diversification of rocky-shore biotas through geologic time

DIVERSIFICATION OF ROCKY-SHORE BIOTAS THROUGH GEOLOGIC TIME

MAaKES E. JOHNSON & B. GUDVEIG BAARLI

JOHNSON M.E. & BAARLI B.G. 1999. Diversification of rocky-shore biotas through geologic time. [Diversification des biotes des cStes rocheuses au cours des temps g6ologiques]. GEOBIOS, 32, 2: 257-273. Villeurbanne, le 30.04.1999.

Manuscrit d6pos6 le 08.07.1998; accept~ d6finitivement le 05.11.1998.

ABSTRACT - Changes in biodiversity of rocky-shore ecosystems from the early Precambrian (3,500 Ma) to the last interglacial epoch (125 Ka) are summarized on the basis of the fossil record associated with geological unconformities that reflect coastal paleotopography. This analysis is derived from data reported in 130 published papers culled and updated from previous bibliographic reviews. Minimum total diversity of fossil and extant species treated herein is 655 species. The highest biodiversity from any single locality is a mollusk-dominated biota of 62 species from San Nicolas Island on the Pacific coast of North America dating from the last interglacial epoch. Diversification was affected by mass extinctions, as rocky-shore ecosystems expanded and contracted through a combination of species attributed to Archaic, Paleozoic, Mesozoic, and/or Modern biotas. Stromatolites dominated Precambrian rocky shores, but continued as the principal Archaic biota through to the Miocene. The Paleozoic rocky-shore biota is characterized by encrusting inarticulate brachiopods, tabulate corals, and polyplacophorans, as well as ichnofossils representative of boring sipuneulid worms (ichnogenus Trypanites) and acrothoracican barnacles (ichnogenus Zapfella). Boring bivalves (ichnogenus Gastrochaenolites), encrusting bivalves (including oysters and rudists), scleractinian corals, and coralline red algae, as well as terebratulid brachiopods, are typical of an enhanced Mesozoic rocky-shore biota. The much expanded biodiversity of the Modern rocky-shore biota is demonstrated by clinging but mobile gastropods, fixed bivalves that adopted byssate and wedging habits, and by balanomorph barnacles. Adaptive innovations played critical roles in the long-term colonization of rocky-shore substrates, but the primary force behind the expansion of rocky-shore ecosystems through geologic time was selective biotic displacement from offshore low-energy to onshore high-energy settings. Rocky coastlines subjected to strong and persistent wave shock are effective "safe places" where species living in the intertidal zone often find refuge from predators and other competitors. This thesis is tested by checking the offshore origins of successful rocky-shore groups including barnacles, bivalves, corals, and coralline red algae. Concepts of keystone species and ecological locking in ancient rocky-shore ecosystems are explored. Latitudinal gradients and other geographic relationships among Pleistocene rocky-shore groups are commensurate with the Recent record, but only vaguely apparent for groups dating from earlier periods such as the Cretaceous. Time intervals for which even the most rudimentary data on rocky-shore biotas are most sparse include the Paleocene, Triassic, and the Devonian.

KEYWORDS: ROCKY-SHORE ECOSYSTEMS, BIODIVERSITY, GEOLOGICAL UNCONFORMITY, PALEOECOLOGY, ECOLOGICAL-EVOLUTIONARY UNITS.

Rt~SUMI~ - Les changements dans la biodiversit~ des ~cosystSmes des cStes rocheuses, du d~but du Pr~camblien (3 500 Ma) jusqu'~ la derni~re ~poque interglaciaire (125 Ka), sont examines d'apr~s les fossiles associ~s ~ des dis- continuit~s g~ologiques qui refl~tent la pal~otopographie des cStes. Cette analyse est r~alis~e t~ l'aide de donn~es publi~es darts 130 revues, s~lectionn~es et actualis~es par des r~visions bibliographiques ant~rieures. La diversit~ totale minimum d'esp~ces fossiles et actuelles trait~es iciest de 655. La plus grande biodiversit~ dans une seule localit~ est celle d'un biota de 62 esp~ces, domin~ par les mollusques, situ~e sur File de San Nicolas sur la cSte paci- fique nord-am~ricaine et datant de la derni~re ~poque interglaciaire. La diversification a ~t~ infiuenc~e par des extinctions en masse tandis que les ~cosyst~mes des cStes rocheuses se sont ~tendus et r~tract~s par le jeu de com- binaisons d'esp~ces attributes ~ des biotas archa~ques, pal~ozoiques, m~sozoiques, et/ou modernes. Les stromatolites ont domin~ les cStes rocheuses au Pr~cambrien mais sont rest~s le biota archa~que principal jusqu'au Miocene. Le biota pal~ozo~que de ces cStes est caract~ris~ par des brachiopodes inarticul~s encrofitants, des tabul~s et des poly- placophores, ainsi que par des ichnofossiles de vers et de sipunculides perforants (ichnogenre Trypanites) et de cir- rip,des acrothoraciques. Les bivalves perforants (ichnogenre Gastrochaenolites), les bivalves encrofitants (compre- nant les hu~tres et les rudistes), les coraux scl~ractiniaires et les algues rouges calcaires ainsi que les brachiopodes t~r~bratulides sont typiques du biote des cStes rocheuses plus important du M~sozo~'que. La plus grande biodiversit~ du biota moderne de ces c6tes est domin~e par des gast~ropodes se fixant mais mobiles, des bivalves fixes (g byssus) et fouisseurs, et par des bernacles balanomorphes. Les innovations adaptatives ont jou~ un r61e critique dans la colonisation ~ long terme des substrats des c6tes rocheuses mais le facteur principal qui a provoqu6 l'expansion des 6cosyst~mes sur celles-ci h travers les temps g6ologiques fut le d6placement s61ectif des biotas de sites offshore de basse ~nergie h des sites onshore de haute 6nergie. Les littoraux rocheux exposfis ~ des chocs de vogues puissants et continus sont des endroits favorables pour les esp~ces vivant dans les zones intertidales car elles y trou- vent souvent refuge contre les pr6dateurs et autres comp6titeurs. Cette hypoth~se est test~e en v6rifiant les

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origines offshore des groupes/t succ~s des cStes rocheuses, y compris bernacles, bivalves, coraux et algues rouges calcaires. Les concepts d'esp~ces-pivots et de fermetures ~cologiques dans les 5cosyst~mes des c6tes rocheuses sont exa- mings. Les gradients latitudinaux et les autres relations g6ographiques entre les groupes pl6istoc~nes des cStes rocheuses sont comparables au registre r~cent, mais difficilement d~celables pour les groupes datant de p~riodes plus anciennes comme le Cr6tac~. Les intervalles de temps pour lesquels des donn~es, m~me indigentes, sur les biotas des cStes rocheuses sont les plus rares, correspondent au Pal~ocgne, au Trias et au DSvonien.

MOTS-CLt~S: I~COSYSTI~MES DES COTES R OCHEUSES, BIODIVERSITI~, DISCONTINUITIES GI~OLOGIQUES, PALEOI~COLOGIE, UNITIES t~COLOGIQUES EVOLUTIVES.

INTRODUCTION

No other ecological boundary on planet Earth is more definitive or profound than the interface 'between land and sea. Sea cliffs of one kind or another are estimated to back 80% of the modern global coastline (Emery & Kuhn 1982), but perhaps only 33% of the present coastline entails rocky shores that are in direct contact with sea water on a regu- lar basis (Johnson 1988a). Hard substrates exposed to intertidal and shallow-subtidal waters provide varied habitats for colonization by marine algae and invertebrates. Rocky shorelines range geographically across tropical to boreal latitudes today, and must have done so throughout much of the geological past. Physical and biological constraints on contemporary rocky-shore ecosys- terns have been the subject of intense study by marine ecologists (Lewis 1964, Stephenson & Ste- phenson 1972; Moore & Seed 1986; Denny 1988), arguably more so than for any other marine ecosystem. Despite pioneer contributions on littoral encrusting and boring faunas from the fossil record (Hecker 1965; Radwanski 1970), scant attention has been paid by paleoecologists to ancient rocky- shores or their ecosystems. Indeed, those who have given the problem some consideration (Schopf 1978; Valentine 1980; Bambach 1986), reason that marine biotas are not expected to survive the fossilization process in high-energy settings associated with rocky shores.

