E L S E V I E R Review of Palaeobotany and Palynology 86 (1995) 265-285

REVIEW OF

PALAEOBOTANY AND

PALYNOLOGY

Taxonomy of fossil coralline algal species: Neogene Lithophylloideae (Rhodophyta, Corallinaceae)

from southern Spain

Juan Carlos Braga, Julio Aguirre Departamento de Estratigrafia y Paleontologia, Universidad de Granada, Campus Fuentenueva s/n, 18002 Granada,

Spain

Received 30 March 1994; revised and accepted 9 September 1994

Abstract

The anatomy of coralline algae is relatively simple. This, together with high intraspecific variability, reduces characters used as diagnostic criteria in delimiting species in present-day coralline algae to a very few, most of which can be recognized in fossil representatives of this family. Similar taxonomic procedures may thus be used at the species level both in modern and fossil coralline algae. Extant species of this subfamily can be recognized in fossil material. This study of Lithophylloideae from the Neogene of southern Spain describes five species (Lithophyllum dentatum, L. incrustans, L. nitorum, L. orbiculatum, and L. pustulatum), which are all found in the present-day Atlantic and western Mediterranean. Palaeontological studies on coralline algae, at least those from the late Cenozoic, have to take into account modern species and their current taxonomy, as coralline algal species have long stratigraphic ranges and many extant species were presumably already present in the Neogene.

I. Introduction

Traditionally, species taxonomy of fossil non- geniculate Corallinaceae has been separated from that of present-day coralline algae. Names applied to recognized fossil species have in most cases been different f rom those of modern representatives of the group and are based exclusively on fossil material and types, even when diagnostic criteria in delimiting fossil species have been quite similar to those used by botanists. Exceptions have been the identification in Cenozoic deposits of some particularly distinct coralline species, such as Lithoporella melobesioides (Foslie) Foslie (i.e. Lemoine, 1939, 1976) and scarce references to a few modern taxa among inventories of many strictly fossil species (i.e. Johnson, 1961, 1964; Segonzac, 1990). As a consequence of this custom,

0034-6667/95/$9.50 © 1995 Elsevier Science B.V. All rights reserved SSDI 0034-6667(94)00135-9

tens of established coralline species with long temporal ranges during the Cenozoic suddenly become "extinct" just before the Holocene or the Quaternary, which seems to be a taxonomic artifact in species survivorship.

Using the Neogene Lithophylloideae of southern Spain, our aim is to demonstrate that most of the diagnostic criteria used by botanists in delimiting coralline algae species can be recognized in fossil material. Therefore, the taxonomy, and sometimes the names, of modern corallines can be applied to fossil specimens. We stress the importance of taking into account the high intraspecific variabil- ity affecting the relatively simple vegetative and reproductive structures of these algae. This vari- ability restricts the number of diagnostic features but also implies that extensive descriptions and good illustrations are required to convey an ade-

266 J. C. Braga, J. Aguirre/Review of Palaeobotany and Palynology 86 (1995)265 285

quate idea of the broad morphological spectrum of a species.

Studies on lithophylloids in the British Isles and southern Australia published in the last decade (Edyvean and Moss, 1984; Chamberlain, 1986, 1991; Chamberlain et al., 1988, 1991; Woelkerling and Campbell, 1992), and redescriptions of type collections of coralline taxa (Woelkerling, 1983; Woelkerling et al., 1985; Chamberlain et al., 1988, 1991; Chamberlain, 1991; Woelkerling and Campbell, 1992) provide useful information on modern species of this subfamily. Detailed descrip- tions of plant anatomy included in these papers allow comparisons between fossil and present-day specimens of the group to be made, and give a precise idea about intraspecific variability of vege- tative and reproductive characters. At the same time, these descriptions clarify the nomenclatorial problems, making the status of many taxa accessi- ble to palaeontologists.

2. Vegetative and reproductive anatomy of non- geniculate coraUine algae

pendicular to the basal layer from primigenous- filaments cells (Woelkerling, 1988). Both types of construction may co-exist in a single plant in some genera (e.g. Woelkerling and Campbell, 1992). One coralline genus (Tenarea) shows isobilateral organization instead of dorsiventral, in which case two central rows of primigenous filaments give way on both sides to short postigenous ones (Woelkerling, 1988).

The sexual cycle of non-geniculate coralline algae is presumed to consist of a gamete-producing phase (haploid), a carpospore-producing phase (diploid) and a tetra/bispore-producing phase (dip- loid) (Chamberlain, 1987; Woelkerling, 1988). Gametes and spores are produced in conceptacles, which are chambers enclosing the reproductive structures. The vegetative anatomy of gamete- and tetra/bispore-producing phases is thought to be essentially similar in most corallines, while carposporophytes (carpospore-producing phase) are very small thalli which develop inside concep- tacles of the female gamete-producing plant (Woelkerling, 1988).

According to Woelkerling (1988) the thallus structure of non-geniculate corallines is made up of filaments joined pseudo-parenchymatously. Most plants are organized dorsiventrally and two types of construction can be recognized. Monomerous construction comprises a single system of branching filaments (Woelkerling, 1988), which grow subparallel to the thallus surface and then curve to become more or less perpendicular to the thallus surface. The portion of the thallus in which filament orientation is subparallel to the surface is called the core (Woelkerling, 1988), a term equivalent to medulla (Chamberlain, 1990) and the traditional term hypothallium. The remainder is the peripheral region (Woelkerling, 1988) or cortex (Chamberlain, 1990), equivalent to the traditional perithallium. Dimerous construc- tion consists of two systems of filaments. One constitutes a basal (ventral) layer of primigenous filaments (axial filaments; Chamberlain, 1991) and produces the lateral expansion of the thallus, The other system comprises postigenous filaments (erect filaments; Chamberlain, 1991) arising per-

3. Diagnostic characters in present-day coralline species

Descriptions of present-day coralline species include detailed observations about many different characters from external appearance of plants to reproductive or developmental features (e.g. Chamberlain, 1986, 1988; Steneck and Paine, 1986; Chamberlain et al., 1988, 1991; Woelkerling and Campbell, 1992). These accounts give useful infor- mation on thallus morphology, vegetative and reproductive anatomy, and their variability in indi- vidual coralline species. Many of these characters have been used for delimiting species throughout the history of taxonomic research on coralline algae. Woelkerling and Campbell (1992) have listed up to 81 qualitative and quantitative charac- ters applied for species delimitation among litho- phylloids in some selected publications since the beginning of this century. In recent papers dealing with species taxonomy of corallines, however, diag- nostic features allowing different species to be distinguished are relatively few and most, if not

J. C. Braga, J. Aguirre/Review of Palaeobotany and Palynology 86 (1995) 265-285 267

all, are preservable in fossil plants. These features are usually restricted to size, shape, and location of tetra/bisporangial conceptacles, features of con- ceptacle roof and pore canal, and size, shape, and arrangement of cells in the different parts of vegeta- tive tissues (Table 1). External morphology of plants may be an additional, less diagnostic charac- ter (e.g. Adey and Adey, 1973; Chamberlain et al., 1988, 1991).

Diagnostic criteria are few as coralline algae show high intraspecific morphological variability besides the relatively simple anatomy summarized above. Sources of this variability can be grouped in two main types: reproductive and vegetative.

