: (1) the P. stolonifera COl short-lived larval phase of this taxonomic com- sequence from the Australian specimen differed plex of Pyura species does not support the hy- from those of the Chilean specimens by 0.34%, pothesis of an oceanic large-scale epiplanktonic 0.51 %, 0.68%, and 1.03%, respectively; (2) none larval dispersal through drifting and thereby oce- of the 4 Chilean P. stolonifera specimens had anic interchanges between the disjoint identical sequences and the variation ranged be- populations. tween 0.17% and 1.03%; (3) a much greater dif- The juvenile/adult dispersal hypothesis (H3) ference in COl sequences, 18.81%, was observed and anthropogenic dispersal hypotheses (H4 ): between P. stolonifera from Australia and P. Monniot & Bittar (1983), Monniot (1994), stolonifera from South Africa; and ( 4) a similar Monniot & Monniot 1994 and Clarke et al. ( 1999) difference. in COl sequences, ranging between have suggested that the Chilean population of P. 18.81 and 18.82%, was observed between P. stolonifera may have been recently introduced to stolonifera from Chile and P. stolonifera from the Bay of Antofagasta, via accidental anthropo- South Africa. Other results were: ( 1) the two COl genic or non-anthropogenic dispersal agents (i.e. sequences for M. ficus were identical, and they ships' fouling, drifting objects). In fact, the re- differed from the other COl species sequences sults of the molecular genetic data discussed above between 36.78 and 39.69%; (2) the COl sequence suggests that the hypotheses of oceanic dispersal for H. roretzi differed from the other COl se- of adults, via rafting (H3), or the accidental an- quences between 24.35 and 37.59%; (3) the COl thropogenic (i.e. ship's fouling) dispersal hy- sequence for A. humilis differed from the other potheses (H4) are both likely. We don't have COl sequences between 22.76 and 38.63%; and evidence to reject either. ( 4) the COl sequence for P. chilensis differed from the other COl sequences between 23.26 and 37.98%. Aulacomya ater: a species with a long free- We demonstrated, (Castilla et al., unpublished swimming planktonic larvae period data) a very close genetic similarities between the P. stolonifera from Australia and P. stolonifera Trans-Atlantic disjoint distribution: The ribbed from Chile (of the same order of magnitude than mussel, Aulacomya ater, is widespread (Fig. 4) those found in Chilean intrapopulations), and on both Atlantic and Pacific coasts of South conversely large genetic differences between them America, from El Callao (Peru) to Estrecho de and P. stolonifera from South Africa. Therefore, Magallanes (Chile), from southern Brazil to Tie- we propose to keep the specific name of Pyura rra del Fuego (Argentina), the Falkland Islands, praeputialis for the Australian and Chilean pyurid and the Kerguelen Islands (Soot-Ryen 1955, 1959, populations and Pyura stolonifera for the South Lozada 1968, Osorio & Bahamonde 1968, Cancino African pyurids. According to these results, and & Becerra 1978, Suchanek 1986, Linse 1999). observed genetic distances, the authors suggested Also, the species is found in the Atlantic coast of DISJOINT GEOGRAPHICAL DISTRIBUTION OF MARINE INVERTEBRATES 593

Africa, from Rocky Points in northern Namibia to the larval dispersal hypothesis (H2) can be con- Port Alfred in the southeastern coast (van Erkom sidered as a possible explanation for the disjoint Shuring & Griffiths 1990). geographical distribution of the species. The vicariance (Hl) and the anthropogenic dis- The ribbed mussel is usually found as a common persal (H4) hypotheses: Fossil for A. ater in South component of nearshore kelp-bed communities America and South Africa shores are known from and algae holdfasts in central Chile, subantarctic Pleistocene deposits (at least 2 million years ago) and Antarctic waters (Ojeda & Santelices 1984, but not from the Pliocene deposits (Herm 1969, V asquez & Santelices 1984, Castilla 1985) and Pether 1997). However, the genera Aulacomya, South Africa (van Erkom Shuring & Griffiths represented by fossils of Aulacomya anderssoni 1990). So, it is possible that juveniles or adults of (Zinsmeister 1984, Stilwell & Zinsmeister 1992) the species could also be dispersed by kelp-rafting. were reported from the late Eocene (approxi- Therefore, the vicariance hypothesis (H1), and/or mately 42-33 mya) from La Meseta Formation the juvenile (H2) or adult hypothesis (H3) are (Antarctic