The understanding that ancient rocky shores possess utility as unambiguous markers of former sea levels preserved in the geological record has provo- ked fresh research. Practical applications include (Johnson 1988b): direct mapping of paleocoastlines, mapping of offshore paleocommunities, analysis of paleoshore hydrodynamics, and differentiation between eustatic and tectonic sea-level changes. A rocky shore from the Upper Ordovician on Hudson Bay in Manitoba, Canada, is a clear reference point for the onshore-offshore relationships of faunal associations (Johnson et al. 1988). Fifty kilometers of Upper Cretaceous rocky shoreline are exposed along the present Pacific coast of Baja California, where variations in fossil biotas associated with windward and leeward settings imply that the energy flow of coastal dynamics was from a different direction than today (Johnson et al. 1996). In

conjunction with other regional data, analysis of a Lower Silurian karst shore in Guizhou Province, South China, indicates a 63-m rise in eustatic sea level (Rong & Johnson 1996). An entire archipelago of islands with rocky shorelines scattered over 25 km 2 is mapped from the Lower Pliocene on the Gulf of California in Baja California (Simian & Johnson 1997). Likewise in comparison with global data, it is possible to interpret regional tectonic subsidence of this archipelago on the order of 75 m during 2 Ma. As a consequence of studies such as these, slow progress is made with the registration of fossil biotas linked to ancient rocky shores. An example is a previously unknown species of rock-encrusting organism with affinities to sponges or calcareous green algae from the Upper Ordovician of Hudson Bay (Johnson et al. 1998). Few papers focus on the autecology of species from ancient rocky-shore environments, but a good example concerns articulate brachiopods from the Upper Cretaceous of Sweden (Asgaard & Bromley 1991).

Consideration of changes in rocky-shore ecosystems and their biological diversification through geologic time is an ambitious goal that not only requires assimilation of previous research, but depends on a minimum critical mass of global and temporal data. Early bibliographic surveys on the subject cite fewer than 45 references (Johnson 1988a,b), and stress the novelty of ancient rocky shores in the geological record. A bibliography offering wider geological coverage lists 155 references, with 92 (nearly 60%) providing information on associated fossil biotas (Johnson 1992). Another bibliography by Johnson & Libbey (1997) summa- rizes 60 references on rocky-shore localities correlated with the maximum sea-level rise during the last interglacial epoch (Oxygen Isotope Substage 5e). Almost all the Substage-5e references, therein, relate some paleontological data. In the later bibliographies (Johnson 1992; Johnson & Libbey 1997), ancient rocky shores are not regarded so much as rarities in the geologic record but as features easily overlooked by geologists and paleontologists. The relative abundance of abandoned rocky shores in the Upper Pleistocene raises expecta- tions that significant discoveries can and will continue to be made from deposits representing more remote ages.

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The oldest described rocky shoreline features stromatolites that date from 3,500 Ma (Byerly et al. 1986). Maximum known diversity of fossils belonging to a rocky-shore habitat from a single locality is represented by a mollusk-dominated fauna of 62 species from San Nicolas Island on the Pacific coast of North America dating from the last interglacial epoch (Russell 1991). How has the rocky- shore ecosystem changed or evolved over this interval? Is there a steady increase in biodiversity with time, or is change punctuated by major extinctions and the success of adaptive replace- ments during recoveries from mass extinctions? Where do the species adapted to life on wave-swept rocky shores originate? Do they evolve in place or are they mostly immigrants from other environments? What are the primary controls over biodiversity in rocky-shore communities? On a local level, to what extent does the concept of keystone species in contemporary communities apply to paleocommunities? On a temporal scale, to what degree is ecological locking a mitigating factor? On a global scale, how do latitudinal gradients or other paleogeographic relationships assert themselves with respect to ancient ecosytems? As flawed as the available fossil record is, our present vibrant rocky-shore ecosystems may be related to their counterparts from the geological past.

DEFINIT IONS AND METHODS

Contemporary rocky shorelines embrace diverse environments ranging from outer to inner, exposed to protected, and windward to leeward settings. All ancient rocky shores preserved in the geological record are recognized as some variant on an unconformity, where littoral deposits rest on resistant rocks. With the possible exception of karstic shores, the littoral deposits above the unconformity surface typically consist of a basal conglomerate with clasts eroded from parent rocks below the uncon- fortuity surface. Even those rocky shores interpreted as having formed under low-energy conditions (protected, enclosed, or otherwise leeward in paleogeographic setting) exhibit rounded clasts indicati- ve of marine abrasion. Thus, past or present, all rocky shores have been or are subjected to harsh conditions including intermittent exposure to waves of moderate to high energy levels.

Modern rocky-shore biotas include a range of communities, in which the constituent organisms are linked together by their effects on one another and their shared response to the physical environment. Marine biologists have no difficulty deciding what organisms belong or do not belong to rocky-shore communities. For example, Morris et al. (1980) list 753 species of invertebrates from the intertidal zone of coastal California. Of these, 412 (53%) are

characterized as living on rocky substrates, under rocks, on the shaded sides of boulders, in rock cre- vices, or in rock borings. Among paleoecologists, however, there is widespread aversion to the term community or paleocommunity. This is partly due to the fact that all possible community members from any given time interval do not share an equal chance of becoming fossilized. At minimum, 208 (or only slightly more than 50%) of the living 412 rocky-shore species listed by Morris et al. (1980) possess hard parts adequate to insure fossilization. The largest number of these are mollusks.

A serious difficulty for many paleoecologists is uncertainty in differentiating between those fossils representing organisms that lived in a particular environment, those that were winnowed away, and those that were admixed after death from other environments. In this respect, ancient rocky-shore biotas are appealing to work with because many species exemplify encrusting, boring, or otherwise attached and immobile lifestyles. With regard to the clinging but mobile lifestyle of some rocky- shore mollusks, particularly gastropods, it is possible to trace many Neogene fossils to extant species and some genera may be traced from the Mesozoic. In addition to Morris et al. (1980), other references used by us in tracking extant species include Keen (1971) for the tropical west Americas, Brusca (1980) for the Gulf of California, and Wells & Bryce (1988) for Western Australia. Many extra- neous species transported into ancient rocky-shore deposits are readily excluded from consideration by checking their extant life habits. Autochthonous rocky-shore deposits with a high percentage of encrusting species are easily distinguished from allochthonous fossil deposits, which may be dominated by rocky-shore species (Zwiebel & Johnson 1995), but typically are not (Veevers & Roberts 1966). While accepting that 50% of any given rocky-shore biota may elude fossilization, we none- theless feel justified in applying the term paleocommunity to ancient rocky shore biotas demons- trably preserved in situ.

The paleontological data used for this study are derived from 130 published papers re-evaluated and expanded from the bibliographies of Johnson (1992) and Johnson & Libbey (1997). Some cita- tions formerly included in those bibliographies are rejected here due to controversy over interpretations or duplication of data. For example, bryozoan build-ups from the Lower Carboniferous previously attributed to a rocky shoreline developed on a drowned karst surface in Newfoundland (Dix & James 1987) were redescribed as belonging to a deep-water rift valley with associated hydrother- mal activity (Von Bitter et al. 1992). References with useful paleontological information applied to this project represent a 41% increase since 1992. A

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complete list of the biota used in this study and references to the literature may be obtained from the authors or viewed at the Geobios Web cite http.//geobios.univ.lyonl.fr. In order to facilitate sorting and comparison of biotas by geological age (and other attributes such as substrate type), all pertinent data were computerized using File Maker Pro by Claris for Macintosh.

Basic patterns in the development of rocky-shore communities through time are described through the use of spindle diagrams that track the diversity of particular constituents, such as byssate bivalves. Trends in the possible origins of rocky- shore species are tested by seeking the oldest known occurrence of key groups from offshore subtidal settings. The bibliography on hardgrounds and hardground faunas by Wilson & Palmer (1992) is especially helpful in checking for data regarding offshore subtidal biotas preserved in situ. Controls on the biodiversity of rocky-shore communities are examined by comparison with the effects of mass extinctions and the recovery from mass extinctions tabulated more generally for marine animals through the Phanerozoic (Sepkoski 1997), in addition to consideration of other possible ecological factors such as keystone species, ecological locking, and latitudinal gradients. Base maps used for plotting latitudinal gradients are derived from the atlas of Smith et al. (1994).

