Bathymetric distribution of ichnocoenoses from recent subtropical algal nodules off Fraser Island, eastern Australia

Palaeogeography, Palaeoclimatology, Palaeoecology 369 (2013) 58–66

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Bathymetric distribution of ichnocoenoses from recent subtropical algal nodules off Fraser Island, eastern Australia Davide Bassi a,⁎, Yasufumi Iryu b, 1, Juan C. Braga c, Hideko Takayanagi b, Yoshihiro Tsuji d a

Dipartimento di Fisica e Scienze della Terra, Università degli Studi di Ferrara, via Saragat 1, I-44122 Ferrara, Italy Department of Earth and Planetary Sciences, Graduate School of Environmental Studies, Nagoya University, Nagoya 464–8601, Japan Departamento de Estratigrafía y Paleontología, Universidad de Granada, Campus Fuentenueva s/n, 18002 Granada, Spain d Exploration Department, Japan Oil, Gas and Metals National Corporation, Toranomon Twin Building, 2-10-1 Toranomon, Minato-ku, Tokyo 105–0001, Japan b c

a r t i c l e

i n f o

Article history: Received 21 March 2012 Received in revised form 1 October 2012 Accepted 4 October 2012 Available online 11 October 2012 Keywords: Ichnocoenosis Coralline red algae Subtropical carbonates Bioeroder distribution Recent Australia

a b s t r a c t Coralline algal nodules living on the subtropical shelf off Fraser Island, eastern Australia, from the inner to the uppermost outer-shelf, from 28 to 117 m water depth are pervasively bioeroded. Five ichnogenera have been identifed as nodule borers, comprising one ichnotaxon attributed to bivalves (Gastrochaenolites), one to sponges (Entobia) and three to polychaetes and barnacles (Trypanites, Maeandropolydora, Rogerella). Microtraces comparable to those produced by fungi, algae, bacteria and/or sponges are also present. Two ichnocoenoses have been recognised. The ‘shallow’ water ichnocoenosis (EGTM) occurs at 60 m and shallower depths and includes all identified ichnogenera. The ‘deep’ water ichnocoenosis (from 68 to 117 m) is characterised by Trypanites and the Trypanites/Maeandropolydora network (TM ichnocoenosis) with a generally higher boring density than in shallower nodules. Decreasing size of algal nodules and reduced thickness of the coralline thalli probably explain the decrease in diversity of ichnogenera with depth, as the larger bioeroders are excluded from the ichnoassemblages. Lower growth rates favour higher density of bioerosion in deeper algal nodules. © 2012 Elsevier B.V. All rights reserved.

1. Introduction Ichnological data such as tiering, ichnotaxonomic composition, and trace density can be used to reconstruct a wide range of paleoenvironmental parameters (Taylor et al., 2003). In particular, spatial patterns of macroborings and microborings can be applied as proxies of water paleodepth if they can be attributed to the action of specific borers, particularly those associated with photosynthetic algae (Bromley and Asgaard, 1993; Bromley, 1994; Perry, 1998; Blanchon and Perry, 2004). For example, Gnathichnus, the structure produced by algal-grazing echinoids, and Entobia gonoides, the work of the sponge Cliona virides (with algal symbionts) have been considered restricted to depths of a few metres (Taylor et al., 2003). Perry and Hepburn (2008, fig. 7) broadly characterised different reef sub-environments by the types and relative abundance of key boring species, which can potentially be applied to interpret ancient examples. Using a uniformitarian approach, paleodepths can be inferred for Neogene and younger sediments, if borings can be attributed to extant taxa. For example, Gastrochaenolites formed

⁎ Corresponding author. E-mail addresses: [email protected] (D. Bassi), [email protected] (Y. Iryu), [email protected] (J.C. Braga), [email protected] (H. Takayanagi), [email protected] (Y. Tsuji). 1 Present address: Institute of Geology and Paleontology, Graduate School of Science, Tohoku University, Aobayama, Sendai 980–8578, Japan. 0031-0182/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.palaeo.2012.10.003