3.1 Reproductive

Most corallines are dioecious, i.e. male and female gametes develop in separate plants. Leaving aside carposporophytes, three different types of plants can be expected in a coralline species: male, female, and tetra/bisporangial. In well-preserved modern material, reproductive features within the conceptacles of each type of plant are clearly distinct. Spermatangia in male conceptacles are easily distinguished from carpogonia in female and from spores in tetra/bisporangial conceptacles. From a palaeontological point of view it is interes- ting that, in addition, the general conceptacle shape of the three types of plants is different in many groups of corallines. Tetra/bisporangial concepta-

cles are multiporate while the gamete-producing conceptacles are uniporate in the subfamily Melobesioideae (sensu Woelkerling, 1988). In the other three subfamilies all conceptacles are unipor- ate, but there sometimes are differences in shape and size of conceptacles among the different reproductive types of plants, although no general pattern can be established for the entire family.

3.2 Vegetative

The morphology of corallines is highly suscepti- ble to ecophenotypic factors (sensu Raup, 1972). As they grow on a substrate, changes in substrate topography and interactions with other sessile organisms, including conspecific plants, induce modifications of thallus morphology. Other environmental factors, such as hydraulic energy (Adey and Macintyre, 1973; Bosence, 1976), light intensity/depth (Adey and Macintyre, 1973), differences in microenvironment (i.e. shallow- subtidal sites vs. tidal pools; Steneck and Paine, 1986) and grazing (Steneck and Paine, 1986) also induce changes in the final form of the plant. The external appearance of coralline species is therefore highly variable and, except for some peculiar traits in particular species, the general plant morphology can not be considered diagnostic.

Internal anatomy is also affected by the environ- ment. Changes in cell organization in response to changes in the substrate have been reported (e.g.

Table 1 Diagnostic characters in lithophylloid species used (x ) in recent phycological papers

Chamberlain et al. Chamberlain et al. Chamberlain (1991 ) Woelkerling and (1988) ( 1991 ) Campbell (1992)

Tetra/bisporangial conceptacle Location Roof elevation x :< Diameter x Shape x x Pore canal" Columella x

Thallus structure a x x Origin of branches Cell arrangement x x

X X

X X

X X

"Some of the features considered in these characters are not preserved in fossils.

268 J. C Braga, J. Aguirre/Review of Palaeobotany and Palynology 86 (1995) 265~85

loss of the basal region in some unattached plants; Penrose and Woelkerling, 1988) as well as lateral expansion of filaments over grazing wounds (Steneck and Paine, 1986).

Development of protuberances, branching, and curvatures of crusts imply constructional modifi- cations of cell size and shape. As is shown in Fig. 1, growth of a protuberance or branch has to be achieved by differential size and shape of cells according to their location. Differential cell sizes and changes in shape are needed in a simple crust curvature to accommodate the differences in volume between the inner and outer sides of the curve. Periodic changes in growth rate also produce changes in cell size (mainly cell height) resulting in tissue zonation frequently reported in descriptions of corallines (e.g. Lemoine, 1939; Bosence, 1983). Since these features appear as the thallus develops, plant ontogeny has to be consid- ered as a source of variability. Protuberances and branches may arise from an initially laminar thal- lus later in the ontogeny, and zonation needs more than one stage of growth to develop.

All this makes coralline morphology highly vari- able in most analysable features, restricting those characters with a diagnostic value at the species level. Good descriptions must take into account this variability and attempt to explain how mor-

protuberances

coralline thallus l 500 ~m

| l U l l [ ",g,~ ~

Fig. 1. Diagram showing changes in cell size and shape caused by the development of a protuberance in a coralline thallus. Cells in the central part of the structure are longer and trapezoid to accomodate volume differences. Simplified from a thin section of L. dentatum (Sample Ju-I-2, Lower Pliocene, Almeria Basin).

phological variations are produced, i.e. relating changes in size and shape of cells to formation of protuberances or to zonation of growth.

4. Diagnostic characters in fossil species

Descriptions of fossil coralline species usually refer to a few anatomical characters, mainly the general shape, size, and thickness of the thallus, and the size and arrangement of cells. In some cases the size and, rarely, the shape of conceptacles are also described. As pointed out by Bosence (1983), cell and conceptacle sizes are in most cases considered as the main taxonomic criteria at the species level. Hundreds (!) of coralline species have been established on the basis of cell size, sometimes with conceptacle size and cell shape and arrange- ment being taken into account as well. The descrip- tions of these new species, however, refer to cell sizes only by giving their range, in the best of cases, making further comparisons almost impos- sible (Bosence, 1983). To demonstrate the diffi- culties involved, Fig. 2 represents cell-size ranges of species ascribed to Lithophyllum by Lemoine (1918a,b, 1924, 1926, 1928a,b, 1929, 1939). Except for a few species, cell-size ranges overlap to a great extent, and no discrimination can be made using these data. Rarely (e.g. Bosence, 1983), changes in cell size have been related to particular aspects of thallus development, such as protuberances and zonation. Useful cell-size descriptions must include the number of measurements made, means, stan- dard deviations, and ranges (Bosence, 1983). The relationship of cell-size and cell-shape changes to constructional features such as thallus curvatures, protuberances, lateral expansions, and zonations should be stated as well.

The lack of adequate original descriptions of type material of fossil taxa is quite common in many groups of organisms, and revisions of origi- nal collections need to be undertaken to update and clarify taxonomy. In the case of fossil coralline algae, the situation is made worse because a sig- nificant proportion of species types or syntypes have been lost or cannot be located at the moment. The status and distinctive characters, if any, of a large number of published coralline species cannot

J. C Braga, J. Aguirre/Review of Palaeobotany and Palynology 86 (1995) 265-285 269

I.tm 70-

60-

50-

40. ==

30"

20.

10,

Ilm 70-

:hallial' cells 60-

;o 2'o 3b.~ width

number of overlapping species

50-

40-

_0 30-

20-

lO-

'perithallial' cells

10 20 30~m width

~ ] 0 ~ 2-3 ~ 4-5

6-7 I s-o I 10-11

Fig. 2. Cell-size ranges of coralline species assigned to Lithophyllum by Lemoine (1918a,b, 1924, 1926, 1928a,b, 1929, 1939). Except for a few cases, cell-size ranges significantly overlap, making the use of these data in delimiting species difficult.

be assessed, making the use of their names by later authors very interpretative and often meaningless.

In summary, although the observable features in extant corallines are more numerous than in fossil ones, most diagnostic characters used by botanists in delimiting modern species can be recognized in fossil plants and some have tradition- ally been used in palaeontological studies of these algae. Size, shape, and arrangement of cells in the different parts of the vegetative plant and size, shape, and location of tetra/bisporangial concepta- cles are readily recognizable in fossil specimens. No taphonomic processes prevent one from trying to identify present-day species in ancient corallines, at least in those from young Cenozoic deposits. Recent work on fossil coraUines has already shown that taxonomic criteria currently used by botanists at generic and subfamily levels can be identified in fossil material (Bosence, 1991; Braga et al., 1993). Below is a study of lithophylloids from the Neogene of southern Spain (Fig. 3), demonstrat-

ing that all the recorded corallines of this subfamily can be assigned to well-know modern taxa.