CHANGES IN ECOSYSTEM BIODIVERSITY

TEMPORAL SURVEY OF MAJOR CONSTITUENTS

Results on the biodiversity of rocky-shore paleocommunities are summarized by spindle diagrams in 15 components grouped mostly by phylum or

class (Fig. 1), as derived from a data base of 655 fossil and extant species. These are arranged from left to right to emphasize their order of appearance through time. Because bivalves within the Phylum Mollusca form one of the largest components, it is further subdivided into categories that reflect basic differences in benthic lifestyle (Fig. 2). Based on temporal groupings, the expansion and decline in raw numbers of species are tentatively defined by four major clusters consisting of Modern, Mesozoic, Paleozoic, and Archaic representatives. Species lists for each cluster are available from the authors or on the web. The Archaic biota is dominated by stromatolites that date from 3,500 Ma (Byerly et al. 1986), but continued to reappear on rocky shores through to the Miocene. A typical Paleozoic biota is characterized by polyplacophorans, encrusting inarticulate brachiopods, and tabulate corals, as well as trace fossils left probably by sipunculid worms (ichnogenus Trypa- nites) and acrothoracican barnacles (ichnogenus Zapfella). Inarticulate brachiopods persist today, but tabulate corals disappeared at the end of the Paleozoic. Trypanites borings on rocky shores are last found in the Pliocene, but boring barnacles are extant. Revival and expansion of rocky-shore biotas during the Mesozoic was dependent foremost on boring bivalves (ichnogenus Gastrochaenolites), encrusting bivalves (including oysters and rudists), but also coralline red algae, scleractinian corals, as well as thecidean brachiopods (cemented forms) and terebratulid brachiopods (forms with an enlarged pedicle foramen). All survive on rocky shores today, except for rudist bivalves which became extinct at the end of the Cretaceous. Robust expansion of diversity in the Modern rocky-shore biota is reflected by clinging but mobile gastropods,

FIGURE 1 - Spindle diagrams that represent various components of the rocky-shore biota, mostly by phylum or class, track changes in composition and biodiversity through geologic time (E = early, M = middle, L = late). Lateral scale for diversity = 10 species. Diagrammes repr6sentant les divers composants des biota de cStes rocheuses, p r inc ipa lement par phy lum ou par classe, les changements de composit ion des traces et la biodiversitg au cours des temps g~oIogiques (E = inf,- rieur, M = moyen, L = sup~rieur). Echelle horizontale de diversit~ = 10 esp~ces.

E. Cletaceous L. Jurassic

"P.I M. Jurassic 0 E. Jurassic

L. Triaesic ~- M, Triassic ~= E. Triassic L, Permian "~ E. Permian L, Carboniferous " E. Carboniterou~ L Devonian

,~ M. Devonian

N E, Devonian i ~ L Silurian

~. E. Silurian L. Ordovician ~ I M. Ordoviclan E. Ordovician L. Cambrian M. Cambiian E. Cambrian Precarnbrian

=nmmnmnunnmnnmm nn ~ n m m I mmmmm mmmmmm m m mmm m mmmmmmmmmm m m m m m

) ) . )

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Pleistocene

Pliocene

Miocene

Oligocene 0

Eocene

Paleocene

L. Cretaceous E. Cretaceous

o L. Jurassic "N ~ M. Jurassic

E. Jurassic

i L. Triassic M. Triassic

E. Triassic

o L. Permian "N ~ E. Permian ~ L. Carboniferous ~- E. Carboniferous

! II l !1

g

FIGURE 2 - Spindle diagrams for categories of Class Bivalvia (Phylum Mollusca) that reflect basic differences in life style on rocky shores and changes in diversity through geologic time. Lateral scale for diversity = 10 species. Diagrammes pour des catggories de la Classe Bivalvia (Phylum Mollusca) refl~tant des differences profondes de modes de vie sur les c6tes rocheuses et des modifications de la diversit~ de ces modes au cours des temps g~ologiques. Echelle horizontale de diversit~ = 10 esp~ces.

fixed bivalves that adopted byssate and wedging habits, and by balanomorph barnacles. Among these, balanomorph barnacles and byssate bivalves (Fig. 2) made promising starts as members of rocky-shore communities during the Cretaceous, but became even more important during the Cenozoic.

RECOVERY FROM MASS EXTINCTIONS

Genus-level changes in the diversity of marine invertebrates affected by mass extinctions are treated by Sepkoski (1997) as distinct trends in the composition of Cambrian, Paleozoic, and Modern evolutionary faunas. The marine Paleozoic fauna, for example, began at a low level of diversity during the Cambrian and rapidly expanded through the Paleozoic Era. Some ele- ments still survive today, although the fauna was hit hard by the Late Permian mass extinctions and subsequently regained only about 30% of its former diversity. Patterns comparable to those noted by Sepkoski (1997) are recognized at the species level in the temporal development of Archaic, Paleozoic, Mesozoic, and Modern rocky- shore biotas. The Precambrian to Phanerozoic history of diversity in these biotas is summarized by the survivorship trends shown in Fig. 3.

The stromatolitic Archaic biota makes sporadic appearances on rocky shores from the Precam- brian through the Phanerozoic. Like their shallow

subtidal relations, the rocky-shore stromatolites were probably opportunistic, or disaster forms (Schubert & Bottjer 1992). Normally, such taxa thrive in marginal or environmentally unstable environments, but become more abundant and widespread following mass extinctions. Apparen- tly, this was the case for encrusting stromatolites during the earliest Paleocene (Pomoni-Papaioan- nou & Solakius 1991). The Paleozoic biota made its appearance on rocky shores during the Early Cambrian, hit its peak during the Late Cretaceous, but survived with substantial cuts during the Cenozoic. Trypanites is a trace fossil belonging to this cluster that may represent another long-lived disaster form, albeit one limited to karstic shores and probably represented by different organisms at different times.

The Mesozoic biota has its roots in the Early Carboniferous but hit a major diversity peak dominated by scleractinian corals and cemented bivalves during the Late Cretaceous. Thereafter came a tremendous decline associated with the terminal Cretaceous mass extinctions, followed by a gradual recovery (Fig. 3). The Modern biota shows traces of failed experiments during the Late Permian, as with the southern hemisphere, high- latitude Eurydesma fauna named for large byssate bivalves that are especially common in Australia. Byssate bivalves added significantly to the diversity of the Modern fauna to reach an initial diversity peak subordinate to the Mesozoic biota during Late Cretaceous time. Following the terminal Cretaceous mass extinctions, the Modern biota made a strong recovery that outstripped the Mesozoic fauna by more than 3:1 in diversity by Pleistocene time (Fig. 3). The surge in diversity represented by the Modern biota was largely influenced by the recovery of byssate bivalves and the radiation of rocky-shore gastropods (Figs 1, 2).

Adaptive radiations clearly played critical roles in the recovery and expansion of rocky-shore biotas that survived mass extinctions. A dozen different groups of epibyssate bivalves radiated from only a few ancestral endobyssate and free-burrowing forms (Stanley 1972). Predatory gastropods, notably including many species from among the superfamilies Muricacea and Conacea as rocky-shore specialists, underwent an expansion during the middle Cenozoic described as "one of the more remarkable diversifications in the evolutionary history of the Mollusca and the invertebrates" (Taylor et al. 1980: 400). Likewise, the Suborder Balanomorpha sustained a major radiation through the Cenozoic that took off following the evolution of species within the Superfamily Chtha- maloidea during the Late Cretaceous (Stanley & Newman 1980; Newman & Stanley 1981). An adaptive radiation of brachiopods surviving the

-180

-140 !~:~Paleozoic "~:I M esozoic

n = 591 species

~Modern

-100

"6 -80

E -6~ Z

-40

20

~Archaiv

FIGURE 3 - Changes in the diversity of the rocky-shore biota through geologic time, as arrayed in four sequential clusters consisting of Archaic, Paleozoic, Mesozoic, and Modern representatives. Diversity is given in numbers of species (total N=591). Variations de la diversitg des biotas de cStes rocheuses au cours des temps gdologiques prdsentdes en quatre groupes sdquentiels correspondant aux reprdsentants du Prdcambrien, du Paldozo~que, du Mdsozo~que et de l'Actuel. La diversitd est donnde en nombre d'espOces (N total = 591).

Late Permian mass extinction concerns development of the transapical foramen in the terebratu- lids. This innovation allowed the pedicle to enlarge and strengthen itself through resorption of sur- rounding shell material (Rudwick 1970). Other than cemented forms, brachiopods that lacked such capacity for resorption were unable to retain the strong attachment necessary for life in the low intertidal to shallow subtidal environments of rocky shores.

ORIGINS OF SOME ROCKY-SHORE BIOTAS

Encrust ing cora l l ine red a lgae

The oldest encrusting (non-erect) red algae are well represented by species belonging to the genus Solenopora. Rounded, hemispherical forms are common in this genus, which ranges from the Cambrian to the early Paleogene (Wray 1977). Although they are generally treated as distinct from the Corallinaceae, the group including Solenopora is widely considered to be ancestral to true coralline algae. The earliest association of encrusting red algae with a high-energy, rocky-shore environment is found in the basal Trenton Group (middle Ordovician) of Quebec, where Solenopora gravels occur in tidal pools eroded in Precambrian gneiss. At Montmorency Falls, some examples of hemispherical colonies are found in growth position adhering to the gneiss substrate or eroded gneiss boulders (Harland & Pickerill 1984). The crustose coralline algae so abundant today in intertidal and shallow subtidal settings trace their direct ancestry to the Jurassic (Wray 1977), as grouped into three subfamilies: the Melobesioideae, Lithophylloideae, and Mastophoroideae (Woelkerling 1988). The earliest connection of likely Litho- thamnium with rocky shores is traced to the (Aptian) Tano- hata Formation of Japan, where it occurs in buildups together with rudist bivalves and corals on an andesite surface (Sano 1991). Occurrences of crustose coralline red algae on submari-

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ne hardgrounds are notably lacking from the analyses of T. Palmer (1982) or Wilson & Palmer (1992).

