Bioerosion versus colonisation on Bivalvia: A case study from the Upper Miocene of Cacela (southeast Portugal)

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Geobios 41 (2008) 43–59 http://france.elsevier.com/direct/GEOBIO

Original article

Bioerosion versus colonisation on Bivalvia: A case study from the Upper Miocene of Cacela (southeast Portugal) Bioe´rosion versus colonisation chez les bivalves du Mioce`ne supe´rieur de Cacela (sud-est du Portugal) Ana Santos *, Eduardo Mayoral Department de Geodinámica y Paleontología, Facultad de Ciencias Experimentales, Campus de El Carmen, Universidad de Huelva, Avda. de las Fuerzas Armadas s/n., 21071 Huelva, Spain Received 31 October 2005; accepted 16 January 2007 Available online 18 January 2008

Abstract A study of the bioerosion structures and the skeletobionts associated with the most common bivalves (infauna and epifauna) from the classic Upper Tortonian site of Cacela, Algarve region, SE Portugal, revealed 24 different ichnotaxa and five systematic groups of encrusters (Foraminifera, Annelida, Bryozoa, Balanomorpha and Bivalvia). Despite a relatively high ichnodiversity, the percentage of bioerosion in the specimens analysed is quite low (10–12%). This is explained by rapid sedimentation with only short periods of exposure on the sea-floor. The dominant bioerosion structures were linked to the boring activity of nonpredatory organisms. Algal microborings are the most common, followed by annelid borings (Caulostrepsis-Maeandropolydora), sponge borings (Entobia) and ctenostome bryozoans (Pinaceocladichnus). Spatial distribution of bioerosion structures and encrusters allow the reconstruction of three successive stages. The first was restricted to the biosubstrate lifetime, with structures showing a preferred orientation and situated exclusively on the outside of the shells. The second comprises the period immediately after death, with structures that extend outwards and start with the colonization of the interior of the valves, losing their initial orientation. The third stage relates to later postmortem colonisation, with structures on both sides of the valves and without a preferential orientation. # 2008 Published by Elsevier Masson SAS. Résumé On a étudié les structures de bioérosion et de skeletobiontes associées avec les bivalves les plus représentatifs (infaune et épifaune) du gisement classique de Cacela (Tortonien supérieur), dans la région de l’Algarve, sud-est du Portugal. Vingt-quatre ichnotaxons différents et cinq groupes systématiques parmi les skeletobiontes (Foraminifera, Annelida, Bryozoa, Balanomorpha et Bivalvia) ont été identifiés. Le pourcentage de bioérosion dans les exemplaires analysés est assez bas (10–12 %), malgré l’ichnodiversité assez considérable. Cette caractéristique implique une dynamique sédimentaire très active, gouvernée par des périodes courtes d’exposition des coquilles sur le fond marin, suivis par de fréquents épisodes d’enfouissement soudain. Les structures bioérosives dominantes sont dues à l’activité d’organismes non prédateurs. Les microperforations des algues sont les plus fréquentes, suivies par celles des annélides (Caulostrepsis, Maeandropolydora), des éponges clionaides (Entobia) et des bryozoaires ctenostomates (Pinaceocladichnus). L’étude de leur emplacement, leur orientation et/ou leur distribution spatiale permettent d’établir la relation existant entre les biosubstrats (les bivalves) et les producteurs des structures. On a pu révéler une succession temporelle avec trois étapes. La première se déroule sur les biosubstrats encore vivants, avec les structures orientées et situées exclusivement sur la face extérieure des valves. La deuxième correspond à la période immédiatement postmortem, avec des structures plus répandues à la surface, qui commencent à coloniser l’intérieur des valves et en perdant leur

* Corresponding author. E-mail address: [email protected] (A. Santos). 0016-6995/$ – see front matter # 2008 Published by Elsevier Masson SAS. doi:10.1016/j.geobios.2007.01.009

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orientation initiale. La troisième étape est clairement postmortem, avec les structures présentes partout sur les deux surfaces des valves et sans aucune orientation préférentielle. # 2008 Published by Elsevier Masson SAS. Keywords: Bioerosion; Incrustation; Ecological succession; Bivalves; Upper Miocene; Portugal Mots clés : Bioérosion ; Encrustation ; Succession écologique ; Bivalves ; Miocène supérieur ; Portugal

1. Introduction Hard substrates, including skeletons of living and dead organisms as well as rock clasts, may be colonised by a diverse array of borers and grazers. This biological process, defined as bioerosion (Neumann, 1966; Bromley, 1970; Taylor and Wilson, 2003), is recognised as a complex of biogeochemical interactions capable of significantly modifying carbonate skeletal material and carbonate rocky surfaces. In intertidal and shallow sublittoral environments, the diversity of microand macroborers present on hard substrates is usually quite high, occurring in addition to encrusters. The borers are the primary agent of shell destruction (Cutler and Flessa, 1995) involving mechanical and/or chemical processes. Bioeroders attack living and dead shell material alike, although some are highly selective. In a general way, their importance increases with productivity and decreases with higher rates of sedimentation (Lescinsky et al., 2002). In recent decades, the effects of bioerosion on particular organisms have been the subject of several neontological and palaeontological studies (see Taylor and Wilson, 2003; Wilson, 2006). However, the bioerosion processes themselves, as well as the role of bioerosion in ecology and sedimentology, have sometimes remained unclear. The present contribution aims to document and study shell bioerosion from a palaeoecological perspective, analyzing a classic outcrop of the Cacela Formation (Upper Miocene, SE Portugal) (Fig. 1). Bioerosion rates and the patterns of spatial

Fig. 1. Geological setting of the section studied (Santos, 2005). Fig. 1. Situation géologique de la section étudiée (Santos, 2005).