Peninsula). A. anderssoni is also known plausible explanations for the present disjoint from the late Eocene-early Oligocene from the distribution of the species. The anthropogenic San Julian Formation, Patagonia (Crame 1999). related hypotheses can be discarded as This suggests that the genera originated in the explanations for the present disjoint distribution southern hemisphere, around Antarctic, during of A. ater. the Paleogene, and therefore, a vicariance expla- nation (H1) cannot be rule out. However, the above allows us to reject the anthropogenic dis- Concholepas concholepas: a species with a long- persal hypothesis (H4 ). lived pelagic and planktotrophic larvae The larval (H2) and the juvenile/adult dispersal (H3) hypotheses: As most of mussels, A. ater Present, paleobiogeographical distributions and larvae are expected to spend two to four weeks in the vicariance hypothesis (H1): The present the free-swimming planktotrophic stage geographical distribution of the "loco" C. (Ramorino & Campos 1983, Suchanek 1986), so concholepas (Gastropoda: Muricidae), the only

Aulacomya ater

Fig. 4. Southern hemisphere extant disjoint geographical distribution of the bivalve Aulacomya ater (see stippled areas). Distribuci6n geognifica disyunta de !as poblaciones actuales del bivalvo Aulacomya ater en el hemisferio sur (ver areas achuradas). 594 CASTILLA & GUINEZ

living species in the genus, is restricted to South early Miocene, Chipola formation, Florida, North America, from Islas Lobos de Afuera in Peru, 6° America); (2) E. deshayesi Rambur, I862 (= 27' S (Sanchez Romero 1973) to Cape Horn, Concholepas deshayesi: Helvetian, from the Chile, and in the Juan'Fernandez Islands (Stuardo middle Miocene, Touraine, France); (3) E. I979) (Fig. 5). DeVries (1995) published antiquata Tate, I894 ( =Concholepas antiquata: information showing that there are 4 South Balcombian, from the middle Miocene, Victoria, American fossil species in the genus Concholepas Australia) and ( 4) E. pehuensis ( = Lippistes Lamarck, 180 I, extending from the middle pehuensis Marwick, I926: Tongaporutuan, from Miocene up to the Holocene: (I) C. ungis De Vries, the late Miocene, Nort Taranaki, New Zealand). 1995 (middle Miocene, from Lomitas, Peru); (2) In our opinion, the taxonomic and phylogenetic C. kieneri Hupe, I854 (late Miocene to Pliocene, problems described for the genera Concholepas from Peru and Chile); (3) C. nodosa Moricke, and Edithais complex have not yet been solved I896 (middle and late Pliocene, from Peru and (see Discussion below). Nevertheless, in this pa- Chile) and ( 4) C. concholepas (Bruguiere, I789) per we follow DeVries ( 1995) and Vermeij (I998) (Quaternary, in the Pleistocene and Holocene, preliminary conclusions. In doing so, it appears from South Africa, Peru and Chile). The author that the fossil complex of species of Edithais suggested that the South American and South have been found in the southern hemisphere in African species of Concholepas should be New Zealand (E. pehuensis, in the late Miocene) considered an endemic lineage and that 4 extra and approximately during the middle Miocene, in non-South American species originally referred Australia (E. deshayasi); in France (E. deshayesi) to Concholepas (i.e. Beu I970, Yokes I972) are and in Florida (E. drezi), and also around the not closely related taxa. On the other hand, middle Miocene. So far, no explanation about this Vermeij (1998) described Edithais as a sister rather odd paleobiogeographical distribution of genus of Concholepas Lamarck, I80 I, for the 4 Edithais species has been offered. Nevertheless, non-South American Cenozoic fossils of muricids, such odd paleo-biogeographical distributions are designating Concholepas drezi Yokes, I972 as not uncommon. For example, fossil relatives to the type species. The four Edithais species listed extant species of the genus Lyreidus de Haan, by Vermeij (1998) are: (1) Edithais drezi, Yokes, I839 (Crustacea, Decapoda, Ranididae), with 1972 (=Concholepas drezi: Burdiglian, from the western North Atlantic and Indo-West Pacific

Concholepas concholepas

Fig. 5. Southern hemisphere extant disjoint geographical distribution of the gastropod Cone holepas concholepas (see stippled areas and discussion in the text). The arrow indicates the presence of Pleistocene and Holoce'ne fossils of C. concholepas in South Africa. Distribuci6n geogr:ifica disyunta de las poblaciones actuales del gastr6podo Concholepas concholepas en el hemisferio sur (ver areas achuradas y discusi6n en el texto). La flecha muestra la presencia de f6siles de C. concholepas en el Pleistoceno y Holoceno en Sud Africa. DISJOINT GEOGRAPHICAL DISTRIBUTION OF MARINE INVERTEBRATES 595