Boring sponges

The ichnogenus Entobia was redefined by Bromley (1970) for borings from the Mesozoic and Cenozoic that closely resemble the work of living clionid sponges. The earliest known occurrence of a boring sponge on a high-energy rocky shore is in the Albian of the Kizil-Kum region in Turkestan (Pyanovskaya & Hecker 1966). The authors cite Polifera cliona, which would now probably be referred to Entobia. Drowned karstic shores that date from the Miocene and Pliocene are typically reported to include borings assigned to this ichnogenus or clionids identified with extant species (Radwanski 1970; Martinell & Domenech 1986). Living clionid sponges occur widely in reefs today, and did so during the Mesozoic and Cenozoic. An example of Entobia from Portlandian patch reefs in the Portland Stone of England is reported by Ftirsich et al. (1994). Smaller borings referred to as clionid sponges by Elias (1957) occur on shells in subtidal deposits from the Mississippian Redoak Hollow Formation of Oklahoma.

Encrnsting tabulate corals

The earliest association of encrusting tabulate corals with a high-energy, rocky-shore environment is traced to the Upper Ordovician Port Nelson Formation of Manitoba (Johnson & Baarli 1987; Johnson et al. 1988). Examples have not been identified to species level, but clearly belong to the favositid tribe of tabulate corals. The oldest probable tabulate coral is Moorowipora chamberensis from the Lower Cambrian reef rocks belonging to the Moorowie Formation of South Austral ia (Sorauf & Savarese 1995).

Encrusting scleractinian corals

The earliest known examples of encrusting scleractinian corals on a high-energy, rocky shore come from the Hettangian Sutton Stone of South Wales (Johnson & McKerrow 1995). Two species, AEocoeniopsis gibbosa and Heterastraea sp., occur as small, flat encrustations on larger clasts or directly on the hard substrate of a drowned carbonate bench. The oldest scleractinian corals may trace their origins to the Permian of Tunisia, or perhaps even the Ordovician of Scotland (Ezaki 1998). True scleractinian corals were widespread in occurrence through the middle Triassic Tethys seaway (Stanley 1981), but were exclusively ahermatypic. According to Stanley (1995), symbiosis between scleractinian corals and zooxanthellae evolved during Norian time and led to the onshore development of localized scleractinian framework builders. Large fra- meworks constructed by scleractinian corals did not appear until the end of the Triassic.

Encrusting inarticulate brachiopods

Craniids provide an example of extant inarticulate brachiopods that are encrusters with a long geologic record. Upon larval settlement, the ventral mantle edge is in contact with the substrate such that the entire ventral valve is cemented in place. There is no development of a pedicle. Rudwick (1965: H202) concludes this is the strongest form of attachment achieved by brachiopods, and notes that "Crania occurs in more strongly current-swept environments than any other living brachiopod." In addition to rocky shores, contemporary craniids may be found attached to boulders in waters up to 90 m in depth (Surlyk & Christensen 1974). Abundant, large individuals (up to 4 cm in length) of Crania stobaei are well known from an Upper Campanian rocky coast preserved at Iv5 Klack in southern Sweden (Surlyk & Christensen 1974). Much smaller, but abundant individuals of Craniscus strambergensis occur attached to fissure walls from the Upper Berriasian-Valanginian Olivetsk~ Hora Formation in the Czech Republic (Nekvasilov~ 1982). Among Paleozoic craniids is an undetermined species belonging to the genus Philhedra that encrusted a subtidal

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hardground from the Middle Ordovician Galena Group of Iowa (T. Palmer 1982).

Articulate brachiopods

Some Recent terebratulid and rhynchonellid brachiopods are known to have the ability to produce shallow borings due to the attachment of their pedicle to other shells or hard carbonate substrates. Fossil traces that replicate a circlet of small pits similar to the scars left by Recent species are designated by the ichnogenus Podichnus centrifugalis (Bromley & Surlyk 1973). The only example that connects such scars with the adaptation of brachiopods to life on high-energy rocky shores is with regard to "Rhynchonella" triangularis from deposits in the Upper Campanian at Iv5 Klack in southern Sweden (Asgaard & Bromley 1991). The oldest known occurrence of Podichnus is reported from the valves ofLeiorhynchoidea carboniferus from the Mississippian Chainman Formation of Utah (Alexander 1994). The makers of the scars are attributed to juveniles of the same species. Based on the presence of black ferruginous micrites in this rock unit, colonization is interpreted to have taken place in a subtidal dysoxic habitat. Thecidean brachiopods are small articulates that lack a pedicle and are usually cemented to a hard substrate. Abundant speci- mens of Moorellina? vesna are attached to fissure walls from the Upper Berriasian-Valanginian Olivetsk~ Hora Formation in the Czech Republic (Nekvasilov~ 1982). An example of a related encrusting brachiopod from a more exposed rocky-shore setting is represented by Eothecidellina imperfecta from the Ceno- manian-?Turonian Korycany Formation in the Czech Republic (Zitt & Nekvasilov~ 1996). According to Elliott (1958), thecidean brachiopods first appeared in the Triassic as highly modified descendants of Paleozoic strophomenid or atypical terebratulid brachiopods. The oldest known articulate brachiopod fulfilling an encrusting habit is the strophomenid Liljevallia gotlandica from Sheinwoodian bioherms in the Upper Visby Beds of Gotland, Sweden (Nield 1986).

Encrus t ing bivalve mol lusks

With the exception of species belonging to the genus Limanomia from the Upper Devonian of Russia and the Lower Carboni- ferous of Wales, encrusting bivalves on hardgrounds are shown by T. Palmer (1982) and Wilson & Palmer (1992) to have been essentially a Mesozoic phenomenon dominated by oysters. The oldest representatives are traced to species of Gryphaea from the Upper Triassic of Nevada and Italy. The presence of nacreous structure in these forms implies that the common ancestor to the Order Ostreoida was either a member of the Pterioida or Pectinoida (McRoberts & Carter 1994). Hudson & Palmer (1976) argue that some true oysters dating from the Cretaceous to the Recent are descended from primitive gryphaeids via Liostrea and Praeexogyra. In particular, the coiled and thickened left valves typical of Gryphaea were modified as young oysters remained attached for a longer period of their life cycle and became better accommodated to bottom currents. Species belonging to the genera Lopha, Exogyra, and Liostrea were the dominant encrusters on Jurassic hardgrounds (Palmer 1982). The earliest known record of encrusting oysters on a rocky shore concerns Liostrea sp. from the Hettangian Sutton Stone of South Wales (Johnson & McKerrow 1995). The earliest Ostrea (unidentified as to species) found encrusted on rocky shores appear in the Albian of the Kizil-Kum region in Turkestan and northern Cali- fornia (Pyanovskaya & Hecker 1966; Rodda 1989). At the beginning of the Late Cretaceous (Cenomanian-Turonian) in the region of eastern Germany and the Czech Republic, several species belonging to the genera Lopha, Exogyra, and Spondylus appear for the first time (in addition to Ostrea) as rocky-shore members (Pietzsch 1962; Zitt & Nekvasilov~ 1996).

Byssate bivalve mol lusks

Byssally attached bivalves typified by several epifaunal species belonging to Mytilus, Modiolus, Brachidontes, and Barbatia are among the most successful and prolific rocky-shore dwellers.

According to Stanley (1972: 194), the intertidal byssate forms we are familiar with today, evolved from Devonian modiomorphs such as Lyromytilus attenuatus that lived as endobyssates half submerged in subtidal sediments. The first occurrence of Mytilus associated with an ancient rocky shore is known from the Upper Oligocene of Oregon (Miller & Orr 1988). Species of Mytilus very similar in shape to living M. edulis or M. californianus, but smaller in size, were common as subtidal, soft-substrate dwellers during Oxfordian-Kimmeridgian times. A good example of Mytilus from this interval occurs in the Marly-Lumachelle Formation from the Holy Cross Mountains of Poland (Kutek 1968). An older, endobyssate ancestor comes from the Lower Pennsylvanian, as represented by Promytilus pottsvillensis from the Mercer Limestone of Ohio (Hoare et al. 1978). The earliest clear association of Modiolus with a near-shore rocky substrate comes from the Upper Cretaceous (Piripauan) of New Zealand (Crampton, 1988). Modiolus hillanus is attributed to an intertidal setting of Triassic age in South Wales (Kelling & Moshrif 1977). An older endobyssate ancestor that lived partly buried in subtidal soft sediments, is Modiolus radiatus from the Upper Carboniferous Mercer Limestone of Ohio (Hoare et al. 1978). Brachidontes cowlitzensis, from the Eocene Crescent Formation of Washington State, is the earliest known representative of the genus to be affiliated with a near-shore rocky substrate (Squi- res & Goedert 1994). Among its oldest known endobyssate ante- cedents restricted to a soft-sediment subtidal setting is B. filis- culptus from the Cenomanian Dakota Formation of Arizona (F~irsich & Kirkland 1986). The earliest known affiliation of Barbatia with a near-shore rocky substrate is indicated by an unidentified species from the Maastrichtian Ripley Formation of Alabama (Bryan 1992). Like Brachidontes, one of the oldest known endobyssate relations of Barbatia limited to a soft-sediment subtidal setting comes from the Upper Cretaceous Dakota Formation of Arizona (Ffirsich & Kirkland 1986). The oldest known epibyssate bivalve that accommodated itself to life on rocky shores, is Eurydesma playfordi from the Lower Permian of Australia (Runnegar 1979). Species belonging to this genus spread throughout the cold-water, high latitudes of Gondwana, including Australia, India, South Africa, and Argentina. Global warming through the Permian is interpreted to have caused the group's demise. Attachment by byssal threads clearly developed as an evolutionary innovation at an earlier time, but was not adapted as an anchorage to high- energy rocky shores until the early Permian. A remarkable example from the Mississippian Bear Gulch Limestone of Montana shows that epibyssate pterioid bivalves assigned to Caneyella were able to attach themselves to kelp-like algal fronds (McRoberts & Stanley 1989). Epibyssate predecessors associated with the Pterioida, such as Ambonychia ulrichi and A. alata, may be traced to the Upper Ordovician (Cincinna- tian) of the Ohio River valley. Although superficially similar to mytilid bivalves, their byssal anatomy is interpreted as having been functionally less stable and the group is not regarded as ancestral to the Mytilacea (Stanley 1972).