distribution of borers and encrusters on mollusc shells of a shallow sandy-silt facies have been analysed. In order to assess the sequence of boring and encrusting both left and right valves were analysed, as well as different features of the shells, such as interior/exterior surfaces and different sectors of the valves. An attempt was made to distinguish between the skeletobiont colonisation of living and dead bivalve shells. This allowed reconstructing events during the lifetime of the host, as well as after its death. 2. Geological setting The outcrop studied, called Ribeira de Cacela, is located near Cacela Velha, a village not far from the Spanish border and situated in the Algarve region of SE Portugal. This Neogene marine deposit has been the subject of several geological and palaeontological investigations with publications dating back to the mid-1800s (Pereira da Costa, 1866; Cotter, 1879; Dollfus et al., 1903–1904; Boucart and Zbyszewski, 1940; Chavan, 1940; Ribeiro et al., 1979; Civis et al., 2000; Santos, 2000, 2005). The strata belong to the Cacela Formation of Ribeiro et al. (1979). The lower levels of this formation are best exposed along the margins of a river bank. According to Silva (1984), these strata, ca. 5–6 m thick, overlie the Triassic (‘‘Gress de Silves’’), Hettangian (vulcanosedimentary complex) or later Jurassic units with angular unconformity. The Ribeira de Cacela site shows only two of the three members that characterise the Cacela Fm in the region (sensu Cachão et al., 1998) (Fig. 2). The lower one consists of 5–6 m of fossiliferous conglomerates and silts, whilst the higher member, 5–13 m thick, contains orange to yellow silts with grey pelitic intercalations of 50 cm thickness. The outcrop studied lies within the lower member of the Cacela Fm (Fig. 2). The sediments that crop out along the Ribeira de Cacela contain an especially rich and diversified fauna, with particularly well-preserved molluscs (Cotter in Dollfus et al., 1903–1904; Santos, 2000), in combination with ichnofossils (bioturbation and bioerosion structures) (Cachão et al., 2000; Santos et al., 2003, 2005; Santos, 2005). In contrast, the overlying sediments are poorly fossiliferous, as a result of leaching which affected preservation. As a result, more moulds are seen than body fossils. Calcareous nannoplankton (Cachão, 1995) from the lower member of the formation, dates the sediments between 8.2 (FADs of Discoaster berggrenni and D. quinqueramus) and 7.5 million years (LAD of Minylita convalis), which corresponds to the Late Tortonian (Late Miocene). These dates are consistent with results obtained from planktonic Foraminifera (Legoinha, 2001), 87Sr/86Sr isotope studies (Studencka et al.,

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Fig. 2. Stratigraphy of the Ribeira de Cacela section. Fig. 2. Stratigraphie de la coupe de Ribeira de Cacela.

2003), and the malacofauna (Cotter in Dollfus et al., 1903– 1904; Santos, 2000).

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same kind of information and, therefore, facilitate its interpretation. Recording isodensity zones, three different degrees of occupation are represented by different shadings and, in cases where the bioerosion structures showed apparent polarity, their orientation was taken into consideration. With the aim of maintaining uniformity, the terminology proposed by Taylor and Wilson (2002, 2003) for organisms colonising hard substrates was adopted. Following Taylor and Wilson (2003), bioerosion structures produced during the host lifetime and postmortem structures were differentiated. Criteria used were such as skeletal intergrowth and interlayering, distortion or other reaction of host skeleton, size distribution of skeletobionts along host substrate, preferred orientation or distribution of skeletobionts relative to host morphology, and skeletobionts colonising internal and/or soft tissue surfaces. The taphonomic criteria proposed by Puig et al. (1984) for the interpretation of malacological fossil assemblages have been chosen for the specimen quantification. So, two complete and articulated valves have been regarded as equivalent to one specimen; whereas one complete valve is counted as equivalent to half a specimen, and a hinge fragment about the equivalent to one quarter specimen. 4. Results 4.1. Shell bioerosion rates

3. Material and methods The Cacela site possesses particularly rich and diversified fossil content, mainly molluscs (Santos, 2000) and ichnofossils (bioturbation and bioerosion structures) (Cachão et al., 2000; Santos et al., 2003, 2005), which are generally very wellpreserved in taphonomic terms (Santos, 2005). Fossils were collected from Levels C3, C6 and C7 (Fig. 2), but only Level C3 supplied a significant number of bivalves allowing the quantitative study. All shells were collected and identified but only the most representative species of bioeroded infauna (3.8% regarding the total species of C3, and represented by Megacardita jouanneti (Basterot), Glycymeris bimaculata Poli, and Circomphalus foliaceolamellosus (Dillwyn)) and epifauna (2.5% regarding the total species of C3, as represented by Ostrea edulis Linnaeus, and Gigantopenten tournali (De Serres)) were used for this study. However, all the associated fauna remains were recorded. After identification, contour plots were drawn for each bivalve taxon. These plots were divided into nine areas of equal dimensions, by combinating the anterior–medial–posterior sectors with the dorsal–central–ventral sectors of each valve. This allowed all bioerosion structures to be located exactly after identification. The interior and exterior surfaces of each valve (right or left) were examined so as to record the presence or absence of borers or encrusters. The numbers and percentages of bioeroded valves were calculated. Bioerosion structures were then ordered in terms of importance. Conspecific structures on homogeneous biosubstrate were subsequently grouped on a single plot in order to compile the

The material from Cacela presents a great variety of direct and indirect evidences of boring, encrusting and scraping organisms that use others as hard substrate, whether the surface is internal or external. These different biotic relationships constitute a record of some complexity. Morphological analysis of different bioerosion structures preserved has permitted the recognition of no less than 24 different traces. These include structures attributed to algae (Cavernula pediculata Radtke, 1991; Ichnoreticulina elegans Radtke and Golubic, 2005; ‘‘Semidendrina-form’’ Glaub, 1994), fungi (Saccomorpha terminalis Radtke, 1991), polychaete annelids (Caulostrepsis taeniola Clarke, 1908; C. contorta Bromley and D’Alessandro, 1983; Maeandropolydora sulcans Voigt, 1965; M. decipiens Voigt, 1965), clionaid sponges (Entobia isp.), ctenostome bryozoans (Pinaceocladichnus onubensis Mayoral, 1988b; Pennatichnus moguerenica Mayoral, 1988b; P. luceni Mayoral, 1988b), cheilostome bryozoans (Leptichnus peristroma Taylor et al., 1999; L. dromeus Taylor et al., 1999), echinoids (Gnathichnus pentax Bromley, 1975), endolithic bivalves (Gastrochaenolites dijugus Kelly and Bromley, 1984), sipunculid or terebellid worms (Umbichnus inopinatus Martinell et al., 1999), predatory gastropods (Oichnus simplex Bromley, 1981; O. paraboloides Bromley, 1981), gastropods or chitons (Radulichnus inopinatus Voigt, 1977), anomiid bivalves (Centrichnus eccentricus Bromley and Martinell, 1991), encrusting gastropods (Lacrimichnus cacelensis Santos et al., 2003) and acorn barnacles (Anellusichnus undulatus Santos et al., 2005; A. circularis Santos et al., 2005).