distribution, can be traced as relict from Miocene ing on the capsule size. Hatching time ranged related species showing an Atlantic-Tethyan dis- between 36-128 days (Gallardo 1973, Castilla & tributional pattern, and from related species from Cancino 1976). Spontaneously eclosed C. the late Eocene in the southern hemisphere (see concholepas veliger larvae cultured in laboratory Fig 14, Feldmann 1992). conditions, fed on monospecific cultures of On the other hand, the South American microalgae, grow from an initial protoconch shell Concholepas complex of species appears to con- length of approximately 250 mm to near 1700 mm form an endemic lineage of fossils: C. ungis > C. in 111-124 days (DiSalvo 1988). According to kieneri > C. nodosa > C. concholepas in sites of DiSalvo & Carriker (1994 )'s laboratory experi- Peru and Chile, from the middle Miocene up to ments the metamorphosis of competent C. the Holocene (DeVries 1995). Nevertheless, dur- concholepas larvae is slow and the modification ing the late Pleistocene and Holocene C. of its veliger behavior, from along-lived natatorial concholepas fossils showed a notorious disjoint independent planktonic stage, to a benthic slow paleobiogeographic distribution in the southern crawling, shell-boring carnivore individual, can hemisphere, represented by fossils found in Peru- be delayed for hours, days or weeks before a Chile and West South Africa-Namibia (Kensley suitable settling site is identified and the teleconch 1985, De Vries 1995). According to Kensley starts to form. On the contrary, our own experi- ( 1985) the South African C. concholepas fossils ence (laboratory conditions) with competent C. are indistinguishable from those in South America. concholepas veligers collected from the plankton (J.C. Castilla examined the set of 5 South African in central Chile (P. Manrfquez personal comm.) Concholepas fossils, deposited in the South Afri- indicates that competent larvae collected from can Museum, Cape Town and agrees with Kensley, the superficial plankton (once the protoconch of 1985). Furthermore, the South Africa fossil shells the larva reaches approximately 1,800-1,900 mm do not differ from the approximately 8,000-9,000 ) readily settles within minutes to a few hours in years archeological shell midden excavated C. presence of settlement surfaces such as glass, concholepas, from central Chile (Jerardino et al. plastic, mussel and loco's shells, granitic rock or 1992). on substratum offered at the water surface. Labo- Kensley ( 1985) suggested that the Concholepas ratory cultures indicate that after 3-month period South African fossils represented a chance short- juveniles of C. concholepas reach 10-20 mm maxi- lived pioneer population, probably established mum diameter of the peristome (DiSalvo 1988). via larvae drifting from South America, follow- Undoubtedly, after several months of free-swim- ing the West Wind Drift (see Shannon et all989, ming planktonic life, and with the possibility of a Schafer & Krauss 1995, Florenchie & Verron delay in the metamorphosis and settlement (see 1998, Stutzer & Krauss 1998 and Stramma & above), this species is a c.andidate to advocate England 1999 for main oceanic drifting direc- larval dispersal through planktonic drifting in the tions between the southern tip of South America southern hemisphere (i.e. Kensley 1985, Pether and South Africa). However, this seems problem- 1997). Nevertheless, taking into account: (a) the atic as the Benguela current it is not a continua- characteristics of the planktonic larvae of C. tion of the West Wind Drift, but it is separated by concholepas, (b) the predominant surface oce- the well marked Subtropical Convergence. Nev- anic circulation in the area and (c) the unlikeness ertheless, Shannon et al. (1989) has suggested that the South African-Namibian fossils repre- that perturbations occurring in the Subtropical sent a relict population of the late Cretaceous that Convergence are likely to be important for the included the west and south-west coasts of the transfer of biota between the Southern and Atlan- separating masses of South America and Africa tic oceans. In any case, according to present knowl- (Kensley 