5. Systematic palaeontology

Division RHODOPHYTA Wettstein, 1901 Class RHODOPHYCEAE Rabenhorst, 1863 Order CORALLINALES Silva and Johansen, 1986 Family CORALLINACEAE Lamouroux, 1812 Subfamily LITHOPHYLLOIDEAE Setchell, 1943

Type genus Lithophyllum Philippi, 1837

This subfamily includes non-geniculate corallines in which cells of contiguous filaments are normally joined only by secondary pit- connections. Cell fusions are very rare or absent. Tetra/bisporangial conceptacles are uniporate, lacking apical plugs (Woelkerling, 1988).

In fossil Lithophylloideae, filaments appear as continuous, aligned rows of cells clearly delimited from adjacent ones. This type of arrangement is easy to distinguish from that of the subfamilies Mastophoroideae and Melobesioideae both in thin section or using SEM techniques (Braga et al., 1993). In these latter subfamilies, cell fusions interconnecting adjacent filaments can be observed and the tissue has a spongy appearance with irregularly shaped and sized cells. Secondary pit-connections can sometimes be observed with SEM (Braga et al., 1993). The subfamily Choreonematoideae, including only the small, endophytic genus Choreonema, never found as a fossil, has a similar type of organization with well- defined adjacent filaments, lacking any interfila- mental cell connections (Woelkerling, 1987).

The corallines belonging to the subfamily Lithophylloideae recorded in the Neogene deposits of southern Spain can be assigned only to Lithophyllum. Other lithophylloid genera, such as Ezo and Tenarea (as circumscribed by Woelkerling et al., 1985), have never been found as fossils.

Genus Lithophyllum Philippi, 1837

Lectotype species: Lithophyllum incrustans Philippi, 1837: 388; designated by Foslie (1898a).

270 J.C. Braga, ,L Aguirre/Review of Palaeobotany and Palynology 86 (1995) 265 285

N Neogene basins

basement 1 O0 km

Fig. 3. Neogene basins in southern Spain and localities studied.

Here we follow the generic circumpscription of Lithophyllum proposed by Campbell and Woelkerling (1990) and Woelkerling and Campbell (1992), including Titanoderma as a younger het- erotypic synonym of Lithophyllum. According to Woelkerling and Campbell (1992), characters delimiting this genus from other lithophylloids are the dorsiventral organization of crustose portions of the thallus and the absence of haustoria.

Descriptions of modern species of Lithophyllum show clearly distinct shapes of male, female and tetra/bisporangial conceptacles. Spermatangial conceptacles are smaller than the other types, being flat-triangular in section. Female and tetra/bispor- angial conceptacles are quite similar in shape but, in the latter, the center of the floor is usually raised by the presence of sterile filaments (columella). Carposporangial conceptacles are enlarged female conceptacles but do not have a clearly distinct shape. The morphological features of the concepta-

cle chambers in Lithophyllum species allow male and tetra/bisporangial plants to be differentiated in fossil samples (e.g. Bosence, 1983).

Many Cenozoic species previously included in this genus should be transferred to genera of the subfamily Mastophoroideae (Braga et al., 1993). The recognition of the type of interfilamental cell connections in fossil material leads those species with cell fusions to be excluded from Lithophyllum. This supraspecific taxonomic character has not traditionally been applied in palaeontological studies, and all corallines with uniporate concepta- cles and a multistratose thallus lacking heterocysts have been assigned to Lithophyllum. The actual number of species belonging to this genus in Cenozoic deposits is probably very low. In fact, we have found only five Lithophyllum species in the Neogene of southern Spain.

J. C Braga, J. Aguirre/Review of Palaeobotany and Palynology 86 (1995) 265-285 271

Comments: Campbell and Woelkerling (1990) con- sidered Titanoderma a heterotypic synonym of Lithophyllum. In the southern Australian litho- phylloids, palisade and non-palisade squarish cells coexist in primigenous filaments of the dimerous portions of thalli, both in single specimens and in different specimens of a population. According to these authors, Titanoderma and Lithophyllum cannot, therefore, be delimited by the presence or absence of palisade cells. To maintain the genus, Chamberlain et al. (1991) redefined Titanoderma as "a lithophylloid genus which is non-frondose, non-parasitic and does not have a back-to-back thallus. It has, in juvenile and regenerating plants, a bistratose margin with oblique, palisade hypo- thallial cells. Cells of the unistratose hypothallial layer remain predominantly palisade throughout the plant". In a similar argument, Chamberlain (1991) considered the predominance of palisade in Titanoderma and squarish cells in Lithophyllum to be basis enough for separating the two genera. In addition, bistratose margins occur only in plants with predominantly palisade cells in primigenous filaments (Chamberlain, 1991). This latter approach was followed by Braga et al. (1993) in a recent revision of Cenozoic fossil coralline genera. Woelkerling and Campbell (1992) found, however, that in the same species dimerous por- tions of some plants show bistratose margins but many other plants lack bistratose margins or have no detectable margins of dimerous construction; that is, they have monomerous construction, making it impossible to assess this diagnostic char- acter. They concluded that the presence or absence of a bistratose margin is not a significant character at the generic level and that, consequently, there is no evidence for maintaining two separate genera.

In the fossil lithophylloids of the southern Spanish Neogene, two distinct groups of plants occur. In one, cells of primigenous filaments are mainly squarish, i.e. non-palisade. The other group comprises plants that can be included in a single species and show a majority of palisade cells in primigenous filaments. Although the evidence pro- vided by Woelkerling and Campbell (1992) pre- vents two separate genera from being formally delimited, they probably represent two evolution- ary lines within Lithophyllum.

Lithophyllum dentatum (Kiitzing) Foslie, 1898b: 10

Basionym: Spongites dentata KtRzing, 1841: 33.

See Woelkerling (1985, p. 125) for a detailed account of the nomenclatorial history and refer- ences to this species in botanical literature. Woelkerling (1985, figs. 1-8) illustrated the holo- type specimen of L. dentatum, from the Gulf of Naples (Italy), housed at the Rijksherbarium, Leiden, The Netherlands (specimen L 943..7..69).

External appearance: Fossil representatives of this species occur as encrusting plants up to 1.2 mm thick, which develop wedge-like expansions (Plate I, 1 ) in any direction and irregular protuber- ances caused by curvature of the thallus. When two thalli contact, they curve outwards forming wedge-like crests. All this results in an external appearance with a complex and highly incised relief sometimes recalling "desert-rose" structures.

Vegetative anatomy: Thallus dimerous or dimerous and monomerous in the same plant. In portions of the thallus showing dimerous construction, primigenous filaments run parallel to the substrate (Plate I, 2). These cells are 10-18~m (mean 14.6/~m, sd 2.6) in length and 15-34/~m (mean 24.8 ktm, sd 5) in height. Fig. 4 provides a sketch of cell orientation and dimensions used in this and other species descriptions in the text.