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No detailed taxonomic descriptions of trace forms are presented here since the authors’ description are regarded as adequate for their recognition. However, in the case of the problematic trace ‘‘Semidendrina-form’’, which exhibits an anastomosed branching pattern, it is noted that this is considered here as a microboring alga instead of a foraminiferal boring (Glaub, 1994) (produced by Globodendrina monile Plewes et al., 1993); there is no evidence of a small agglutinated chimney around the entrance of the boring neither is there a foraminiferal test in their chamber as Cherchi and Schroeder (1991) observed. It is also noted that these traces appear commonly associated with algal borings. Despite the great ichnodiversity displayed, the total percentage of bioerosion in the samples examined is quite low, giving an average value of merely 11%, varying between 10 and 12% in the different levels analysed (Fig. 3). Even though the bioerosion percentage is roughly the same in the three levels studied, the number of bioeroded bivalve shells is significantly different. After statistical sampling, only the sample from Level 3 shows a

Fig. 3. Histograms of total bioerosion rates from the Ribeira de Cacela section. Fig. 3. Histogrammes de la bioérosion totale de la coupe de Ribeira de Cacela.

significant number of bivalves (N: 1613). In contrast, the other two levels produced very low numbers of bivalves (N: 4.25 for the Level 6 sample and N: 25.25 for that of Level 7). This may be related to the dissolution of exposed shells, which is an important process capable of destroying aragonitic shells prior to fossilisation. This explains why Level 3 was the only one to yield an acceptable number of bivalves for analysis (compare Kidwell et al., 2001). For this reason, an in-depth study of this level was decided on. Regarding non-predatory organisms (Table 1 and Fig. 4A), structures related with microbial euendoliths (Cavernula, Ichnoreticulina and Semidendrina-form, 20.69%), polychaete annelids (Caulostrepsis-Maeandropolydora, 12.48%), clionaid sponges (Entobia, 9.43%) and ctenostome bryozoans (Pinaceocladichnus, 7.35%) are dominant. The remaining bioerosion evidence (Saccomorpha, Pennatichnus, Gastrochaenolites, Umbichnus, Leptichnus, Centrichnus, Lacrimichnus and Anellusichnus) gives values of less than 4% (Table 1 and Fig. 4A).

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Table 1 Bioerosion data of infaunal (n = 682) and epifaunal (n = 134) bivalves from the Ribeira de Cacela outcrop Tableau 1 Données de bioérosion pour les bivalves de l’infaune (n = 682) et l’épifaune (n = 134) de la coupe de Ribeira de Cacela

# Biovalves: number of bioeroded valves; % Biovalves: percentage of bioeroded valves. # Biovalves : nombre de valves bioérodées ; % Biovalves : pourcentage de valves bioérodées.

With regard to scraping activity (Table 1 and Fig. 4A), percentages are low, with only Gnathichnus (7.35%) being of any note, whereas Radulichnus give values inferior to 1%. The predatory boring Oichnus represent a total of 28.98%. The percentage of skeletozoans (annelids, bryozoans, foraminifers, barnacles, ostreid and anomiid bivalves) that conserve their shell and appear directly fixed onto the biosubstrates is also very low (only 58 valves, Table 1), representing a total of 6.6% altogether. Among the total encrusters, barnacles and briozoans are dominant (25 and 21%, respectively) (Fig. 4D). When bivalves are separated into infaunal and epifaunal categories, the proportions of dominant bioerosion structures are maintained without great alterations. There do appear, nonetheless, certain ‘‘exclusive’’ ichnotaxa specific to each category. For both groups there is a dominance of euendolith

microborings, with values ranging from 16.41% for the infauna to 42.40% for the epifauna (Fig. 4). In descending order of importance for the infauna are Maeandropolydora and Entobia, both around 9%, followed by Gnathichnus (7.77%) and Pinaceocladichnus (7.47%). The remaining structures give values inferior to 4%. With regard to the epifauna, in decreasing order of importance are Maeandropolydora and Entobia, both around 11%, and Caulostrepsis (7.45%). Pinaceocladichnus accounts for 6.71% and Gnathichnus, 5.22%. The remaining structures also give values below 4%. The presence of structures related to the activity of predators (Oichnus) is greater for the infauna (33.95%) than for the epifauna (3.73%). With regard to the sclerozoans (serpulids, spirorbids, bryozoans, foraminiferans, barnacles, Anomiidae and Ostreidae), as expected, their encrusting value is greater for epifauna (18 valves, representing

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Fig. 4. Pie diagrams concerning the bioerosion and encrusters found at Level C3 of the Ribeira de Cacela section. A. Total bioerosion. The ichnotaxa at lower than 0.4% (Saccomorpha, Centrichnus and Lacrimichnus) are not represented. B. Total bioerosion of infaunal bivalves. The ichnotaxa at lower than 0.3% (Saccomorpha, Centrichnus) are not represented. C. Total bioerosion for epifaunal bivalves. D. Total encrusters. E. Total encrusters for infaunal bivalves. F. Total encrusters for epifaunal bivalves. Fig. 4. Graphiques circulaires relatives à la bioérosion et les encroûtantes correspondant au niveau C3 de la coupe de Ribeira de Cacela. A. Bioérosion totale. Les ichnotaxons à moins que 0,4 % (Saccomorpha, Centrichnus et Lacrimichnus) ne sont pas représentés. B. Bioérosion totale pour les bivalves infaunales. Les ichnotaxons à moins que 0,3 % (Saccomorpha, Centrichnus) ne sont pas représentés. C. Bioérosion totale pour les bivalves épifaunales. D. Encroûtantes totales. E. Encroûtantes totales pour les bivalves infaunales. F. Encroûtantes totales pour les bivalves épifaunales.