1985), it appears odd that so far only 2 edge the vicariance Gondwanaland explanation fossil records of C. concholepas have been lo- for the amphiatlantic disjointed biogeographical cated in South Africa (-and none for the 3 South distribution of this species must be rejected. American former middle and late Miocene The epiplanktonic larval dispersal (H2) and the Concholepas paleo-species-). Probably juvenile/adult dispersal (H3) hypotheses: C. Concholepas larvae drifting along the West Wind concholepas shows internal fertilization (copula- Drift could not be the only (and/or the most tion); females cement egg capsules to rocky important) mechanism for dispersal of extant or substrates year-round, with two peaks: January/ paleo populations of the loco. This view would February and May/July (Castilla 1979). Labora- contradict the prevailing hypothesis about the tory observations indicate that the number of mechanisms behind the disjoint paleogeographical larvae inside the capsules (no nutritious eggs distribution of C. concholepas in the southern present) varies between 600 and 14,000, depend- hemisphere. We feel that such a mechanism for 596 CASTILLA & GUINEZ dispersal should include not only the larvae char- represent a case(s) of rare event of juvenile/ acteristics of the species, but also the potential adult group of Cone holepas arriving to the western for adult/juvenile dispersal through drifting agents African coast via some consolidated drifting sub- and the biological characteristics of the snail strata. The scarcity of Concholepas fossils re- such as its trophic ecology. ported from South West Africa-Namibia shores, The biology and the trophic ecology of C. which presents rich oceanographic upwelling char- cone holepas was reviewed by" Castilla ( 1982, acteristics similar to those of the Humboldt Cur- 1988, 1997b ). Cas till a ( 1999) summarized the rent System in Chile and Peru, suggests that the ecological role of species such as the loco in the arrival of Concholepas to that continent may rep- rocky intertidal of central Chile. The species is a resent a rare/unusual dispersal event. The other carnivore, limpet-like, slow moving muricid, prey- possibility is that there is not enough pal eo exca- ing predominantly on mussels, barnacles and vations in the west coast of South Africa. Never- ascidians (DuBois et al. 1980). In its early life theless, this is unlikely since the African coast stages (less than approximately 20 mm) C. from which Concholepas fossils were discov- concholepas is a shell-boring species (Mendez & ered, is extensively known from its paleo record Cancino 1982). Later on develops more efficient due to diamond mining operations (Kensley prey-attacking behavioral strategies (Castilla et 1985). al.1979). Laboratory and field observations indi- cate that for Concholepas to perform successfully any of its prey-attacking strategies, the individual GENERAL DISCUSSION AND FUTURE DIRECTION needs to be strongly attached to the substratum (Castilla et al. 1979). Therefore, from the trophic With reference to the southern hemisphere extant point of view Concholepas differs substantially and pal eo biogeographical disjoint distribution of from the filter feeders (bivalves and tunicates) the 5 species discussed: (a) the vicariance (Hl) analyzed in this paper. hypothesis can be almost completely discarded Hereby we suggest that Concholepas larvae for 0. chilensis, Pyura stolonifera taxonomic drifting via the West Wind Drift might not be an complex and Concholepas concholepas .. This is efficient dispersal agent, as could be the case for no so for G. trapesina and A. ater. (b) The the mytilid A. ater. Otherwise, we don't see the epiplanktonic larval hypothesis (H2) appears as a reason why more fossil or present species of likely explanation for A. ater and less so for C. Concholepas have not been found in the West concholepas. (c) The juvenile/adult dispersal hy- Coast of Africa, as for example it is the case of A. potheses (H3) by rafting, alone or in conjunction ater. Instead, we suggest that Concholepas egg with other hypotheses, can not be rejected for the capsules may raft by themselves or that adult or 5 species analyzed and (d) the anthropogenic juvenile Concholepas specimens may be rafted dispersal hypothesis (H4) is hereby rejected for on solid/consolidated substrates, such as the 0. chilensis, A. ater and C. concholepas. holdfast of kelps. Nevertheless, these