Postigenous filaments are perpendicular to the primigenous ones. Lateral alignment of contigu- ous-filaments cells is well defined, and the thallus shows a regular net-like structure (Plate I, 1-4). Cells are 8-22#m (mean 12.9/~m, sd 3.1) long and 6-12/~m (mean 7.9/~m, sd 1.2) in diameter. Original postigenous filaments may expand later- ally on the substrate, as well as in any upward direction, and then these portions of the thallus acquire a monomerous organization (a single set of filaments) with coaxial arrangement in the ventral side of the crust (Plate I, 3) and the centre of the wedge-like expansions (Plate I, 1). Well- defined lateral alignment of cells determines the coaxial nature of the cell organization. In the coaxial areas, cell size and shape adjust to the differences in volume caused by thallus expansion

272

P L A T E I

J. C. Braga, Z Aguirre/Review of Palaeobotany and Palynology 86 (1995) 265 285

J.C. Braga, J. Aguirre/Review of Palaeobotany and Palynology 86 (1995) 265-285 273

e

i

ce l ls

P

P

pr conceptacle

Fig. 4. Diagrams representing dimensions measured in cells and conceptacles; pr=cell of primigenous filament, p--cells of postigenous filament, i= initials, e= epithallial cell, h = height, /=length, d=diameter (modified from Chamberlain et al., 1988).

(Fig. 1; Plate I, 1, 3). Cell length may reach 55/~m in the centre of coaxial organization.

Epithallial cells have not been recognized in samples studied.

Conceptacles: Male conceptacles have small cham- bers triangular in section, measuring 60--84 #m (mean 74 #m, sd 9.1) in diameter and 18--24/~m (mean 20/~m, sd 3.3) in height. The roof is slightly convex-upward with a short pore-canal (Plate I, 4). The tetra/bisporangial conceptacles are bean- shaped in section with a raised chamber bot tom reflecting the original columella. Chambers are 262 339 #m (mean 294.8 #m, sd 27.3) in diameter and 108-154/zm (mean 140.8/~m, sd 18.7) in height. The pore canal is cylindrical to slightly bulbous, with parallel to gently curved sides in section (Plate I, 5). Conceptacle chambers in some plants, similar in size but all with a flat bo t tom

may be interpreted as carposporangial concepta- des. All types of conceptacles are sunk in the thallus. No unfertilized, untransformed female conceptacles have been found.

Remarks: L. dentatum can be distinguished from L. incrustans by: ( 1 ) well-defined lateral alignment of cells of contiguous filaments; (2) slightly larger conceptacles; (3) and lateral and wedge-like expan- sions of thallus with well-developed coaxial arrangement of cells (Tables 2 and 3).

Distribution: This species has been recorded in the Tortonian temperate carbonates of the Granada Basin (Escflzar), in the Tortonian reefs of the Almanzora Corridor (Purchena), in the Upper Miocene temperate carbonates of the Sorbas Basin (Rio Aguas), and in the Pliocene temperate car- bonates of the C~idiz province (Cabo Roche and San Roque), and Los Juanorros and Almeria in the Almeria Basin (Fig. 3). Present-day records of the species need verification. Outside the western Mediterranean it has been reported from the Nor th Atlantic (France and Ireland) (Hammel and Lemoine, 1953). It occurs on the Mediterranean and Atlantic coasts of southern Spain (Cabo de Gata, Adra, Algeciras, and C~idiz, pers. observ.).

Lithophyllum incrustans Philippi, 1837:388

Lectotype: Designated by Woelkerling (1983, p. 315) on the single specimen from Philippi's original collection from Sicily (Italy), housed at the

PLATE1

1. Protuberance of L. dentatum thallus. The core is coaxial. Size of cells changes from center to periphery to resolve volume differences caused by growth of protuberance. Sample TB-S-1. Almeria (Almeria Basin). Pliocene. Scale bar= 250 pan.

2. Dimerous portion of an L. dentatum thallus. Primigenous filaments (arrows) composed of rectangular cells. Postigenous filaments arise at right angles from cells of primigenous filaments. Sample TB-S-7. Almeria (Almeria Basin). Pliocene. Scale bar = 50 Ima.

3. Monomerous portion of an L. dentatum plant. Coaxial core at the ventral side of thallus. Note longer cells in the centre of coaxial arrangemet. Sample TB-S-12. Almeria (Almeria Basin). Pliocene. Scale bar= 100 ~n.

4. Postigenous filaments and male conceptacles of L. dentatum. Sample TB-S-5. Almeria (Almeria Basin). Pliocene. Scale bar = 100 ~tm.

5. Tetra/bisporangial conceptacle of L. dentatum. The raised floor is interpreted as columella remains. Note long pore canal. Sample AZRA-1. Rio Aguas (Sorbas Basin). Upper Miocene. Scale bar = 100 ~tm.

6. Postigenous filaments and tetra/bisporangial conceptacles in an L. inerustans protuberance. Note coaxial arrangement of cells in center of protuberance (bottom). Conceptacles show a raised floor, interpreted as a columella relic. Sample TJ-31. Bayarque (Almanzora Corridor). Upper Tortonian. Scale bar= 250 ~tm.

274 J. C. Braga, £ Aguirre/Review of Palaeobotany and Palynology 86 (1995) 265-285

Table 2 Cell and conceptacle dimensions, and diagnostic characters in the species studied

L. dentatum L. incrustans L. nitorum L. orbiculatum L. pustulaturn

n= 18 n=32 n-31 n= 18 n=90

10-18 6-12 8 15 6 11 6-14 14.6 ± 2.6 9.4_+ 1.9 11.3 _+ 2.2 8 ± 1.3 9.7 _+ 1.7 15-34 6-17 10 24 6 14 8-77 24.8_+5 10.8_+3.1 18.1 _+3.9 8.9_+2.3 36.6_+ 15.4

n=62 n - 6 3 n= 121 n=96 n=90

8 22 (up to 55 in 8-22 (up to 37 in 6-22 6 12 14 42 coaxial coaxial arrangement) arrangement) 12.9_+3.1 13.3+2.9 11.6_+3.3 8.4_+ 1.3 27.3+6.4 6-12 6-11 6-22 6 11 6 14 7.9_+ 1.2 7.9_+ 1.1 10.6_+2.7 7.9+ 1.1 9.7-+ 1.7

Yes No Yes No Yes

n= 13 n - 5 4 n= 11 n= 13 n=26

262-339 180-300 216 396 156 204 192-408 294.8 ± 27.3 250.7 +_ 23.1 293 _+ 66.7 193.4 _+ 15.9 307 ± 56.9 108-154 72 144 84-168 84 108 78-150 140.8_+18.7 102.8±15.3 122_+28.5 90.5_+8.6 117+19.2

No No Yes No Yes

Cylindrical Cylindrical Conical Conical Cylindrical

n = 12 n = 10 n = 8 60 84 72 108 114 252 74_+9.I 92.4_+9.9 173+50 18 24 24 30 30-54 20+_3.3 26.4_+3.1 44_+7.8 Coaxial Longer cells in Thin thalti Palisade cells, thin arrangement, wedge- conceptacle roof thalli, applanate like protuberances branches

Primigenous- filament cells

Length range Mean + sd Height range Mean ± sd

Postigenous- filament cells

Length range

Mean ± sd Diameter range Mean ± sd

Lateral cell alignment

Tetra/bisporangial conceptacles

Diameter range Mean + sd height range Mean + sd

Roof elevation

Pore canal

Male conceptacles Diameter range Mean + sd Height range Mean + sd Other

n = number of measures; sd = standard deviation. All dimensions in/~m.

R i j k s h e r b a r i u m , Le iden , T h e N e t h e r l a n d s ( n u m -

be red L943, 10.. .34). W o e l k e r l i n g (1983, figs.