11.8%) than for infauna (40 valves, representing 5.54%). In this way, encrusters on infaunal bivalves are mainly representing by barnacles (29%) and foraminifera (25%) (Fig. 4E), while on epifauna bivalves are Ostreidae (34%) and briozoans (22%) (Fig. 4F). Occasionally, certain epifaunal bivalves exhibit particular structures. Gigantopecten. tournali bears Lacrimichnus (2.23%), which seems exclusive to this group and which results from the attachment of Crepidula gastropods (Santos et al., 2003). Similarly, Umbichnus (3.95%) appear only on some shallow infaunal bivalves (M. jouanneti and C.

foliaceolamellosus) and hard-shelled venerids. The spatial distribution patterns of boring and encrusting structures show a very similar pattern for both infaunal and epifaunal bivalves. 4.1.1. Microbial euendoliths (algae) Their borings in infaunal bivalves appear on both outside and inside of the valves. The greatest concentration of microborings is observed within to the middle dorsal (umbonal) and posterior zones of the outside surface of the valves (Fig. 5A1–C6). The concentration of borings on the inside

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lateral parts of the edge where the adductor muscles are located is generally low. With regard to epifaunal bivalves these microborings appear on the interior as well as the exterior sides of both the right and left valves of ostreids. They show a tendency either to follow a pattern of bands close to the lateral and ventral edges, or to occupy all area available (Fig. 6A1–2, B1–2, C1–2). It is noted that the interior surfaces along the lateral and ventral edges always show a higher occupation density than the central areas of the shell. 4.1.2. Fungi Saccomorpha terminalis is a very rare boring and it does not show any topological preference; neither does it show a welldefined surface distribution pattern, appearing on both the inside and the outside of the valves of infaunal bivalves. 4.1.3. Bryozoans Similar to the fungi borings, Pinaceocladichnus onubensis, Pennatichnus moguerenica, P. luceni, Leptichnus peristroma and L. dromeus (Figs. 5D1–8 and 6E1–2, F1–4) are located on both the inside and outside parts of the valves of infaunal bivalves, covering the total available surface area, and not presenting either a pattern, spatial distribution preference, or any preferential orientation. The same is observed on epifaunal bivalves (Fig. 6 D1–2, E1–2). 4.1.4. Sponges Entobia ichnogenus is frequent on the valves studied. It occurs as commonly on the inside as on the outside of the right and left valves (Figs. 5G1–10 and 7(5, 6)). The greatest density of borings is found on the medial and ventral zones of the posterior parts of shells. On the shell interior no preferential area was observed, the borings being equally distributed. On epifaunal bivalves, Entobia shows a distribution pattern similar to that on the infauna with regard to the external surface (Fig. 6F1–2). However, on the interior no preferential distribution is observed. 4.1.5. Annelids Caulostrepsis and Maeandropolydora are preferentially located on the external surface of the posterior part. Oriented apertures are found towards the edges on infaunal bivalves. The presence of these structures on the inside surfaces of the valves shows a certain preference for borings in the areas close to the lateral and ventral edges of the valves (Figs. 5H1–3, I1–3, J1–J9 and 7(5)). Caulostrepsis and Maeandropolydora on specimens of Ostrea also display a preferential orientation of their apertures towards the edges on the external surface of the right valves. When these borings are found on the interior surfaces, they are also seen to be oriented towards the shell edges (Fig. 7(13, 14)) as well as being arranged in narrow bands close to the lateral and ventral edges. These ichnospecies also occur on the outside at the ventral edges of the lower valves (left), showing a preferential orientation towards the edges, especially in the ventral and lateral zones (Fig. 7(12)).

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Equally noteworthy is the presence of Caulostrepsis on the left valves of G. tournali and Pecten benedictus (Lamarck) with a development parallel to the ventral edge of the valve in the rib intervals (Fig. 7(9)), i.e., following the growth lines of the bivalve. 4.1.6. Boring bivalves Gastrochaenolites appears in both left and right valves, on both the external and internal surfaces of infaunal bivalves (Figs. 5K1–6 and 7(3, 5)). However, in M. jouanneti, they are more frequent on the outer part of the shells, particularly in the posterior–medial and ventral zones (Figs. 5K1–3 and 7(3)), with the apertures oriented towards the posterior area. In any case, regardless of whether they occur on the outer or inner surface, the majority of these borings maintain their siphonal apertures towards the shell edges. In ostreids, Gastrochaenolites appears in the right valve oriented towards the lateral edge (Fig. 6J1–2). On the other hand, in G. tournali these structures appear in both the left and right valves, and on both the external and the internal surfaces (Fig. 6U1–3), without any preferred orientation. 4.1.7. Other worms The boring Umbichnus inopinatus is restricted to the cardinal zone of shallow infaunal bivalves, where the ligament is situated. 4.1.8. Echinoderms/Gastropods Scraping traces Gnathichnus pentax and Radulichnus inopinatus normally appear on the inside of the left and right shells, and without a notable distribution pattern (Fig. 5Q1–6, R1–4). 4.1.9. Encrusting skeletobionts Ostreids, anomiids, balanomorphs, bryozoans and serpulids are the main encrusting skeletobionts identified both in infaunal and epifaunal elements. Differences in encrustation were apparent between concave shell interior surfaces and convex shell exteriors. There is an apparent tendency of the skeletobionts to settle in protected areas of disarticulated shells, usually on the concave interior in the lower part of the umbonal area of infaunal bivalves. Oyster-encrusting skeletozoans appear mainly in sheltered areas of shells, normally on the left valves, which are more concave. However, it is worthy of note that ostreids and serpulids occur in bands near the ventral and lateral edges on the external surface of the specimens studied. Pectinidencrusting skeletobionts such as ostreids and balanomorphs are normally located on the outer side of the left valves. Lacrimichnus cacelensis, a trace fossil which is left by encrusting gastropods of the genus Crepidula (Santos et al., 2003, 2004), is found on both left and right valves of G. tournali (Figs. 6W1–2 and 7(7, 8)). These bioerosion structures are basically located in the rib intervals of the ventral area, oriented perpendicularly towards the edge.