dispersal Vicariance hypothesis (Hl): The southern ori- mechanisms make the transoceanic crossing be- gin of G. trapesina and A. ater, associated to the tween the tip of South America and Africa less evolution of the Antarctic continent, has been likely (Nelson 1994). There are evidences for the well documented in the literature (see Zinsmeister recruitment and establishment of juvenile and 1984 ). Previous to the discover of the occurrence adult Concholepas, mussels, barnacles and of both genera in the upper Eocene at La Me seta ascidians inside the holdfast of the South Ameri- Formation, Seymour Island (Antarctic Peninsula), can kelp Lessonia nigrescens (Cancino & the oldest known occurrences were from the late Santelices 1981, 1984, V asquez & Santelices Pleistocene of New Zealand (Gaimardia) and 1984 ). Newly settled individuals of Concholepas South America and South Africa shores (A. ater). inside these holdfasts encounter a permanent solid This lead to Fleming (1963) to suggest that some substrate and abundant prey items (mussels, bar- Neoaustral taxa (southern Pacific taxa that first nacles, ascidians, crabs etc). If this is so, C. appear along the southern circum-Pacific during concholepas may be kelp-rafted throughout the late Neogene) originated from tropical or Lessonia or others macroalgae across oceanic subtropical stocks, that during the late Neogene routes (but see Nelson 1994). Furthermore, we entered the southern oceans from Australasia, suggest that there exist the possibility that the South Africa, or South America. According to fo~sils of C. concholepas excavated in South West this author these immigrants were then distrib- Africa-Namibia shores may not represent a short- uted around the southern hemisphere by the West lived pioneer population, started from larvae trans- Wind Drift . However, the Eocene occurrence of ported from Chilean waters, but that they may Gaimardia, Aulacomya and other bivalves DISJOINT GEOGRAPHICAL DISTRIBUTION OF MARINE INVERTEBRATES 597

(Gomphina and Eurhomalia) around Antarctic belongs to a species with direct development or demonstrates that these taxa originated around which produces very short-lived planktonic lar- the Antarctic and suggests that not all Neoaustral vae, the low mobility of all life-stages will main- taxa followed the Flemming's proposition. On tain the population within a restricted area so that the contrary, according to Zinsmeister & Feldman mates will be likely to encounter each other. The ( 1984) and Zinsmeister ( 1984 ), derived Neoautral opposite may occur to a species with long-lived taxa originated in the Antarctic moved northward planktonic larvae, such as C. concholepas. This into the lower latitudes during the late Miocene, can be considered as an alternative explanation at the onset of markedly cooler conditions in the for the reduced success of a C. concholepas southern hemisphere (Neogene) and eventually founder populations across the southern oceans. dispersed along the West Wind Drift. Thus, the Rafting is an alternative dispersal mechanism actual geographical distribution pattern exhib- potentially available for species without or with ited by Gaimardia and Aulacomya may reflect a reduced larval development time, which has been complex history of vicariance, geographical range proposed as more effective (lOOs to 1,000s of shifts and dispersal events. km) than planktonic larval development (Jokiel Epiplanktonic larval (H2) vs. juvenile/adult 1984, 1989, Highsmith 1985, Jackson 1986, dispersal (H3) hypothesis: The disjoint biogeo- Johannesson 1988, 6 Foighil 1989, 6 Foighil et graphical transoceanic distribution is the com- al. 1999). Fell (1962) using inferential evidence mon characteristics of the five selected species, based on species of benthic echinoderms showing which present different development strategies, southern circumpolar ranges, proposed that indi- ranging from strictly brooder (G. trapesina) to a viduals adhered to macroalgae might complete several months long-lived free-swimming plank- trans-Pacific oceanic d i' persal by means of the tonic veliger (C. concholepas). This permits to Antarctic Circumpolar West Wind Drift, moving postulate that the transoceanic disjoint distribu- unidirectionally from west to east. This mecha- tion is not only determined by the larval dispersal nism has also been suggested to explain the capacity as expected (Mileikovsky 1971, eunicemorph polychaete annelids