1 5 - 2 3 ) i l lus t r a t ed the l ec to type s p e c i m e n a n d also

r e fe r red to the m a n y i n t e r p r e t a t i o n s o f the species

in b o t a n i c a l l i t e ra tu re m a d e w i t h o u t c o m p a r i s o n

wi th Ph i l i pp i ' s o r ig ina l co l l ec t ion . A c c o r d i n g to

W o e l k e r l i n g (1983, p. 317), " p u b l i s h e d r eco rds o f this species m u s t be r e g a r d e d wi th s u s p i c i o n " unt i l

r ev i s ions i n v o l v i n g c o m p a r i s o n w i t h type m a t e r i a l a re u n d e r t a k e n .

Synonym: L i thophy l lum viennotii L e m o i n e , 1929: 269, figs. 3 - 5 , p la te 24, figs. 1 - 2

E x t e r n a l appearance: Fossi l e x a m p l e s o f L. incrus- tans o c c u r as mass ive enc rus t i ng o r p r o t u b e r a n t p l an t s a t t a c h e d to a h a r d subs t ra te . C r u s t o s e par t s o f p l an t s a re u p to 2 m m thick. P r o t u b e r a n c e s are up to 4 m m wide at the i r base a n d up to 6 m m high. In m a n y cases they are wide r in the dis ta l p o r t i o n , a c q u i r i n g a b u l b o u s shape. A d j a c e n t p ro - t u b e r a n c e s m a y fuse at the i r ex t remes , g iv ing the p l an t a " b r a i n - l i k e " ex te rna l a p p e a r a n c e .

T h e g r o w t h hab i t seems to h a v e been c o n t r o l l e d by e n v i r o n m e n t a l t u rbu lence . Thus , mass ive crus ts d e v e l o p e d in t u r b u l e n t e n v i r o n m e n t s , s o m e t i m e s as c o m p o n e n t s o f r h o d o l i t h s wi th f r e q u e n t over -

.L C. Braga, J. Aguirre/Review o f Palaeobotany and Palynology 86 (1995) 265-285 275

Table 3 Dichotomous key to Lithophyllum species in the Neogene of southern Spain

l a. Primigenous filaments composed of predominantly squarish

2a.

lb .

non-palisade, cells Conceptacle pore canal cylindrical to slightly bulbous

3a. Well-defined lateral alignment of cells. Coaxial arrangement at the ventral side of monomerous portions and in the centre of protuberances Wedge-like expansions of thallus ..... L. d e n t a t u r a

3b. Lateral cell alignment absent or poorly defined. Thallus thick and protuberant . . . . . . . L. i n c r u s t a n s

2b. Conceptacle pore canal conical 4 a . Well-defined lateral alignment of cells. One or

two layers of cells in conceptacle roof longer than surrounding cells . . . . . . . . . . . . . . . . . . . . . . . . . L. n i t o r u m

4b. Lateral cell alignment absent or poorly defined. Thallus thin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. o r b i e u l a t u m

Primigenous filaments composed of predominantly palisade cells. Conceptacles raised. Floors of tetra/bisporangial conceptacles one to three cell layers below thallus surface. Thallus thin, branches applanate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . L. p u s t u l a t u m

turning (e.g. shallow-coastal and beach deposits; Braga and Martin, 1988, as L. v i enno t i i ; Aguirre et al., 1993). Knobby thalli grew preferentially in quieter, sheltered settings.

V e g e t a t i v e a n a t o m y : Thallus dimerous or dimerous and monomerous in the same plant. Cells of primigenous filaments (Plate II, 1) are 6 - 1 2 # m (mean 9.4/tm, sd 1.9) in length and 6--17 #m (mean 10.8 #m, sd 3.1) in height.

Postigenous filaments are well-developed (Plate I, 6). Cell filaments are clearly distinct and conspicuous since cells of adjacent filaments are only joined by secondary pit-connections and are neither fused nor horizontally aligned (Plate I, 6; Plate II, 1-3). Cells in massive thalli are 8--22 #m (mean 13.3 #m, sd 2.9) long and 6-11/~m (mean 7.9/~m, sd 1.1) in diameter. When a protuberance is formed, cell filaments arch upwards to the periphery in a fan-like array, which produces changes in cell size, shape, and number to resolve volume differences between the center and outer side of the structure (Plate I, 6). In the central part of the protuberances, cells become longer (up to 37 #m) and trapezoidal in section, and diminish in length towards the periphery, acquiring the dimensions common in non-protuberant thalli. In addition, cells are more numerous in filaments in the center of protuberances.

The external cells of the distal portions of adja-

cent protuberances can fuse as the protuberances meet laterally. This fusion of cells produces an intracoelomic interchange in some present-day corallines (Afonso-Carrillo, 1985).

No epithallial cells have been recognized in the samples studied.

C o n c e p t a c l e s : Male and tetra/bisporangial con- ceptacles usually occur in separate plants. Spermatangial conceptacles are sunken, triangular in section, and small, 72-108/~m (mean 92.4, sd 9.9) in diameter and 24-30 pm (mean 26.4/~m, sd 3.1 ) in height (Plate II, 2). Tetra/bisporangial con- ceptacles are recognizable by the remains of a columella, a prominent rise of the conceptacle bot tom at its center (Edyvean and Moss, 1984; Edyvean and Ford, 1986). They are sunken, bean- shaped in section and uniporate. The pore canal is cylindrical to slightly bulbous with parallel to gently curved sides in section (Plate II, 3). Size ranges from 180 to 300#m (mean 250.7 #m, sd 23.1) in diameter and from 72 to 144 #m (mean 102.8 #m, sd 15.3) in height. Carposporangial con- ceptacles cannot be directly recognized by distinct features. In some plants there are large concepta- cles, similar in shape and size to the tetra/bisporan- gial ones, all of which lack remains of a columella. We assume that these represent carposporangial conceptacles, formed by the expansion of female conceptacles after fertilization, as is the case in

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present-day plants of the species (Edyvean and Moss, 1984). No unfertilized female conceptacles (as small as the male ones but elliptical in section; Edyvean and Moss, 1984) have been found in the samples studied.

Remarks: The type material ofL. viennotii Lemoine has not been located and seems to be lost (Ardrf , pers. commun., 1991). We have sampled the type localities of this species: Padul-E1 Ventorrillo de San Diego, south of Otura, south of La Zubia, road f rom Padul to Escflzar (Lemoine, 1929) in the Granada Basin (Fig. 3), to re-examine their coralline assemblages. In all sites, the lithophyl- loids matching the original description of L. vien- notii can be assigned to L. incrustans as interpreted in this paper. We therefore assume that L. viennotii may be considered a younger heterotypic synonym of L. incrustans.

Li thophyl lum microsporum Maslov (1962), established on male plants with small conceptacles triangular in section, probably corresponds to male plants of L. incrustans. Nevertheless, revision of Maslov 's original material, if conserved, is needed for a precise interpretation of this taxon.