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Fig. 5. Contour diagrams showing the spatial distribution of the main bioerosive structures on the most representative bivalves from Cacela. Infauna: Microboring algae: A1–A7: Cavernula pediculata. B1–B12: Semidendrina-form. C1–C6: Ichnoreticulina elegans. D1–D8: Pinaceocladichnus onubensis. E1–E2: Pennatichnus moguerenica. F1–F4: P. luceni. G1–G10: Entobia isp. H1–H3: Caulostrepsis taeniola. I1–I3: C. contorta. J1–J9: Maeandropolydora sulcans. K1–K6: Gastrochaenolites dijugus. L1–L2: Umbichnus inopinatus. M1–M4: Anellusichnus undulatus. N1–N2: Centrichnus eccentricus. O1–O2: Leptichnus dromeus. P1–P2: L. peristroma. Q1–Q6: Gnathichnus pentax. R1–R4: Radulichnus inopinatus. S1–S2: encrusting annelids. T1–T4: encrusting bryozoans. U1–U3: encrusting ostreids. V1–V5: encrusting balanomorphs. Degrees of density: 1: lightest shadow, occupation area values 0–30%; 2: intermediate shadow, occupation area values 30–60%; 3: darkest shadow, occupation area values over of 60%. Fig. 5. Diagrammes de contour schématique montrant la distribution spatiale des principales structures bioérosives sur les bivalves les plus représentatives à Cacela. Infaune : Microperforations d’algues : A1–A7 : Cavernula pediculata. B1–B12 : Semidendrina–form. C1–C6 : Ichnoreticulina elegans. D1–D8 : Pinaceocladichnus

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Fig. 5. (Continued ).

5. Discussion In general terms, infaunal bivalves show a higher incidence level of bioerosion than epifauna. A large majority of

bioerosion structures found on infaunal bivalves are normally produced postmortem and after suffering transport, particularly after disarticulation. On the exterior of right and left valves the posterior area is the most heavily colonised, whereas on the

onubensis. E1–E2 : Pennatichnus moguerenica. F1–F4 : P. luceni. G1–G10 : Entobia isp. H1–H3 : Caulostrepsis taeniola. I1–I3 : C. contorta. J1–J9 : Maeandropolydora sulcans. K1–K6 : Gastrochaenolites dijugus. L1–L2 : Umbichnus inopinatus. M1–M4 : Anellusichnus undulatus. N1–N2 : Centrichnus eccentricus. O1–O2 : Leptichnus dromeus. P1–P2 : L. peristroma. Q1–Q6 : Gnathichnus pentax. R1–R4 : Radulichnus inopinatus. S1–S2 : annélides encroûtantes. T1–T4 : bryozoaires encroûtants. U1–U3 : ostreides encroûtantes. V1–V5 : balanes encroûtantes.

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Fig. 6. Contour diagrams showing the spatial distribution of the main bioerosive structures on the most representative bivalves from Cacela. Epifauna: microboring algae: A1–A2: Cavernula pediculata. B1–B2: Semidendrina-form. C1–C2: Ichnoreticulina elegans. D1–D2: Pinaceocladichnus onubensis. E1–E2: Pennatichnus moguerenica. F1–F2: Entobia isp. G1–G3: Caulostrepsis taeniola. H1: C. contorta. I1–I2: Maeandropolydora sulcans. J1–J2: Gastrochaenolites dijugus. K1: Leptichnus dromeus. L1: L. peristroma. M1–M3: Gnathichnus pentax. N1–N2: encrusting annelids. O1: encrusting bryozoans. P1–P2: encrusting ostreids. Q1: P. onubensis. R1–R2: C. taeniola. S1: C. contorta. T1–T4: M. sulcans. U1–U3: G. dijugus. V1–V2: Anellusichnus undulatus. W1–W2: Lacrimichnus cacelensis. X1: L. peristroma. Y1–Y2: encrusting bryozoans. Z1: encrusting annelids. AA1: encrusting balanomorphs. BB1–BB3: encrusting anomiids. See Fig. 6 for shadow legend.

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inner surface a slight preference for the ventral areas is noted. Epifauna is the most susceptible to bioerosion from epi- and endolithic organisms, thus producing a wider range of ethological categories. Specimens of Ostrea show evidence of bioerosion almost exclusively on their exterior right valve, which is the exposed upper valve most accessible to colonisation. Other epifaunal elements, in particular G. tournali, show similar characteristics. The right valves being the lower ones therefore show less evidence of bioerosion during their lifetime. The bioerosion structures and occupation patterns observed in this study are very similar for both infauna and epifauna.

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5.2. Fungi The absence of any topological preference or a well defined surface distribution pattern of fungal borings may mean that these were made either during the lifetime of the bivalve (when they appear on the outside) or in a more or less advanced postmortem stage of the biosubstrate (where they are more common on the interior of the valve and appear equally distributed). In the latter case, the valves would have been open and probably even disarticulated, and on top of the sediment, thus being exposed completely to the action of microborers. 5.3. Bryozoans

5.1. Microbial euendoliths (algae) The occupation patterns observed on infauna are related to the fact that bivalves, particularly those living near the sediment-water interface, such as G. bimaculata and M. jouanneti, will be the more likely to be exposed to colonisation where uncovered, and thus prone to colonisation on the posterior external surface. When colonisation of this kind is recorded, it can normally be deduced that the structures were produced during the lifetime of the bivalve, normally during a short period of time, or in stages after its death, usually during more prolonged period of time. The concentration of borings located on the inside lateral parts of the edge where the adductor muscles are located is generally low or even nonexistent. This may be due to the dense shell microstructure at the place of attachment of the adductor muscles (Cox, 1969). However, other factors could also play a role, such as remnants of fibrous muscle tissue which normally stay attached for a long time. This tissue, which takes longer to decompose than the softer parts, inhibits microborers from colonising this area (Mayoral, 1986). Another possibility (Mayoral, 1988a) is that the ligament passively opens the shell after the death of the organism, thus allowing sediment to enter and lessening the available space for colonisation. In this context, an interior valve surface with borings means postmortem colonisation. The presence of microborings all over the inside of the valves suggests relatively long periods of exposure free of sediment, during which the skeletophytes had ample time to occupy the entire area. On the other hand, where the internal zones close to the pallial line display well-defined bands of microborings, thus showing a certain amount of concentration, it is likely that the borings were made shortly after death, when the valves began to open, offering ever-widening free areas colonisation inside.