distribution in Scheltema 1978, 1986a, Crisp 1978, Jablonski Antarctic and subantarctics areas (Orensanz 1990), 1986), but also other mechanisms must be consid- and for 0. chilensis thought the northern deflec- ered. tion of the West-Wind Drift along the coast of The planktonic larval has been generally as- Chile, known as the Humboldt Current (Buroker sumed to cause most of the dispersal of these et al. 1983) . Rafting by macroalgae (kelp rafting) organisms; such larvae can be routinely trans- has been shown to occur in Gaimardia trapesina ported over 1Os to 1 ,OOOs of kilometers during (Helmuth et al. 1994 ). The authors suggested that their pelagic development (Crisp 1958, 6 Foighil this mechanism probably accounts for the wide- 1989), and are even capable of transoceanic dis- spread distribution of the species. As G. trapesina persal (Scheltema 1971, Pechenik et al. 1984). is found in rafts and also associated to kelp-beds For instance, among central Pacific islands it has and kelp holdfast (Castilla 1985), also other spe- been proposed that the colonization has been cies associated to kelp beds may be subjected to accomplished by means of planktonic larval dis- kelp rafting. According to our field experience, persal (using information from 210 plankton tows we predict that in the southern Atlantic it may be collected over a period of 26 years, between 1953 possible to discover juvenile/adult specimens of and 1979; Scheltema 1986b ). A comparable col- A. ater and C. concholepas being rafted by kelps lecting effort is lacking in the southern hemi- holdfast of Durvillaea antarctica or Macrocystis sphere. On the other hand, it has been proposed pyrifera (Ojeda & Santelices 1984, Castilla 1985). that species with planktotrophic larvae have The rafting via L. nigrescens probably is not as greater geographic range (for a review, see 6 likely as via Durvillea or Macrocystis, because Foighil 1989), but this prediction does not ex- the Lessonia 's plants have solid non-buoyant plain the disjoint transoceanic distribution of at blades and stipes (Nelson 1994 ). Nevertheless, least three of the five selected species: G. according to the time elapsed for drifting kelps to trapesina, 0. chilensis and P. praeputialis, nor become negatively buoyant (particularly in open other species (Jokiel 1984, 1989, Jackson 1986, ocean situations, see Edgard 1987) we also pre- Johannesson 1988, Safriel & Hadfield 1988, 6 dict that those probabilities will increase between Foighil 1989). Johannesson (1988) discussed the relatively short coastal-oceanic distances within decreasing density effects that mortality and dif- the southern tip of South America (i.e. between fusion can produce on larvae with extended plank- the Beagle Channel or the Magellan Strait and the tonic larvae period, able to cross-oceans. Further- Falkland Islands), and that they will decrease more, the author argued that if the founder group over extensive open oceanic routes.lt might be an 598 CASTILLA & GUINEZ

extremely unlike event for a drifting kelp to cross munities (Carlton 1987). Among the major mecha- the oceanic distance separating the southern tip nism for this kind of dispersal are shipping (foul- of South America and the South West coast of ing and ballast water) and the transportation of South Africa, particularly for a carnivore species. commercial shellfish and fish. Tunicates are This may also explain the scarcity of founder among the species of invertebrate which are most populations and fossils of Concholepas reported readily transported by ships as fouling organisms for the west coast of Africa-Namibia. Since the (Monniot & Bitar 1983, Carlton 1987, Monniot & present populations of C. concholepas are abun- Monniot 1994) or in ballast sea water (water taken dant in Chile, and A. ater in Chile and Argentina, in a port and released on ports of call, Carlton & future analysis on kelp drifting associated inver- Geller 1993 ). Both dispersal agents may explain, tebrate fauna in the high latitudes of the southern through the species invasion mechanism, the par- Atlantic ocean may help to enlighten cases as the ticular disjoint and odd geographical distribution above. Dispersion by infrequent chance rafting of P. praeputialis in Australia (along 1,000's of events have been suggested for the occurrence of km of coast) and in Antofagasta, Chile (along South African and Indian late Miocene fossil taxa only 70 km of coast; Clarke et al. 1999, Castilla et of the Genera Bullia (Gastropoda: Nassariidae) al. 2000). 