Distribution: L. incrustans is the commonest litho- phylloid coralline algae in the Neogene of southern Spain. Our observations reveal its occurrence in the Lower Miocene rhodalgal sediments of the Prebetic Zone (Santiago de la Espada, Jaen); in the Tortonian temperate carbonates and reefs of the Granada Basin (Padul, Otura, Escflzar y Ventorrilo de San Diego), in the Tortonian coastal and reef deposits of the Almanzora Corridor

(already reported as L. viennotii and L. micro- sporum by Braga and Martin, 1988), Sorbas Basin (Cruce de Tahal) and Elche (Alicante), in the Upper Miocene temperate carbonates of the Sorbas Basin (Rio Aguas), and in the Pliocene of Cabo Roche, San Roque, Almefia, and Los Juanorros (Fig. 3). Segonzac (1990) referred to the presence of this species in the Quaternary deposits of Alicante (Fig. 3). This species has been recorded as L. viennotii and L. microsporum in the Middle and Upper Miocene (Favrega and Vannucci, 1987) as well as in the Pliocene (D'Atr i and Piazza, 1988) deposits of the Piedmont Basin (Italy). Orszag-Sperber and Poignant (1972) reported this species from the Miocene of Corsica as L. viennotii and L. microsporum. Adey and Adey (1973) recorded L. incrustans in the Nor th Atlantic with increasing relative abundance to the south with a southernmost record of the species at Cape Blanco. They reported, after Hammel and Lemoine (1953), the occurrence of L. incrustans in the western Mediterranean, where the type locality is located.

Lithophyl lum nitorum Adey et Adey, 1973:386

Holotype: Designated by Adey and Adey (1973, p. 387), collected at 3-9 m in Port Erin Harbour , Isle of Man. Deposited in the US National Museum (collection number 70-10B, 10-30).

Synonym: Li thophyl lum mgarrense Bosence, 1983: 164. 1982 Lithophyl lum sps. ' a ' Bosence and Pedley.

PLATE II

1. Dimerous construction of an L. incrustans thallus. Rectangular cells of primigenous filaments (arrows) running on the substrate (an older coralline plant). Sample TB.-S-14. Almeria (Almeria Basin). Pliocene. Scale bar = I00 ~m.

2. Male conceptacles of L. incrustans buried in thallus. JU-II-14. Los Juanorros (Almeria Basin). Pliocene. Scale bar= 100 Ixm. 3. L. incrustans tetra/bisporangial conceptacle buried in thallus, showing columella. Note cylindrical pore canal. Sample AG-FT-3.

Cabo Roche (C~tdiz). Upper Pliocene. Scale bar = 250 ~u'n. 4. Dimerous thallus of L. nitorum growing on the remains of an L. pustulatum plant. Note changes in height of cells of primigenous

filaments (arrows) at the ventral side of thallus. Sample AG-B-2A-15. Cabo Roche (C~idiz). Upper Pliocene. Scale bar = 100 ~n. 5. Primigenous (arrow) and postigenous filaments of an L. nitorum thallus. Marginal section of conceptacle on the left reveals

neither pore canal nor long cells of conceptacle roof visible in the one on the right. Sample AG-B-2A-15. Cabo Roche (C~tdiz). Upper Pliocene. Scale bar = 100 ~"n.

6. Tetra/bisporangial conceptacle of L. nitorum. Protruding conceptacle roof characteristically has basal cells three or four times longer than surrounding cells. Note conical pore canal. Sample ELX-A1-5. Elche (Alicante). Upper Miocene. Scale bar = 100 ~rn.

278 J.C. Braga, J. Aguirre/Review of Palaeobotany and Palynology 86 (1995) 265-285

1983 Lithophyllummgarrense n. sp., Bosence, p. 164, plate 16, figs. 5, 6 and text-fig. 9. Holotype designated by Bosence (1983, p. 164), specimen BM V. 60930 (British Museum), from the Miocene Crustose Algal Facies of Malta (Bosence and Pedley, 1982).

External appearance: Studied examples are isolated and broken plants intergrown with other coralline algae in rhodoliths. In thin section they occur as laminar thalli up to 850 #m thick.

Vegetative anatomy: Thallus dimerous. Primi- genous filaments of L. nitorum are formed by rectangular cells, which are usually 8-15 #m (mean l l . 3#m, sd 2.2) long and 10-24#m (mean 18.1 #m, sd 3.9) in height (Plate II, 4, 5). When the primigenous filaments adapt to substrate irreg- ularities, cell shape changes and cell height can reach up to 30 #m.

Postigenous filaments are conspicuous and well- developed. There is a clear lateral alignment of cells of adjacent filaments and the thallus has a net-like appearance (Plate II, 4, 5). Cells of posti- genous filaments are quadrangular in shape and measure 6-22 #m (mean 11.6 #m, sd 3.3) in length and 6-22 #m (mean 10.6 #m, sd 2.7) in diameter. When the substrate is irregular filaments become arched near the bottom (Plate II, 5).

Epithallial cells have not been recognized.

Conceptacles: Conceptacles are uniporate and slightly protruding on the thallus surface. The pore canal is conical, tapering to the conceptacle roof (Plate II, 6). Some have a raised floor which can be interpreted as the remnants of a columella (Plate II, 5, 6). They measure 216-396 #m (mean 293 #m, sd 66.7) in diameter and 84-168 #m (mean 122 #m, sd 28.5) in height. No distinct gamete- producing conceptacles have been found. The roof of the conceptacles is characteristically formed by one or two rows of cells longer than the surround- ing cells and measuring 28-43 #m (mean 34.9 #m, sd 5) in length (Plate II, 5, 6).

Remarks: The diagnosis, description and illustra- tion of L. nitorum made by Adey and Adey (1973) when establishing the species are short and not very illustrative. According to the identification keys offered by these authors, characters diagnostic

for L. nitorum when comparing this species with other North Atlantic species are: glossy, smooth surface, thin thalli, conceptacles raised on the surface, single-layered "hypothallium", weak "perithallial" cell-layering, epithallium one-cell thick, and meristem short. The preserved charac- ters in the fossil Neogene examples ascribed to L. nitorum from southern Spain agree with the diag- nosis and original description of the species. Other distinct characters here considered as typical for this species, such as the conical pore canal and one layer (or two) of longer cells in the conceptacle roof (Plate II, 5, 6), were not mentioned by Adey and Adey (1973) in their diagnosis of L. nitorum. These characters occur, however, in L. nitorum from the British Isles, including the type locality of the species (Chamberlain, pers. commun., 1993). They have also been observed by us in recent plants ascribable to this species from the southern coast of Spain (Adra, Almeria) and the Balears (Cabrera). L. mgarrense was established by Bosence (1983) on fossil plants from the Miocene of Malta. According to the description and illustrations of the type material (Bosence, 1983, p. 164, plate 17, figs. 5-6, holotype), the vegetative anatomy and conceptacle size and shape of this species are similar to those of L. nitorum. The conceptacle roof is raised on the thallus surface and has a distinct layer of long cells. Our own examination of examples from the type locality confirms these observations. We therefore consider L. mgarrense a younger heterotypic synonym of L. nitorum.

The types of L. exiguum Conti (1946, p. 62) show the same characteristic structure in concepta- cle roofs, but cells of postigenous filaments are not well-aligned laterally and their conceptacles are significantly smaller than those of L. nitorum. The conserved type material of L. exiguum is very poor. Only a thin section of a fragmentary thallus, the example figured by Conti (1946), is preserved in the collections of the Dipartimento di Scienze della Terra in Genova, Italy. Studies on plants referable to this species from the type localities (Leithakalk, sample points 1, 7 and 10 (?), Miocene, Vienna Basin) are needed to assess its relationship to L. nitorum.