Bor ing bivalve mol lusks

Flask-shaped borings with a single opening at the smaller end are assigned to the ichnogenus Gastrochaenolites (Kelly & Bromley 1984). Many of the bivalves responsible for such borings on rocky shores and hardgrounds today line their dwel- lings with a calcareous deposit. Species belonging to the genera Gastrochaena and Pholas (Gastrochaenidae and Pholadidae) and Lithophaga (Mytilidae) are typical borers. On many Ceno- zoic and some Mesozoic rocky shores, identifications to genus or species level are possible based on diagnostic shapes or actual shell material found preserved within the borings. The earliest representatives of Lithophaga identified on ancient rocky shores occur in the Hettangian of South Wales (De La Beche 1846; Johnson & McKerrow 1995). The earliest Gastrochenolites borings associated with a rocky-shore setting come from a

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Mississippian paleokarst in Arkansas that was drowned in middle Carboniferous time (Webb 1994). There are no earlier expressions of this ichnogenus presently known from submarine hardgrounds (T. Palmer 1982). The oldest borings attributed to bivalves that occur on submarine hardgrounds come from the Upper Ordovician of Ohio and they are assigned to the ichnogenus Petroxestes (Wilson & Palmer 1988). Corallidomus scobina is one species exhibiting shell material found in such borings, but it has never been reported from a rocky-shore setting.

Encrnsting rudist mol lusks

The earliest association of rudist mollusks with a high-energy, rocky-shore environment is traced to the Aptian Tanohata Formation of Japan, where Praecaprotina yaegashii occurs as buildups together with corals and coralline red algae on an andesite surface (Sane 1991). Bein (1976) also interprets examples of fringing rudist reefs but direct attachment to a hard, inorganic substrate is difficult to show. Right (attached) valves of Coralliochama orcutti are found encrusted directly on andesite boulders interpreted to have sat on the windward coast of a small rocky island preserved by the Maastrichtian Rosario For- mation of Baja California, Mexico (Johnson & Hayes 1993). Evol- ved from megalodontid bivalves, the first rudists belong to the Family Diceratidae from the Oxfordian of the Mediterranean region and beyond (Donovan 1992). These were solitary in habit, living on protected carbonate shelves or in lagoons. Rocky-shore dwellers from among plagioptychid rudists were derived from sediment-dwelling elevator forms (P.W. Skelton, pers. comm. 1998).

Boring (?sipnnculid) worms

Small, simple, unbranched tube borings with a circular apertu- re usually oriented normal to the surface are assigned to the ichnogenus Trypanites. This is a morphogenus under which several different kinds of organisms may have been responsible for similar borings. Unsegmented sipunculid worms, however, are considered to be the most likely candidates (Pemberton et al. 1980). The earliest known occurrence of Trypanites on a karst surface related to a rocky shoreline, is found in Middle Ordovician (Chazyan) limestone belonging to the Mingan Formation of Quebec (Desrochers & James 1988). In contrast, the oldest known examples of Trypanites from the fossil record are reported from the Lower Cambrian Forteau Formation of Labrador (James et al. 1977). The borings penetrate the reefal skeletons of archaeocyathids, as well as cemented hardgrounds.

Boring (acrothoracid) barnacles

Acrothoracid barnacles comprise a subgroup of Cirripedian arthropods that bore their way into shells or hard substrates. The characteristic borings have a slot-like opening and are referred to the ichnogenus Zapfella. The earliest connection between these trace fossils and a rocky-shore environment comes from a Mississippian paleokarst in Arkansas that was drowned in Middle Carboniferous time (Webb 1994). The oldest record of such borings are reported by Baird et al. (1990) exclusively on platyceratid gastropods from the Middle Devonian Ludlowville and Moscow formations of Givetian age in New York State

Pedunculate (lepadomorph) barnacles

Lepadomorph barnacles comprise a subgroup of Cirripedian arthropods that attach themselves to an organic surface or hard physical substrate by means of a peduncle or fleshy stalk. The species Pollicipes polymerus is a living example of a stalked barnacle that is commonly restricted to the middle intertidal zone on rocky shores on the west coast of North America (Morris et al. 1980). A closely related species, P. californicum, occurs only offshore in waters 18 - 400 m deep. The earliest associations of lepadomorph barnacles with a rocky-shore setting are Virgis- calpellum cf. gabbi from the Campanian basal Brownstone Formation of Arkansas (Zullo et al. 1987) and Calantica sp. from the Upper Cretaceous (Piripauan) basal Maungataniwha

Sandstone of New Zealand (Crampton 1988). Stalked barnacles remain unknown from ancient submarine hardgrounds, but the oldest example of attachment to an organic surface is Cyprilepas holmi found preserved affixed to eurpyterid arthropods from the Upper Wenlock Viita Beds of Estonia (Wills 1963).

Encrusting (brachylepadomorph & balanomorph) barnacles

Among the most successful barnacle groups to colonize high- energy, intertidal environments are those with an encrusting habit. The Suborder Brachylepadomorpha includes pollicipoid- like barnacles that lost their peduncle and achieved direct attachment of the mantle (or capitulum) to a hard substrate. The earliest known members of this suborder to be affiliated with a rocky-shore setting are Brachylepas americana from the Campanian basal Brownstone Formation of Arkansas and B. guascoi from the Campanian of southern Sweden (Zullo et al. 1987). Other members of the suborder are traced to the Upper Jurassic, but have not attracted attention as hardground dwellers. Newman (1987) asserts that balanomorph barnacles evolved from Cretaceous species of Brachylepas. Commonly referred to as acorn barnacles, the Suborder Balanomorpha includes three important superfamilies well known for their encrusting lifestyle: the Balanoidea, Coronu- loidea, and Chthamaloidea. The earliest of these are the chtha- maloids, as represented by Chthamalus (Pachydiadema) creta- ceum from the Campanian of southern Sweden (Carlsson 1953). These are the unnamed barnacles referred to from the ancient rocky shores at Iv5 Klack (Surlyk & Christensen 1974; W. K. Christensen, pers. comm. 1998). Balanoids first appeared during the Early Eocene (Stanley & Newman 1980) and the earliest representative associated with a rocky shore is Balanus cf. stellaris from the Oligocene Untere Meeressand in Mainz, Germany (Neuffer et al. 1978). Extant species belonging to the genus Tetraclita fall under the Superfamily Coronuloidea (Morris et al. 1980). Representatives of the family Tetraclitidae are believed to have originated at the close of Oligocene time approximately 22 Ma before present (Stanley & Newman 1980).

ROCKY SHORES AS ECOLOGICAL SAFE PLACES

Except for bor ing b iva lves that made Gastrochaeno- l ites and acorn barnac les f rom among the Chtha- malo idea, the preponderance of rocky-shore biota rev iewed above t race the i r or ig ins to subt ida l ancestors that p redate them by a wide marg in . For many of the dominant rocky-shore species, past and present , the ext reme phys ica l requ i rements of the env i ronment in which they excel make it a haven from predatory and compet i t ive pressures exerted by other species w i th l imi ted abi l i t ies to follow after. Our data suggest that rocky shores represent a safe place that has a t t rac ted biotas cons ist ing pri- mar i ly of immigrants f rom offshore benth ic habitats, as opposed to biotas that evolved in place. This concept runs counter to the onshore-of fshore pattern of evolut ion in Phanerozo ic shel f communi t ies advocated by Jab lonsk i et al. (1983), in which ecological innovat ions are thought to ar ise in nearshore env i ronments and expand outward across the shel f at the expense of older communi ty types. There is reasonable ev idence in favor of the offshore marg ina l i za t ion of older communi t ies , but our var iant of this model is p red icated on the not ion that p r imeva l rocky shores signify an empty niche that f i l led up w i th o rgan isms er rat ica l ly th rough time. Many preadaptat ions were usefu l to the orga-

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nisms that migrated to rocky shores, while compa- ratively few evolutionary innovations arose there in place.