6 Foighil et al. (1999) suggested that (Allmon 1990) and also for the occurrence of careful analysis of Chilean taxa with reduced or subfossil shells of three locally extinct molluscs: absents pelagic larval development, including Tawera philomela, Sassia philomelae and ascidians, may reveal additional cryptic rafted Pareuthria fuse ata, with Subantarctic affinities, immigrants from New Zealand. found in the Benguela region off southwestern Africa (Pether 1993 ). Rafting on pumice was suggested by 6 Foighil FUTURE DIRECTIONS et al. ( 1999) as the more probable dispersal mecha- nism for the trans-Pacific range extension of 0. We have shown the utility of incorporating tech- chilensis. According to Jokiel (1989) major pum- niques of molecular genetics in the study of ma- ice rafting episodes frequently result from vol- rine populations, which may provide evidence for canic eruptions, so volcanism continually injects temporal frameworks for species divergence, and large volumes of floating pumice in the ocean phylogenetic reconstruction (see 0. chilensis and basins. We think that the broader significance of P. stolonijera taxonomic complex sections). We pumice as an invertebrate transoceanic transport propose that the incorporation of this kind of mechanism has been overlooked. For example, resear~h is needed no only to advance in the pumice from the 1962 submarine eruption (see phylogenetic relationships and systematic of the Fig. 4 from J okiel 1989) in the South Sandwich species analyzed here, but also. in the genetic Islands drifted to southern Australia shores, to structure of donors and receiver populations. New Zealand, South America and Africa and prob- According to studies in progress in our labora- ably dispersed over the entire world ocean. How- tory the taxonomic and evolutionary problem of ever, we do not have direct evidence for tunicates Concholepas and Edithais as reported by De Vries (P. praeputialis), oysters (0. chilensis) nor the (1995) and Vermeij (1998), has not yet been other species analyzed in this paper, being found solved. For instance, along the geographical gra- on pumice. Furthermore, related drifting mecha- dient of extant C. concholepas (more than 7,000 nism could be linked to other natural drifting km of coast line and oceanic islands) there is materials, such as driftwood, charcoal, seeds ( co- much more morphological variation than what conut, cycad, mangrove) and heavily fouled float- DeVries (1995) and Vermeij (1998) used to arrive ing nautilus shell, where it has been observed to their conclusions regarding: thickness, the corals, calcareous algae, fleshy algae, oysters, sunking of the spire below adapical margin of the barnacles, polychaetes, forams, bryozoans, outer lip, sculpture, and the presence-absence of tunicates, anemones and teredos (Jokiel 1989). a parietal tooth (Manrfquez and Castilla, personal These information reinforce the suggestion made observations). In the future we will incorporate by Helmuth et al. (1994) that dispersal by rafting Concholepas's shell morphological characteris- (via macroalgae, pumice or floating debris) can tics to describe the range of morphological vari- occur over geological and ecological time scales. ation along its geographical range. This, together Anthropogenic dispersal hypothesis (H4): An- with reported genetic differences between thropogenic passive and active transportation of populations (Guifiez et al. 1992) may help to marine flora and fauna is an emergent and grow- understand the geographical distribution of the ing mechanism for NSBI dispersal, that is chang- species. ing the species composition of many marine corn- DISJOINT GEOGRAPHICAL DISTRIBUTION OF MARINE INVERTEBRATES 599