L. nitorum is similar to L. incrustans but has

C. Braga, .L Aguirre/Review of Palaeobotany and Palynology 86 (1995) 265-285 279

better-defined lateral cell alignment. In addition, L. nitorum has a raised conceptacle roof with one or two layers of long cells clearly distinct from the surrounding cells, and a conical pore canal (Tables 2 and 3).

Distribution: L. nitorum is a minor component of coralline associations in the Langhian (Middle Miocene) reefs of the Granada Basin (Murchas reef), in the Tortonian coastal deposits of the Almanzora Corridor (Bayarque, Almeria), in the Tortonian reefs of Elche (Alicante), and in the Pliocene sediments of Cabo Roche (C~idiz) (Fig. 3). As L. mgarrense in the Late Miocene of Malta (Bosence, 1983). According to Adey and Adey (1973), L. nitorum occurs both on the American and European coast of the North Atlantic. We have found the species on the south- ern coast of Spain (Adra, Almeria) and in the Balears (Cabrera).

Lithophyllum orbiculatum (Foslie) Foslie, 1900:19

Basionym: Lithothamnion orbiculatum Foslie, 1895: 171.

See Chamberlain et al. (1991) for a detailed account of references, misidentifications, illustr- ations, and synonyms of this species in botanical literature. These authors illustrated the holotype specimen (from Kristiansund, Norway) deposited in the Kongelige Norske Videnskabers Selskab Museet, Trondheim (Norway), coll. Ekman, ex Herbarium Areschough (Chamberlain et al., 1991, figs. 1 and 2).

External appearance: The studied fossil examples of L. orbiculatum occur as small (up to 6.5 mm), thin (up to 750 #m) laminar plants overgrown by other coralline algae, serpulids and/or encrusting bryozoans (Plate III, 1), thereby making it impos- sible to observe the external appearance of the plants. In most cases thallus margins are broken by boring or abrasion.

Vegetative anatomy: Thallus dimerous. Cells of primigenous filaments are squarish, 6-11 #m (mean 8 #m, sd 1.3) in length and 6-14 pm (mean 8.9 pm, sd 2.3) in height (Plate III, 2).

Postigenous filaments are distinct, sometimes slightly arched at the base (Plate III, 1). Cells of contiguous filaments are not horizontally aligned (Plate III, 2, 3). Cells are quadrangular, measuring 6-12#m (mean 8.4#m, sd 1.3) in length and 6-11 #m (mean 7.9 #m, sd 1.1) in diameter.

Epithallial cells have not been preserved.

Conceptacles: Conceptacles are always uniporate and buried in the thallus. The pore canal is conical, tapering to the conceptacle roof (Plate III, 3). Two different types of chambers can be observed. Some conceptacles have a convex-upward bottom (Plate III, 3) and can be interpreted as tetra/ bisporangial conceptacles, similar in morphology to modern specimens having a columella (Chamberlain et al., 1991). Other conceptacles have a flat bottom and an elliptical vertical section. These may be attributed to carposporangial conceptacles similar in shape in present-day plants (Chamberlain et al., 1991). Both types have approximately the same size, measuring 156-204/an (mean 193.4 #m, sd 15.9) in diameter and 84-108 #m (mean 90.5 pm, sd 8.6) in height. No distinct gamete-producing plants have been found.

Remarks: L. orbiculatum can be distinguished from L. incrustans by its smaller cells and conceptacles, with a conical pore canal; a smaller, and thinner thallus; and the lack of pronounced columella remains in tetra/bisporangial conceptacles (Tables 2 and 3).

Distribution: Only a few examples of L. orbicula- turn have been found by us in the Upper Pliocene deposits on the Atlantic coast of C~tdiz (Cabo Roche) (Fig. 3). These are shallow-water, temper- ate-platform sediments rich in coralline algae (Aguirre et al., 1993). L. orbiculatum intergrows with serpulids and/or encrusting bryozoans to make up the inner part of some rhodoliths. According to Chamberlain et al. (1991) confirmed present-day records of the species are from localities distributed along the Atlantic coast of Europe and some Mediterranean localities. No other references to this species in fossil material are known.

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PLATE III

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Lithophyllumpustulatum (Lamouroux) Foslie, 1904:8

Basionym: Melobesia pustulata Lamouroux, 1816: 315.

Lectotype collection designated by Woelkerling et al. (1985, p. 325) from a few plants of Lamouroux's original herbarium housed at the University of Caen (France). Woelkerling et al. (1985) illustrated (figs. 34-39) and described this lectotype material. Woelkerling and Campbell (1992, fig. 50) offered SEM photographs of the lectotype as well.

Synonyms: Chamberlain (1991) and Woelkerling and Campbell (1992) gave a detailed account of synonyms of this species based on modern coralline algae.

External appearance: This species occurs as thin (up to 300/~m) laminar thalli (Plate III, 4, 5) constituted by up to five or six layers of cells. Most of the thalli, however, are very thin, having only one or two cell layers. Plants of L. pustulatum adapt to the substrate or become divided, forming contorted bridges (Plate III, 5) that may again overlap underlying plants or branches. The result is a foliaceous, irregular structure of superimposed applanate branches of the same plant or (it is difficult or impossible to distinguish) several super- imposed plants (Plate III, 4).

Vegetative anatomy: Thallus dimerous. Primi- genous filaments are composed of palisade cells, usually oblique and slightly sinuous, which are

6-14 #m (mean 9.7/~m, sd 1.7) long. The height of these cells is very variable, from 8 to 77/~m (mean 36.6~m, sd 15.4), as a consequence of adaptation to substrate irregularities (Plate III, 4).

Cells of postigenous filaments are squarish to rectangular in shape, measuring 6-14/~m (mean 9.7 #m, sd 1.7) in diameter. Their length frequently changes due to substrate irregularities, as does cell height of primigenous filaments (from 14 to 42/~m, mean 27.3/~m, sd 6.4). Postigenous filaments con- sist of up to six cells with well-defined both vertical and horizontal cell alignments. In case of crust division, the postigenous filaments give way to a lateral expansion of the thallus with formation of new primigenous filaments at its base.

A single layer of small, and flat epithallial cells can be recognized in some samples. This cells are 3-5/tm in height and 7 12/~m in diameter.

Conceptacles: Conceptacles are prominent on the crust surface and hemispherical in shape, measur- ing 192 408/~m (mean 307/~m, sd 56.9) in diame- ter and 78-150#m (mean l17/~m, sd 19.2) in height. Conceptacle floors are situated 1 to 3 cell layers deep in the surrounding vegetative portion of the thallus (Plate III, 6). No columella remains have been found in any samples. A few plants show flat, lenticular conceptacle chambers, 114-252 #m (mean 173/~m, sd 50) in diameter and 30-54 #m (mean 44 #m, sd 7.8) in height, prob- ably representing originally male conceptacles (Plate III, 4).

Remarks: Chamberlain (1991) distinguished four varieties of this species (as Titanoderma pustula-

PLATE III

1. Thin, small thallus of L. orbiculatum (central third) overgrown by other coralline algae. Sample AG-I-N. A2-3. Cabo Roche (C~tdiz). Upper Pliocene. Scale bar = 250 Ixm.