Like in the case of fungal borings, the surface distribution pattern of the structures produced by boring ctenostome and cheilostome bryozoans, on infauna as well as epifauna, may reflect colonisation either during the lifetime of the biosubstrate (particularly when found on the outer areas of the posterior edge of the valves), or in early or advanced postmortem stages. According to Pohowsky (1978), several bryozoan taxa settle on both dead and live mollusc shells. Silén (1947) noted that Penetrantia concharum Silén, 1946, only settler on dead shells, and it has been suggested that the larvae of this species would avoid shells with a periostracum (Pohowsky, 1978). 5.4. Sponges The distribution and patterns observed in clionaid borings on infaunal and epifaunal bivalves implies that they were produced after the death of the biosubstrate. After death the valves were disarticulated and separated, thus facilitating the settlement of these sponges on all surfaces. The greatest density of borings is found on the medial and ventral zones of the posterior parts of infaunal shells. This is due to the fact that these areas were exposed first, or stood out from the seabed after the death of the bivalves, this being the case particularly for those infaunal elements which lived close to the surface. No preferential area was observed on the shell interiors, which showed an equal distribution of the borings. This means that these structures were produced after the death of the bivalve and after a long exposure on the seabed after the valves were separated and dispersed. 5.5. Annelids The structures produced by boring polychaete on Glycymeris and Megacardita shells leave no doubt that they were made during the lifetime of the host substrate (Figs. 5H1–3, I1–3, J1–9 and 7(1–3)). These structures,

Fig. 6. Diagrammes de contour schématique montrant la distribution spatiale des principales structures bioérosives sur les bivalves les plus représentatives à Cacela. Épifaune : microperforations d’algues : A1–A2 : Cavernula pediculata. B1–B2 : Semidendrina-form. C1–C2 : Ichnoreticulina elegans. D1–D2 : Pinaceocladichnus onubensis. E1–E2 : Pennatichnus moguerenica. F1–F2 : Entobia isp. G1–G3 : Caulostrepsis taeniola. H1 : C. contorta. I1–I2 : Maeandropolydora sulcans. J1–J2 : Gastrochaenolites dijugus. K1 : Leptichnus dromeus. L1 : L. peristroma. M1–M3 : Gnathichnus pentax. N1–N2 : annélides encroûtantes. O1 : bryozoaires encroûtants. P1–P2 : ostreides encroûtantes. Q1 : P. onubensis. R1–R2 : C. taeniola. S1 : C. contorta. T1–T4 : M. sulcans. U1–U3 : G. dijugus. V1–V2 : Anellusichnus undulatus. W1–W2 : Lacrimichnus cacelensis. X1 : L. peristroma. Y1–Y2 : bryozoaires encroûtants. Z1 : annélides encroûtantes. AA1 : balanes encroûtantes. BB1–BB3 : anomiides encroûtantes.

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Fig. 7. 1–3. Megacardita jouanneti. 1, 2. Bioerosion in stage I. Posterior edge recording Maeandropolydora sulcans and Caulostrepsis taeniola. 1. RC/M5. 2. RC/10. 3. Idem together with Gastrochaenolites dijugus. RC/M51. 4. Anellusichnus undulatus. Interior of M. jouanneti, produce in bioerosion stage III. RC/9. 5. Circomphalus foliaceolamellosus. Bioerosion in stage III. Internal valve showing M. sulcans, Entobia isp. and G. dijugus. RCCF/14. 6. Detail of Entobia isp. on the external surface of the former specimen. 7. Gigantopecten tournali. Valve exterior showing bioerosion associated to stage I (Lacrimichnus cacelensis, thick black arrows; predatory biting on ventral edge, white arrow) and to stage II and/or III (M. sulcans, black arrow, basal plates of balanomorphs, dashed black arrows, and

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located on the external surface of the posterior part and oriented towards the edges, are arranged in a manner suggesting that their grouping is conditioned by the life position (upright) of these bivalves. The annelids occupied a substrate which is optimally situated at the sediment–water interface. In these shallow endobenthic, suspension feeders, the water flow originating in the posterior areas of the shell make this area ideal for settlement and the capture of all kinds of food by the colonisers. For polychaetes, as suspension feeders, there is a double advantage to establish themselves on this part of the shells. Firstly, they can position themselves on a solid and firm substrate and, secondly, this position allows them to catch suspended particles from the water current produced by the host mollusc siphons. There is no obvious advantage for the host substrate, neither does it suffer from the relationship, which is a classic case of commensalism (Mayoral, 1986; Martin and Britayev, 1998). On the other hand, the presence of borings on the inside of the valves is unmistakable evidence of postmortem colonisation. However, there is a certain preference for borings in the areas close to the lateral and ventral edges of the valves (Figs. 5I2–3, J3, J5 and 7(5)), this implying colonisation immediately after death of the biosubstrate, since these areas are the most immediately accessible, serving as starting points for the invasion of the inside of the shells. With regard to the epifaunal bivalves, such as Ostrea and Gigantopecten, the presence of structures with a directional component, e.g. Caulostrepsis and Maeandropolydora which show a preferred orientation of apertures towards the edges (Fig. 7(12)), on the external surface of the right valves, almost certainly results from their production during life of the host (Fig. 6G1–3, H1, I1–2). As ostreids and pectinids are filterings, these areas close to the edges of the valves are suitable places for the capture of nutrients by colonisers, given that a constant water flow is created carrying substantial amounts of food. The presence of these borings oriented on the inner surfaces (Fig. 7(13, 14)) may, to some extent, be related to an initial colonisation by the skeletozoans immediately after the death of the host substrate, in which the first ones to arrive take advantage of the most accessible areas to establish themselves.

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Although the presence of any kind of bioerosion structure on the lower valves of ostreids almost certainly suggests postmortem colonization, their distribution with a directional component may indicate the contrary. In fact, Caulostrepsis and Maeandropolydora show a preferred orientation towards the edges, especially in the ventral and lateral zones, which are free from the sediment substrate of these bivalves and then may be immediately available for colonization (Fig. 7(12)). 5.6. Boring bivalves The presence of Gastrochaenolites with an oriented pattern on the upper area of the outer surface of M. jouanneti, i.e. with the siphonal openings oriented towards the shell edges, probably means that settlement took place when the host substrate was still alive, since advantage may have been taken of the water flow produced by the host mollusc siphons. Either this or the settlement was immediately postmortem when the host still maintained a position in the sediment similar to the life position. M. jouanneti has a thick shell allowing bivalves to bore it without inflicting serious injury causing the death of the host substrate. However, it is likely that the mollusc host suffered a certain degree of stress. Where bioerosion appears on the inside of the valves, it must be assumed that it occurred postmortem, with the host bivalve in a stable position on the sediment. 5.7. Worms Umbichnus inopinatus is another ichnotaxon produced on a live host or immediately after its death. This worm boring, restricted to the cardinal zone where the ligament is located, may be an example of parasitism. The worm may have established itself in the ligament area when the host substrate was still alive or during the early postmortem stage when the ligament was not yet decomposed. 5.8. Echinoderms/Gastropods The absence of a pattern or a preferred area colonised by scraping structures may suggest that their makers were