With regards to the population genetic struc- LITERATURE CITED ture of 0. chilensis, even when 6 Foighil et al. (1999) have confirmed the results of Buroker et al. (1983 ), we suggest caution if the findings are ALLMON WD (1990) Review of the Bullia group (GAS- going to be extrapolated to the natural populations. TROPODA: NASSARIIDAE) with comments on its In fact, Buroker et al. (1983) in their analysis evolution, biogeography, and phylogeny. Bulletins used 36 Chilean oysters obtained from oysterfarm of American Paleontology 99 :5-155. ANDERSON DT, BM WHITE & EA EGAN (1975) The facilities at Coquimbo (29° 53' S, 71 o 18' W), out larval development and metamorphosis of the of the natural range distribution of the species. Ascidians Pyura praeputialis (Helier) and Pyura They did not report from which natural bed the pachydermatina (Herdman) (Pleurogona, Family oysters came from. So, the reported putative Pyuridae ). Proceedings of the Linnean Society of founder effect occurring in the Chilean oyster New South Wales 100: 205-217. "population", with a lower level of genetic vari- BEU AG & PA MAXWELL (1990) Cenozoic Mollusca of ation than the New Zealand oyster population, New Zealand. New Zealand Geological Survey and may be explained because a small effective popu- Paleontology Bulletin. 58:336-341. BEU AG ( 1970) Taxonomic position of Lippistes pehuensis lation number of oysters was used, which were Marwick, with a review of the species of Concholepas & obtained from a farming facility. Guifiez (Gastropoda, Muricidae). Journal of the Malacological Galleguillos ( 1985) reported evidence for popu- Society of Australia 2: 39-46. lation genetic differentiation of oysters within BLANKEY WO & JR GRINDLEY (1985) The intertidal their natural range of distribution in Chile (also and shallow subtidal food web at Marion Island. In: see Toro & Aguila 1996). This suggests that even Siegfried WR, PR Condy & RM Laws (eds) Antarctic when the species may have arrived recently (see nutrient cycles and food webs: 630-636. Springer- 0. chilensis section) to Chile, it has experienced Verlag, Berlin/Heidelberg. BLOTT M, C THIRIOT-QUIEVREUX & 1 SOYER (1988) genetic changes, which could be due to selection Genetic relationships among populations of Mytilus post-settlement (Guifiez & Galleguillos 1985, desolation is from Kerguelen, M. edulis from the North Toro & Vergara 1995). Furthermore, Fujio et al. Atlantic and M. galloprovincialis from the Mediter- (1983) described the genetic variability of oys- ranean. Marine Ecology Progress Series 44: 239-247. ters in New Zealand (same locality as Buroker et BREMER K (1988) The limits of amino acid sequence al. 1983) and reported 67% polymorphic loci and data in angiosperm phylogenetic reconstruction. Evo- 21.6% of heterozygosity. This is contradictory lution 42: 795-803. from the 27.6% polymorphic loci and 6.7% het- BREMER K (1994) Branch support and tree stability. erozygosity reported by Buroker et al. (1983) for Cladistics 10: 295-304. BUROKER NE, P CHANLEY, HJ CRANFIELD & P the same species. We have evidences for even DINAMANI (1983) Systematic status for two oyster lower levels of polymorphism and heterozygosity populations of the genus Tiostrea from New Zealand from oysters collected in the Chilean Pullinque and Chile. Marine Biology 77: 191-200. oyster bed (population protected by law); than CANCINO 1 & R BECERRA ( 1978) Antecedentes sob re la those reported by Buroker et al. (1983). There- biologfa y tecnologfa del cultivo de Aulacomya ater fore, we suggest that more genetic analyses are (Molina, 1782) (Mollusca: Mytilidae). Biologfa needed to gain a comprehensive understanding of Pesquera (Chile) 10:27-45. 1 & the colonization dynamics process and on the CANCINO B SANTELICES (1981) The ecological importance of kelp-like holdfasts as a habitat of in- phylogenetic and systematic relationships of 0. vertebrates in central Chile. 11 Factor affecting com- puelchana and 0. chilensis (Harry 1985, Carriker munity organization. In: Levring T (ed) Xth Interna- et al. 1994, Toro 1995). tional Seaweed Symposium: 241-246. Waiter de Gruyter & Co., New York. ACKNOWLEDGMENTS CANCINO 1 & B SANTELICES (1984) Importancia ecol6gica de los discos adhesivos de Lessonia The paper is dedicated to the late Professor Patricio nigrescens Bory (Phaeophyta) en Chile central. Sanchez Reyes, teacher, tutor and friend. We are Revista Chilena de Historia Natural 56:23-33. CARL TON JT (1987) Patterns of transoceanic marine especially grateful to Dr. J .M. (Lobo) Orensanz biological invasions in the Pacific Ocean. Bulletin of for constructive criticisms that permitted to im- Marine Sciences 41: 452-465. prove importantly this paper. The paper is part of CARLTON JT & JB GELLER (1993) Ecological roulette the Catedra Presidencial en Ciencias awarded to the global transport of nonindigenous marine organ- J.C. Castilla in 1997. We appreciate suggestions isms. Science 261: 78-82. made by Dr. M. Fernandez. Art work by M. Bobadilla. 600 CASTILLA & GUINEZ

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Invited Editor J. C. Castilla