According to the hypothesis of evolution driven by escalation of defensive and offensive capabilities between prey and predator (Vermeij 1987), species under sustained pressure either increase their adaptability notch by notch, go extinct, or restrict themselves to safe places where the inci- dence of encounters with predators is reduced or eliminated. A safe place may provide relief from competitors and the term competitive exclusion refers to habitat shifts that result from such intraspecies pressure. Vermeij (1987) distin- guishes between a safe place and a refuge. Under some circumstances, a refuge may fill the same function as a safe place, but more generally it is a place of geographic restriction due to climatic or other physical changes. Thus, rocky shores might also provide a refuge in the more traditional sense of an isolated geographic entity, perhaps in the context of an endpoint on a diversity gradient.

A celebrated description of dynamics associated with a predator-prey relationship on present-day rocky shores concerns starfish feeding on the bivalve Mytilus californianus (Payne 1966; 1974; 1984). When the starfish, Pisaster ochraceus, was manually removed from controlled space along the outer rocky shores of Washington during trials las- ting 5 years, M. californianus expanded its distribution into the shallow subtidal. The predator- prey relationship between starfish and bivalves is now understood to have occurred during the Late Ordovician based on a specimen of Promopalaster dyeri preserved in characteristic extraoral feeding posture humped over a bivalve (Blake & Guens- burg 1994). Promytilus may have been preyed on by other starfish during the later Carboniferous, but morphologically comparable mytilid descendants eventually found a haven on intertidal rocky shores where the preadaptation of byssal attachment proved functional under conditions of wave shock that prohibited cropping behavior by starfish. Fossil starfish associated with rocky-shore deposits are reported from the Upper Cretaceous (Pietzsch 1962 Stilwell 1997), and are assigned as members of the Mesozoic rocky-shore biota. As noted previously, the earliest known colonization of Mytilus species on high-energy rocky shores dates from the Late Oligocene of Oregon (Miller & er r 1988). In situ preservation is unlikely due to the rapid post-mortem break down and disintegration of byssal threads. An alternative to preservation of mytilid shells in growth position is afforded by the example of sedimentary dikes that incorporate transported Mytilus of Pleistocene age (Zwiebel & Johnson 1995).

The Mesozoic Marine Revolution described by Vermeij (1987) relates to a major burst in the escalation of predator-prey evolution. Harper (1991) notes the coincidence during this era between the evolution of substrate-cemented bivalves and molluscivorous feeding behavior by predaceous cephalopods, crustaceans, asteroids, and fish. She found by experimention with live predator and prey subjects, that cementation renders manipulation of prey more difficult. Drilling by gastropods, however, involves little manipulation and is not inhibited by cementation of the prey (Harper & Skelton 1993). Cementation is also a preadaptation for life on more protected rocky shores and our data show evidence for progressi- ve movement of oysters into this environment beginning during the early Cretaceous.

Barnacles are supremely adapted to life on rocky shores and they offer excellent examples of predation avoidance and competitive exclusion. Trials with live predator and prey subjects undertaken by A.R. Palmer (1982) show that several species of the predatory gastropod Thais selectively attack barnacles at the margins of their lateral and oper- cular plates where drilling is most likely to be successful. It is also noted (A.R. Palmer 1982) that the Late Cretaceous radiation in muricacean gastropods (which include Thais) is coeval with the ini- tiation of design and structural changes in balanomorph barnacles. Development of tubiferous wall plates and the reduction of lateral plates in these barnacles may have been driven by gastropod predation. Ancestral balanomorphs possessed eight lateral plates, but species of the four-plated form are more common today. Plate reduction may have been a preadaptation to intertidal life that favored reduced water loss during subaerial exposure. In any case, drilling activity by predaceous gastropods on intertidal barnacles is limited to access during submergence by tides (or full tidal pools) and the reduction of lateral plates offers fewer susceptible plate boundaries as targets.

On present-day rocky shores, species of the barnacle genus Chthamalus typically occupy the highest part of the intertidal zone and endure the longest subaerial exposure times. Stanley & Newman (1980) suggest that members of the older superfamily Chthamaloidea retreated to this zone due to competitive exclusion exerted by members of the younger superfamily Balanoidea. Larger and faster-growing individuals of the species Semibala- nus balanoides at mean tide level, for example, are able to undercut and overgrow the smaller species of Chthamalus stellatus and C. montagui on the Scottish island of Skye. The latter species survive without interference in the higher part of the tidal zone because they are able to withstand a greater range of temperatures and longer periods of desic-

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cation than their competitors. The importance of competition in this case is contested by Paine (1981), who notes that reduction in overall body size among the Chthamaloidea is a long-term trend dating from the Cretaceous. He points out that smaller body size also reduces susceptibility to predation. Chthamalus often occupy small cracks on rocky shores, affording protection from predators. In reply to Paine (1981), Newman & Stanley (1981) argue that the tubiferous skeleton of the Balanoidea promotes faster growth rates that provides an advantage over the Chthama- loidea in competition for living space. They underscore the fact that peak diversity of living balanoids overlaps exactly with the bathymetric gap in chthamaloid distribution. Although Newman & Stanley (1981) consider the Cenozoic decline in chthamaloid diversity as a sign of inferiority in comparison with the explosion of balanoid species, the physiological superiority of Chthamalus within the upper tidal zone cannot be denied. Whether from predators or competitors, retreat to the upper tidal zone represents security in the ultimate coastal safe place.

Some numerically important species belonging to past or present rocky-shore communities thrive as obligate members, unable to live elsewhere in offshore environments. Others enjoy a wider range of habitats, intertidal and subtidal. Either way, most members of rocky shore communities (including predaceous gastropods with their own predators) benefit from limited predation through vertical zonal patterns that ameliorate competition in a safe place. The original conception of safe places by Vermeij (1987: 102) stipulates that the biota fin- ding shelter are low-energy species characterized by low rates of metabolism. This particular restriction clearly does not accord itself with the interpre- tation of rocky shores as a safe place, because the rate of productivity achieved by some modern rocky-shore biotas (measured as dry matter per unit area of shore per year) rivals that of any other ecosystem on land or at sea (Leigh et al. 1987). We contend that rocky shores are a special case, in which community members are able to attain high levels of metabolism within an environment that sets limitations on many potential predators and competitors.

ADDITIONAL CONTROLS ON BIODIVERSITY

KEYSTONE SPECIES

A keystone species is one whose absence results in a negative effect on community diversity. Field experiments by Paine (1966; 1974; 1984) regarding the predator-prey relationship between the starfish

Pisaster ochraceus and the byssate bivalve MytiIus californianus provide the most graphic illustration of a rocky-shore keystone species. Coexisting with M. californianus in the intertidal zone is a macrofauna of 14 other species, including limpets, chi- tons, and barnacles that also are preyed on by P. ochraceusis. When the starfish is excluded from a given area of shoreline over a period of months to years, the diversity typically falls to 8 species. Free from predation by the starfish, M. californianus and the barnacles increase their population size and crowd out other species for living space. Although fossil starfish are a rarity, their function as predators is well documented in the fossil record (Blake & Guensburg 1994). There is no reason to doubt that starfish filled the role of a keystone species in rocky shore paleocommunities dominated by mytilid bivalves through Late Cenozoic time. The gastropod NuceIla emarginata (a dogwhelk) is also a significant predator of M. californianus on rocky shores along the west coast of North America. This species, which may be considered an auxiliary keystone species, is known to co-occur with M. californianus in a Pleistocene rocky-shore deposit (Zwiebel & Johnson 1995).

Predators are not the only keystone species. Herbivores also function to clear living space in various ecosystems, including rocky shores. Field work on competitive overgrowth among encrusting coralline red algae at mean tide level on the outer coast of Washington demonstrates how Pseudoli- thophyllum lichenare can slowly eliminate all other competitors for living space in the absence of gastropod grazers (Paine 1984). Unimpeded, coralline algae with thicker crusts and raised growing margins, such as P. lichenare, are even capable of knocking over species of erect coralline algae. Gastropod grazers introduce a high level of competitive uncertainty that holds in check the superior overgrowth potential of P. lichenare and thereby promotes the coexistence of a larger number of coralline algae. As indicated in Fig. 1, the expansion of gastropods into the rocky-shore ecosystem is a Cenozoic phenomenon that reached dominance in biodiversity over all other phyla or classes during the Pleistocene. Paleoecologists are able to differentiate between gastropod predators and gastropod grazers only through the observation of extant or closely related species.