ostreids, dashed white arrows). RC/M1. 8. Detail of Lacrimichnus cacelensis. 9. M. sulcans. Structure developed between two ribs in bioerosion stage I. RCGT/3. 10. Cheilostome bryozoan Smittina sp. External side of M. jouanneti, corresponding to bioerosion stage III. RCMJ/11. 11. M. sulcans. Exterior of Pecten benedictus, recorded in the stage III. N/5. 12. C. taeniola. Apertural furrows oriented towards the ventral edge while host substrate was still alive. RCGT/3. 13. Valve interior of G. tournali. Several structures produced during bioerosion stage III. RCGP/2. 14. Detail of the former picture. Anomiid bivalve (left) and M. sulcans (right). 15. Cavernula pediculata. Same specimen. 16. Pinaceocladichnus onubensis. Boring of ctenostomate bryozoan. Same specimen. 17. Gnathichnus pentax. All specimens are housed in the collection of University of Algarve (Portugal). 1–3, 5, 7, 8, 12, 13, scale bar = 1 cm; 4, 9, 11, 17, scale bar = 2 mm; 10, 15, 16, scale bar = 1 mm. Fig. 7. 1–3. Megacardita jouanneti. 1, 2. Bioérosion pendant la phase I. Marge postérieure avec Maeandropolydora sulcans et Caulostrepsis taeniola.1. RC/M5. 2. RC/10. 3. Idem avec Gastrochaenolithes dijugus. RC/M51. 4. Anellusichnus undulatus. Face intérieure de M. jouanneti, enregistrée pendant la phase III. RC/9. 5. Circomphalus foliaceolamellosus. Bioérosion pendant la phase III. Face intérieure montrant M. sulcans, Entobia isp. et G. dijugus. RCCF/14. 6. Détail de Entobia isp. sur la surface extérieure de l’exemplaire antérieur. 7. Gigantopecten tournali. Valve extérieure montrant la bioérosion associée à la phase I (flèche noire : Lacrimichnus cacelensis. La flèche blanche signale une trace de prédation sur le bord ventral) et à la phase II et/ou III (M. sulcans, flèche large, et plaques basales de balanes, flèche noire discontinue et d’ostréidés, flèche blanche discontinue). RC/M1. 8. Détail de L. cacelensis. 9. M. sulcans. Structure développée entre deux côtelettes pendant la phase I de la bioérosion. RCGT/3. 10. Bryozoaire chilostome Smittina sp. Face extérieure de M. jouanneti, correspondant à la phase III de la bioérosion. RCMJ/11. 11. M. sulcans. Sur la valve extérieure de Pecten benedictus, enregistrée pendant la phase III. N/5. 12. C. taeniola. Sillons de l’ouverture orientés vers le bord ventral quand le biosubstrat était encore vivant. RCGT/3. 13. Face intérieure de G. tournali. Plusieurs structures bioérosives sont produites pendant la phase III de la bioérosion. RCGP/2. 14. Détail de la figure antérieure. Bivalve anomiide (gauche) et M. sulcans (droite). 15. Cavernula pediculata. Même exemplaire. 16. P. onubensis. Perforation de ctenostomate bryozoaire. Même exemplaire. 17. Gnathichnus pentax. Tous les exemplaires sont déposés dans la collection de l’université d’Algarve (Portugal). 1–3, 5, 7, 8, 12, 13, barre d’échelle = 1 cm ; 4, 9, 11, 17, barre d’échelle = 2 mm ; 10, 15, 16, barre d’échelle = 1 mm.

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Table 2 Temporal occurrence of bioerosive structures based on their location for infaunal and epifaunal bivalves Tableau 2 Temporalité des phases de colonisation selon l’emplacement des structures bioérosives sur les mollusques bivalves

herbivores feeding on algae occurring on any part of the shell. Naturally, these structures were produced after the death of the host substrate in those cases where they occur on the inside of the valves.

5.9. Encrusting skeletobionts Differences in encrustation are apparent between concave shell inner surfaces and convex shell exteriors. The tendency of

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the skeletobionts to settle in protected zones of disarticulated infaunal shells is apparent and understandable since these areas provide a better chance for the larvae develop (Fig. 5S1–2, T1–4, U1–3, V1–5). This reasoning is based on the position of the skeletobionts (direct evidence) (Fig. 7(10)), or the position of bioerosion structures visible on the biosubstrate (indirect evidence). These skeletozoans must have settled during in a phase in which the host valves were already open, either disarticulated in situ, or separated and dispersed over a longer period of time. This hypothesis is confirmed by the presence of structures like Centrichnus eccentricus and Anellusichnus undulatus located on the central area of the interior valves (Figs. 6M1–2, N2 and 7(4)). Another argument in favour is the presence of Leptichnus dromeus and L. peristroma, appearing all over the valve interior (Fig. 5O1–2, P1–2). When various different kinds of encrusting skeletobionts occur inside the shells, a postmortem colonisation of the substrate is indicated, either at an early stage as suggested by the occupation of areas close to the edges, or in later stages after the valves were separated and dispersed over a longer period of time. When encrusting skeletozoans appear on the outer surface of the shells the colonisation process almost certainly took place during the lifetime of the biosubstrate. The presence of Lacrimichnus cacelensis on the ventral edges of the lower valves of G. tournali (Figs. 6W1–2 and 7(7, 8)) is explained by the fact that these areas are not in contact with the sediment, and therefore, open to colonisation, at the same time providing good protection. Where these structures are oriented perpendicularly to the rib intervals, a clear example of commensalism is suggested. Observations have been made with the aim of reconstructing colonisation sequences. However, distinguishing between life and postmortem skelotobiotic associations is not a simple matter. Difficulties arise particularly when certain skeletobionts are likely to colonise both during the lifetime of the host susbtrate and postmortem. However, certain criteria may be used (Taylor and Wilson, 2003). Using these criteria, three main colonisation stages may be proposed (Table 2):  stage I includes the structures produced during the life of the host substrate. In hemifaunal biosubstrates this stage is characterised by the location of bioerosion structures exclusively on the external shell surface (posterior edges). Most representative borings at this stage are Caulostrepsis and Gastrochaenolites, which present a preferential orientation of apertures towards the outer edge. The area that structures occupy obviously depends on the position of the bivalve in its substrate (e.g., posterior zone when the commissure of the bivalve is oriented perpendicularly to the substrate). In the case of epifaunal biosubstrates, this kind of bioerosion structures is found either on the outside of the upper valves (left valve in pectinids, right valve in ostreids) or on the free areas of the lower valves. Annelid borings are arranged in concentric bands in intervals between the ribs, parallel to the growth lines of the bivalve in the case of Maeandropolydora, or with the apertures