2. Dimerous thallus of L. orbiculatum. Primigenous filaments composed of squarish cells (arrows). Sample AG-I-N. A2-3. Cabo Roche (C~diz). Upper Pliocene. Scale bar = 100 ~trn.

3. Close-up of 1 showing structure of thallus and a tetra/bisporangial conceptacle. Conceptacle has a slightly raised floor, representing columella remains. Note conical pore canal. Scale bar= 100 ~rn.

4. Detail of thallus and a gamete-producing (male?) conceptacle of L. pustulatum (arrow). Primigenous filaments consist of palisade cells (arrow head). Sample AG-CB-5. Cabo Roche (C~idiz). Upper Pliocene. Scale bar= 100 Ixrn.

5. Branching plant of L. pustulatum. Thallus becomes divided (arrow) producing an applanate, contorted branch. Sample AG-TPN-1. Cabo Roche (C~idiz). Upper Pliocene. Scale bar= 100 ~tm.

6. Protruding tetra/bisporangial conceptacle of L. pustulaturn. Sample AG-CB-2. Cabo Roche (C~idiz). Upper Pliocene. Scale bar = 100 pm.

282 J.C. Braga, J. Aguirre/Revie~ of Palaeobotany and Palynology 86 (1995) 265-285

tum) in the British Isles. Thickness (number of cells), size, and morphology of conceptacle roof are the diagnostic characters delimiting these vari- eties. Although some of these features are recogniz- able in the fossil examples from the Neogene of southern Spain it seems unnecessary to determine varieties at this point of taxonomic research on fossil corallines.

L. pustulatum is delimited from other species of Lithophyllum by several characters: (1) the predo- minance of palisade cells in primigenous filaments; (2) raised conceptacles (Chamberlain, 1991); (3) conceptacle floors only 1 to 3 cell layers deep in the surrounding vegetative thallus (Woelkerling and Campbell, 1992); and (4) the common occur- rence of more than one cell in the postigenous filaments (i.e. these postigenous filaments are not restricted to an epithallial cell; Woelkerling and Campbell, 1992) (Table 3).

Distribution: L. pustulatum has been recorded by us in the Messinian reefs of Nijar and Cariatiz (Almeria), encrusting coral skeletons, and other bioclasts. It has also been found in the Pliocene temperate carbonates of Cabo Roche, San Roque, Los Juanorros, and Almeria (Fig. 3), encrusting hard substrata or making up nodules together with serpulids and other corallines (Aguirre et al., 1993). L. pustulatum has a wide geographical distribution in modern seas. Confirmed records of this species extend from the North Atlantic and the Mediterranean (Chamberlain, 1991) to south- ern Australia (Woelkerling and Campbell, 1992), California, and India (Chamberlain, 1991).

6. Concluding remarks

Despite the great number of characters included in the description of present-day coralline species, diagnostic criteria at the species level are restricted to only a few characters, especially those related to the anatomy and size of sporangial conceptacles and the arrangement of cells in vegetative portions (Table 1). Intraspecific variability in these algae is consequently high and produced by variation both in reproductive and vegetative anatomy. Most of the diagnostic characters of present-day corallines

are recognizable in fossil coralline algae and, there- fore, palaeontological studies on corallines should follow the same taxonomic procedures of present- day phycologists.

Coralline algae belonging to the subfamily Lithophylloideae have uniporate tetra/bisporan- gial conceptacles and interfilamental cell connec- tions made by secondary pits without cell fusions. These anatomical characters can be recognized in fossil corallines, excluding from the subfamily many taxa previously ascribed to Lithophyllum without taking into account the type of interfila- mental cell connections (Braga et al., 1993).

Application of current taxonomic criteria at both the supraspecific and specific level reduces the number of representatives of the subfamily Lithophylloideae from the Neogene of southern Spain to five species included in Lithophyllum (Table 3).

All five species can be assigned to extant taxa treated in the recent botanical literature. L. incrus- tans, the commonest species, is already present in the Lower Miocene deposits. The oldest record of L. nitorum is from the Middle Miocene. L. denta- tum and L. pustulatum are found from the Late Miocene onwards and the examples of L. orbicula- tum come from temperate Pliocene carbonates (Fig. 5). These long stratigraphic ranges reduce the biostratigraphic use of these algae, but increase their potential in palaeoenvironmental reconstructions.

uJ z L A T E 0 o_

E A R L Y

Mess in ian

7 ~ la te

w Tor t0n ian - 0 0 ear ly L. incrustans

I M I D D L E

E A R L Y I

L. orbiculatum

I

L. pustulatum

L. dentaturn

L. nitorum

Fig. 5. Stratigraphic ranges of lithophylloid species in the Neogene of southern Spain.

J. C. Braga, J. Aguirre/Review of Palaeobotany and Palynology 86 (1995) 265-285 283

The precise p re sen t -day geograph ic d i s t r ibu t ion o f these species is no t known. As Woelke r l ing (1983) and Woelke r l ing and Campbe l l (1992) po in t ed out for the cases o f L. incrustans and L. pustulatum, m a n y repor t s o f these species require verif icat ion. The Lithophyllum species found in the Neogene o f sou thern Spain have conf i rmed records in the E u r o p e a n coas ts o f the N o r t h At l an t i c and the western Med i t e r r anean . L. incrustans has its sou the rnmos t occur rence in Cape Blanco. L. pustu- latum has a wider d i s t r ibu t ion with conf i rmed records in sou thern Aus t ra l i a , Cal i forn ia , and Ind ia as well. Fossi l records o f these species are res t r ic ted to the M e d i t e r r a n e a n Neogene .

The Neogene l i thophyl lo ids f rom southern Spain h ighl ight the need to t ake into account present- day cora l l ine species and their t a x o n o m y in pa l aeon to log ica l s tudies o f cora l l ine algae. These o rgan isms have long t e m p o r a l ranges, which m a k e it h ighly p r o b a b l e tha t species found in Cenozoic depos i t s are still l iving in m o d e r n oceans.

Acknowledgements

We are mos t grateful to Dr. Y. C h a m b e r l a i n who read a first manusc r ip t o f this w o r k and m a d e m a n y helpful suggest ions. Dr . D .W.J . Bosence and Dr. Wm.J . Woelker l ing revised the w o r k and i m p r o v e d it wi th their comments . Dr . D .W.J . Bosence also k ind ly a l lowed one o f us ( JCB) to examine his pe r sona l col lec t ion o f L. mgarrense and Dr . G. Vannucci a l lowed us to examine the col lect ions o f the D i p a r t i m e n t o di Scienze della Terra in Genova . Dr . F. Ardr6 , M u s 6 u m N a t i o n a l d 'H i s to i r e Nature l le , Paris , p ro - v ided i n fo rma t ion on the s ta tus o f the type collec- t ion o f L. viennotii. Dr. J. Fo rn6s p rov ided the cora l l ine samples f rom C a b r e r a (Balears) . Dr . R. G a g o and R. M a r t i n G a r c i a he lped us in sampl ing coral l ines off A d r a (Almer ia ) . We thank Chr is t ine Lau r in for cor rec t ing the Engl ish text. Dr . J .M. M a r t i n assisted in sampl ing mos t o f the local i t ies s tudied. This w o r k was s u p p o r t e d by the D G I C Y T (Pro jec t PB90-0854) and the Jun ta de A n d a l u c i a ( G r u p o 4076).

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