Ultimately, it is the physical environment of high- energy rocky shores that controls the effect of keystone species as an enhancement to biodiversity. Prohibition of predators due to heavy wave shock stimulates the takeover of bivalve monocultures with the potential to form structural matrices offering protection to associated small taxa. Variable conditions of tides and abatement of wave energy allow limited access to the intertidal

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by keystone predators that function to reduce the scale of monocultures and stimulate the recoloni- zation of competitive macro-organisms. Storms have the same effect as keystone species, by perio- dically tearing out patches of overgrowth where monocultures were well established and reopening the substrate to colonization by other competitors.

ECOLOGICAL LOCKING

The concept of coordinated stasis has generated much interest in testing the stratigraphic record for patterns of abrupt change that demarcate intervals of near-equilibrium in the composition of paleocommunities on the order of every 3-7 Ma. It is under debate whether or not patterns of coordinated stasis are compatible with the hypothesis of evolution and escalation advocated by Vermeij (1987). The result of continuous competition among species in a given community anticipates escalatio- nal change. The implications of coordinated stasis regarding this issue evoke two alternative scena- rios (Brett et al. 1996: 14). One possibility is that competition is minimal during most intervals of geologic time, only to intensify during points of cri- sis. The other is that competition is intense during most intervals of geologic time, but only among community members and potential newcomers. Given the level of predation and competition pressures observed in contemporary rocky-shore communities (Paine 1966, 1974, 1984), the latter sce- nario appears more likely. In this case, ecological locking is a possible mechanism by which coordinated stasis might impose episodes of long-term stability on rocky-shore communities. With a firm hold on community membership by well established species, the immigration of alien species or the succession of newly formed species supposedly would be prevented. Changes in community regime would be expected to take place during the after- math of mass extinctions or other less severe per- turbations in the environment.

Based on a rocky-shore biota from the Upper Pliocene-Pleistocene of the Almeria-N~jar Basin in southeastern Spain and comparison with other biotas dating from the Late Oligocene to the present, it is argued that certain shallow nearshore and rocky-shore communities have undergone an interval of stasis equivalent to approximately half the standard Ecological-Evolutionary Unit for the Cenozoic (Aguirre & Jim6nez 1997). Ecological Evolutionary Units (EEUs) are longer intervals of Phanerozoic time than encompassed by episodes of coordinated stasis, but the concept is similar. Under both, communities maintain stable ecological structures and diversity. A revised definition of EEUs by Sheehan (1996) enumerates 9 units, 6 of which have terminal boundaries corresponding to the major mass extinctions that impinged on the 3

evolutionary marine faunas described by Sepkoski (1997). The Jurassic and Cretaceous periods comprise a single EEU identified as M2 under Sheehan's scheme. Although the picture is likely to be clarified with additional data from this interval, rocky-shore biotas underwent a major expansion and reorganization during the later Cretaceous towards the end of M2. Additional noteworthy changes in diversity with respect to rocky-shore bivalves, gastropods, and barnacles (Figs 1,2) occurred well within the boundaries of the Cenozoic EEU identified as M3. The onshore infil- tration of predatory gastropods into rocky-shore environments is one of the most substantial Cenozoic developments to have taken place within the last EEU (Taylor et al. 1980), but it is uncer- tain whether the accompanying changes in community structure took place gradually ~r episodi- cally. The equilibrium in Neogene and Quaternary rocky-shore communities implied by Aguirre & Jim6nez (1997) is too short to correspond to an EEU and too long for an episode of coordinated stasis. It also ignores the tremendous expansion in diversity of Pleistocene rocky-shore gastropods (Fig. 1). Mass extinctions at the end of the Permian and especially at the end of the Cretaceous clearly had a negative impact on rocky-shore biotas (Figs 1,3). The available data suggest, however, that significant changes in diversity and structure also took place within rocky-shore communities during long EEU intervals. It is still premature to fit rocky-shore biotas into context with regard to shor- ter episodes of possible coordinated stasis.

A profound role in the introduction of alien species may be played by changes in geography, for example the opening of marine passages between formerly isolated oceans or the contraction of a wide ocean with coastal biotas formerly distinct from one another. Such changes usually are not associated with mass extinctions or degradation of the physical environment. As presently defined (Sheehan 1996; Brett et al. 1996), EEUs or intervals of coordinated stasis do not take into account biogeographic expansions resulting from tectonics on a regional or global scale. Recent invasions of alien species abetted by human intent or negligen- ce underscore the impact that such transfers may otherwise have through the perfectly normal evolution of landscapes. The European gastropod Littori- na littorea was introduced to North America inten- tionally as a food item, but probably also uninten- tionally with rocks used as ballast in sailing ships. This rocky-intertidal species landed in Canada during the 1840s, and then spread under its own means down the Atlantic coast, reaching the Gulf of Maine by the 1850s, Cape Cod and Long Island Sound by the 1870s, and the shores of New Jersey by the 1880s (Brenchley & Carlton 1983; Carlton

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1992). The Mediterranean mussel Mytilus gallovo- provincialis was transferred to southern California in the 1940s and to South Africa in the 1980s, where it has locally become the dominant species on high-energy rocky shores (Seed 1992). Another example concerns the Australian barnacle Elmi- nius modestus, which was introduced to the British Isles and then to much of western Europe during the late 1940s and early 1950s where it became very abundant as a rocky-shore species (Barnes & Barnes 1960). In each of these cases, ecological locking failed to repel alien species that were superior competitors. Studies on predation and competition in Recent rocky-shore communities (Paine 1966, 1974, 1984) suggest that ecological locking is very effective against known neighbors, but not stran- gers from afar that carry with them superior growth rates or broader environmental tolerances.

LATITUDINAL DIVERSITY GRADIENTS AND OTHER FACTORS

An empirical observation for many different groups of extant plants and animals is that diversity declines with distance away from the equator north or south (Rosenzweig 1995). Extant marine bivalves, for example, have been analyzed on the generic level for latitudinal variations in turnover rates (Flessa & Jablonski 1996). Little research has been undertaken with respect to fossil species from ancient ecosystems. The approach explored briefly here is to examine cumulative diversity in ancient rocky-shore biotas as a function of paleo- latitude. Potential flaws accompany any database that draws on information collected by different workers fulfilling different goals in different parts of the world. Chief among these are the investiga- tor's thoroughness and accuracy in reporting all possible fossil species from any given locality. Invertebrate paleontologists, for example, may be

more interested in one particular group of fossils than another, and rarely have the necessary back- ground to deal adequately with fossil coralline red algae. The available data on diversity of rocky- shore biotas do, however, provide a sense of conti- nuity with past worlds.

The most extensive geographic data base is for the last inter-glacial epoch (correlated with Oxygen Isotope Substage 5e, approximately 125 Ka) during the Late Pleistocene (Johnson & Libbey 1997). Latitudinal variations in composition belong to three categories: temperate mollusks, subtropical mixed mollusks and colonial corals, and tropical colonial corals. Published work regarding middle latitude biotas dominated by mollusks seems to have been undertaken with greater taxonomic care. As noted previously, the highest diversity of any rocky-shore paleocommunity reviewed for this study is represented by a mollusk-dominated fauna of 62 species from San Nicolas Island on the Pacific coast of North America (Russell 1991). The island is situated between 33 and 34 north latitude. Not surprisingly, the faunal diversity for this Pleistocene locality is basically commensurate with the Recent record for the same island. Unfortunately, many of the reports on marine terraces in the tro- pics use fossil evidence mainly to establish a bench mark for Pleistocene mean sea level. Faunal lists tend to be brief and seldom go beyond the genus level. Despite shortcomings, enough quality data are known to suggest that during the last inter-glacial epoch subtropical rocky-shore biotas pressed farther south along the west coast of Australia and further north in the Gulf of California than today (Johnson & Libbey 1997).

Figures 4 and 5 plot raw diversity data (number of species reported) for rocky-shore biotas on

FIGURE 4 - Diversity gradients based on latest Oligocene-Miocene rocky- shore biotas. Diversity at each locality is given in numbers of species on a map base for the Early Miocene from Smith et al. (1994). Gradients de la diversit~ des biotas de cStes rocheuses pour Oligoc~ne terminal-Miocene. La diversitd pour chaque localitg est donnde en nombre d'esp~ces sur une carte de Smith et al. (1994) pour le Miocene infdrieur. Data: Baluk & Radwanski (1977), Radwanski (1964, 1970) combined; Bosel & Combs (1984); Burchette (1988); Doyle et al. (1997); Eagle & Hayward (1992); Eagle et al. (1994); Fernandez & Rodriguez-Fern~ndez (1991); Gibert et al. (1996); Gutowski & Machalski (1984); Hartley & Jolley (1995); Masuda (1968); Miller & Orr (1988), Linder et al. (1988) combined; Smith (1986); and Zullo & Gurus- wami-Naidu (1982).