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oriented towards the ventral edge, in the case of Caulostrepsis. The homing scars left by the attachment of Crepidula gastropods (Lacrimichnus) also are a good example of a colonisation during the lifetime of the host, since it is possible to see an average size increase in Lacrimichnus towards the older part of the rib intervals of G. tournali;  stage II is characterised by structures produced in a period immediately following the death of the bivalve when, in most cases, it still retained a position close to its life position. In this stage, the bioerosion structures cover a greater area on the external surface of the valves and begin to appear without a well-defined preferred orientation, while colonisation of the internal surface moves inward from the edges. This occurs in both infauna and epifauna;  stage III corresponds to structures clearly produced postmortem, when the valves of the bivalve were already disarticulated and/or separate, showing signs of a relatively prolonged exposure on the seabed. In this stage the bioerosion structures occupy the entire surface area of the valve, both externally and internally. Some of them, especially those produced by fungi, algae, and sponges are postmortem. Encrusters such as bryozoans, balanomorphs, ostreids, anomiids and serpulids presented on the inner surface of valves, such as the internal area close to the cardinal plate, are also postmortem. 6. Conclusions Despite very low boring and encrustation rates, the diversity of bioerosion structures is remarkable, with 24 ichnotaxa identified. The low incidence of bioerosion together with the bioeroders identified were related with substrate ‘‘maturity’’, and appears to reflect only limited exposure time of the shells at the sediment–water interface. From a palaeoecological perspective, the identification of all of these bioerosion structures is in agreement with the palaeoenvironmental characteristics inferred for Level 3 (GonzálezDelgado et al., 1995; Santos, 2000). The abundant presence of microendolithic borings, in comparison with other structures, suggests a shallow euphotic zone in a sublittoral or shallow inner shelf environment. Since many microborers are photosynthetic their abundance can largely be explained by the degree of light penetration through the water column (Golubic et al., 1975; Glaub, 1994; Vogel et al., 1995; Radtke and Golubic, 2005). Some green algae such as Ostreobium quekettii (ichnospecies I. elegans) have been shown to be excellent indicators for the photic limit (Wisshak et al., 2005). Fungal microborers are not constrained in this way since they are heterotrophic (Golubic et al., 1975) and occur throughout a wide bathymetric range (to depths > 500 m; Budd and Perkins, 1980; Vogel et al., 1996). Under normal circumstances, the sandy bottoms of the studied area would be subject to a fairly long lasting, stable regime under moderate-energy conditions. The net sedimentation rate may have been low, favouring polychaete ichnogenera Caulostrepsis-Maeandropolydora which are found to be the

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most abundant, second to microborings. Under this sedimentation regime, repeated short and rapid burial events will have inhibited the establishment of other borers needing a longer time to settle, such as clionaid sponges, lithophagous bivalves, as well as encrusters (balanomorphs, annelids, ostreids, bryozoans, etc.). Experimental studies on bioerosion recorded bivalves and sponges only after three years of exposure (Kiene, 1985; Kiene and Hutchings, 1992). The paucity of Entobia corroborates this interpretation, as its occurrence implies a prolonged stay of the biosubstrates on the seabed. In agreement with Lescinsky et al. (2002) and Rodland et al. (2004), exhumation cycles and reburying by sediments carried in suspense rapidly coated and buried shells after death. This resulted in little time-averaging, and controlled the bioerosion and encrusting rate on mollusc bivalves. According to Bromley et al. (1990) and Lescinsky et al. (2002), the bioerosion intensity would increase with exposure time. Bioerosion structures are scarce in Levels 6 and 7. This could be due to rapid burial or, more likely, considerable loss of information due to diagenetic dissolution. Another factor affecting bioerosion and encrustation patterns is the habit of the host organism. Usually, epifaunal shells present greater bioerosion and encrustation on convex surfaces, compared to infaunal shells, because the latter were colonised during their lifetime. The valves of infaunal bivalves must be exhumed before encrusters or bioeroders can colonise them. Similarly, the external posterior area of shallow endobenthic bivalves is the first one to be colonised, since this is the most accessible area for any bioeroder. Despite certain limitations, the bioerosion structures observed may be ordered chronologically. The first colonisation stage on infauna is associated with lifetime structures, such as preferentially oriented Maeandropolydora and Caulostrepsis, which are only located on external surfaces, mainly in the posterior area. The first colonisation stage on epifaunal hosts is similarly mirrored by annelid borings arranged in parallel bands along growth lines, or oriented towards the outer edges. These zones of the valves are swept by constant water flows along valve edges. In the second colonisation stage, bioerosion structures begin to occupy a larger external area of the valve, and to colonise the ventral area of its interior, without exhibiting any preferred orientation with regard to the host morphology. The last colonisation stage is clearly postmortem, taking place when the valves are disarticulated and showing signs of a fairly long exposure on the sea floor. Acknowledgements Constructive and timely reviews of the final manuscript by two anonymous referees are greatly appreciated. Financial support was provided by Fundação para a Ciência e a Tecnologia (Portuguese government) in the form of a postdoctoral fellowship (Praxis/BPD/20562/2004/FQ9R) cofinanced by POCI 2010 to A. Santos. Financial support was also provided by Junta de Andalucía (Spanish government) to the Research Group RNM316 (Tectonics and Palaeontology) and by Ministerio de Educación y Cultura of Spain (Project CGL2007-60507/BTE).

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