' -

Early Miocene . . . . Flooded continent 20 Ma ~) Number of rocky-shore species

269

maps for the latest Oligocene-Miocene and the Late Cretaceous worlds. In each case, about a dozen localities are summarized and the results are surprisingly consistent in pattern. Data from Africa, South America, and other areas showing 1- 3 species are legitimate in their representation of rocky-shore sites but almost certainly misleading with regard to diversity. They represent either an author's interest in a particular kind of organism or in the establishment of transgressive surfaces. They are plotted only to indicate potential for future work, especially in Africa and South America. Otherwise, we feel confident about the diversities reported because we have either visi- ted the localities ourselves or have questioned the authors as to their paleoecological rigor.

The Late Cretaceous and Miocene geographies share in common an open Tethys seaway, although by Miocene time it is more restricted. Maximum paleocommunity diversity, in both cases, is situated in central or eastern Europe. High Tethyan diversity during these times may have been influenced by coastal upwelling that accompanied a strong circum-equatorial current diverted through the Mediterranean region. Compared to maximum rocky-shore diversities in the European Tethys, coeval Late Cretaceous and latest Oligo- cene-Miocene diversities from high latitudes in the Pacific Ocean are lower by nearly half (Figs 4,5).

The coeval diversities of rocky-shore biotas at some low latitudes are substantially impoveri- shed, especially on the Pacific coast. A maximum diversity of only 12 species is reported for Late Cretaceous rocky shores in Baja California (Johnson & Hayes 1993). For the latest Oligocene- Miocene, a comparable diversity of 15 species is recorded in Baja California (Smith 1986). If the California and Peru currents were reversed due to the strong westward flow of Tethys and the resul- ring formation of regional alongshore density gra-

FIGURE 5 - Diversity gradients based on Late Cretaceous rocky-shore biotas. Diversity at each locality is given in numbers of species on a map base for the Campanian from Smith et al. (1994). Gradients de la diversitd des biotas de cdtes rocheuses au Crgtacd supdrieur. La diversitd pour chaque localitd est donn~e en nombre d'esp~ces sur une carte de Smith et al. (1994) pour le Campanien. Data: Bryan (1992), Crampton (1988), Gonzfilez- Donoso et al. (1983), Johnson & Hayes (1993), Kennedy & Klinger (1972), Pietzsch (1962), Pyanovskaya & Hecker (1966), Stilwell (1997), Surlyk & Christensen (1974), Zitt & Nekva- silovgt (1996), and Zullo et al. (1987).

Late Cretaceous 80 Ma

dients as predicted by Weaver (1990), then upwelling on the west coasts of the Americas would have been displaced well offshore by poleward moving currents comparable to the present-day Leeuwin Current on the west coast of Australia.

Biodiversity data from older rocky-shore localities are still too diffuse in time and space to warrant plotting on paleogeographic maps. Latitudinal segregation is apparent, however, with the Permian Eurydesma fauna of Gondwana (Runne- gar 1979). Surprisingly, no references on ancient rocky shores are cited in the massive bibliography listed by Smith et al. (1994) as sources of information on Mesozoic and Cenozoic coastlines. Ancient rocky shores provide precise information for the verification of existing paleogeographic maps and their future revisions.

CONCLUSIONS

Rocky shorelines represent the physical framework for an ecosystem with a long geological history of change and development. The earliest Precambrian rocky shores were barren and awai- ted colonization by biotas capable of enduring extremes in wave energy, subaerial exposure, sali- nity, and other physical challenges. Rocky-shore environments and the opportunities for their colonization are continually reborn, as tectonic forces create new islands or reshape old coastlines and as coastal storms more frequently clear the stage for ongoing resettlement by potential competitors. The earliest Archaic biotas were simple, consisting essentially of stromatolites. Diversity slowly increased with the cumulative addition and absorption of Paleozoic, Mesozoic, and Modern biotas that gradually migrated onshore from fully subtidal settings. This movement was partly in response to increasing predatory pressures and the exploitation of a high-stress environment, or safe place, where most predators and many potential

I~ Num

- - Land

. . . . Flooded continent Number of rocky-shore specks

270

competitors were unable to follow after. Unlike the inhabitants of other safe places characterized by their "low energy" (Vermeij 1987), the Modern tern- perate rocky-shore biota is well understood to be highly efficient in terms of annual carbon produc- tion per unit area (Leigh et al. 1987).

The overprint of biological expansion into the rocky-shore ecosystem was episodic, however, due to changes brought about by mass extinctions and the redeployment of survivors from offshore environments. New colonists brought with them prea- daptations leading to the rapid success of evolutionary biotas that displaced disaster species, such as stromatolites, from older biotas. Some evolutionary ecological units (Sheehan 1996) clearly punctuate the unfolding changes of biodiversity on rocky shores through geologic time, but the available data are inconclusive regarding the importance of coordinated stasis (Brett et al. 1996). The natural transfer of rocky-shore species from one place to another via biological invasions of alien species due to prehistoric changes in geography unders- cores the fragility of ecological locking as a mechanism for long-term stability on a time scale commensurate with coordinated stasis. Such invasions are completely divorced from deterioration of the physical environment or other catastrophes often associated with punctuational events.

Limits on the biodiversity of Recent rocky-shore biotas are controlled by keystone species. Compa- rable biological relationships among rocky-shore species certainly existed in the past with the development of the Modern biota in late Mesozoic and Cenozoic times. Such relationships are more difficult to trace back through the earlier Mesozoic and Paleozoic eras. Attachment to the substrate is the single most important feature held in common by most rocky-shore organisms, regardless of geological age. The study of ancient rocky-shore biotas is distinguished from those of most other ecosystems by the prevalence of in situ preservation on clearly recognized geological unconformities that allows confidence in paleocommunities.

Studies on ancient rocky shores show much potential to interface with the reconstruction of paleogeographies, as the unconformities that deft- ne rocky shores offer highly precise markers of paleoshorelines and changes in sea level. Patterns in the paleobiogeographic distribution of rocky- shore biotas will become increasingly clear as additional study sites are described and investi- gators begin to move away from local or regional summaries toward global integration of data along time lines. Diversity gradients of various kinds, depending on paleo-ocean width and the configuration of coastal upwelling should become more evident, as should centers of species disper-

sal. The possible global relationships interpreted here for rocky-shore biotas of Late Cretaceous and latest Oligocene to Miocene times provide a focal point for expanded paleobiogeographic studies.

The viewpoint that fossilization is unlikely to occur in high-energy settings where the processes of erosion tend to surpass those of deposition (Schopf 1978; Valentine 1980; Bambach 1986) has proven to be misleading. Many outstanding studies on rocky-shore biotas contributed during the last decade by paleontologists from all corners of the world are emphasized in this synthesis. Much remains to be done in order to fill out important parts of the story that remain blank, but the occurrence of rocky-shore biotas should no longer be regarded as surprising novelties. Almost nothing is known about rocky-shore biotas from the Devonian and Triassic periods or the Paleocene Epoch and we hope this summary may encourage paleontologists to seek new discoveries from the fossil record especially for those transitional intervals. All ecosystems have a geological history, some longer and richer in paleontological details than others. In a living world where the rapid expansion of human populations threatens biodiversity as never before, it is our greatest hope that the value we attach to all ecosystems may be enhanced by our realization of their remarkable transformations through prehistoric time.

Acknowledgments - The authors are grateful to D.B. Blake (University of Illinois, Urbana), W. K. Christensen (Geological Museum, University of Copenhagen), P. Hoffman (Harvard Uni- versity), and T.J. Palmer (University of Wales, Aberystwyth) for taking our questions seriously and answering them with alacri- ty. An early draft of this paper was reviewed by M.A. Wilson (College of Wooster) and P.W. Skelton (Open University, Milton Keynes), whose attention to detail helped significantly to impro- ve the final version. We acknowledge the fellowship and good will shared with us through a far-ranging exploration of ancient rocky shores in the company of J. Aguirre (University of Granada), Rosa Domenech (University of Barcelona), Fawzi H. Hamza (Ain Shams University), J. Kriz (Czech Geological Sur- vey), J. Ledesma-V~zquez (Universidad Autonoma de Baja Cali- fornia), J. Martinell (University of Barcelona), W.S. McKerrow (Oxford University), M. Mergl (Pedagogick~ Fakulta Plzen), A. Radwanski (Institute of Geology, Warsaw University), J. Rong (Nanjing Institute of Geology and Palaeontology), A. Ziko (Zagazig University), and J. Zitt (Czech Academy of Sciences). Former students at Willliams College (especially M. Hayes, H. Lescinsky, L. Libbey, K. MacLeod, M. Simian & J. Zwiebel) gent- ly helped guide their elders to new ways of seeing and thinking about ancient rocky shores. We are indebted to all, although the sole responsibility for the interpretations offered herein remain ours alone.

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diversification of rocky-shore biotas through geologic time

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