by Lithophaga is believed to reflect very shallow water depth (Goldring, 1995; Taylor et al., 2003). There is, however, a sampling bias of living ichnoassemblages toward very shallow-water settings (b10 m; Crimes and Harper, 1970; May et al., 1982; Gibert de et al., 1998; Greenstein and Pandolfi, 2003; Bromley and Heinberg, 2006; Santos et al., 2010) that can potentially lead to misinterpretation of present-day depth zonations and facies models, and affect subsequent palaeobathymetric reconstructions of fossil analogues. Nonetheless, off shore boring ichnocoenoses are common in present-day shelf carbonates (Bassi et al., 2012; Nunes Leal et al., 2012) and their study might provide new insights on the distribution of ichnoassemblages and their application to interpret ancient environments. In fact, an ichnocoenosis so far identified only in shallow-marine rockgrounds and hardgrounds and in firm, compacted, but unlithified substrates, occurs in living macroid assemblages from deep fore-reef to shelf settings in Central Ryukyu Islands (south-western Japan), ranging in water depth from 61 to 105 m (Bassi et al., 2011). This study reports ichnocoenoses constituted by macroborers such as bivalves, sponges, sipunculid and polychaete worms, and barnacles in living algal nodules from the shelf off Fraser Island in southern Queensland, eastern Australia (Fig. 1). Comparable ichnocoenoses were previously considered to be absent in relatively deep-water shelf environments. This contribution demonstrates that variation in ichnodiversity in algal nodules is mainly related to algal-nodule size and thickness of coralline algal plants. Thus, a secondary goal is to provide examples of ichnodiversity grades in present-day subtropical

25°S

50 km

59

Fine-grained quartz sand Coarse-grained carbonate sand

300

0

100 200

D. Bassi et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 369 (2013) 58–66

Fraser Island

24°40'S

Rhodolith-coral gravelly

Australia

Coral bio-lithite Carbonate fine sand

Grab sample

longshore current

Studied area

26°S

Noosa Heads

East Australian Current

Dredge sample 24°50'S

DR008 GS071

GS070 DR007

GS093 GS092

Fraser Island

GS091

25°00'S DR021 DR002 GS089

Gardner Bank DR018

27°S 25°10'S

40

4000 00 30 2000 0 100 500

BRISBANE

20

DR019

rhodolith deposits for evaluation of palaeoenvironmental reconstruction in sedimentary successions bearing conspicuous rhodolith content, regardless of geologic age. Ichnocoenosis distribution studied from Recent deposits provides a useful means for comparison with fossil deposits of all ages.

2. Geographical setting and sedimentary facies The study area is located offshore from Fraser Island, roughly between 24°50′ S and 25°20′ S, at the southern limit of deposition of tropical carbonates in the eastern Australian continental margin (Fig. 2). The area is subjected to occasional high nutrient supply (e.g. upwelling off Fraser Island; Australian Dept. of Sustainability, 2011) and to seasonal low water temperatures, having the greatest impact during late spring/summer (Malcolm et al., 2011). A flat inner shelf extending to 45 m depth, is followed by a gently sloping middle shelf from 45 to 100–110 m, with several banks rising to shallower depths. A nearly continuous terrace at about 105 m marks the boundary with the outer shelf, which descends to 210–450 m (Marshall et al., 1998). Five facies have been distinguished in the shelf surface sediments. Fine-grained quartz sand covers the inner platform, whereas coarse-grained carbonate sand occurs from 40 to 80 m. Coral boundstones appear on the banks and rhodolith-coral gravels extend from the banks to the lower limit of the middle shelf (Harris et al., 1996; Marshall et al., 1998). Carbonate fine sand facies predominate below 110 m water depth (Tsuji et al., 1994a,b; Marshall et al., 1998). Algal nodules occur in all facies but they are most common in the middle-shelf bioclastic gravels.

0

10 km 153°20'E

153°30'E

153°40'E

200

Fig. 1. Geographical map of Fraser Island and location of the studied area. The south flowing East Australian Current provides warm water along the outer shelf and upper slope and support carbonate production along the southeastern Australian margin (Marshall et al., 1998; Schröder-Adams et al., 2008).

25°20'S

GS079

300

154°E

100

153°E

153°50'E

Fig. 2. Facies distribution on the shelf and upper slope off Fraser Island and sample location (from Marshall et al., 1998). Grab and dredged samples were collected during a scientific survey cruise carried out in 1991 jointly by the Australian Geological Survey Organization (AGSO) and Japanese National Oil Corporation (JNOC) (Tsuji et al., 1994a,b). Bathymetry in meters. Dredged-sample segment not to scale.

3. Materials and methods The studied algal nodules were collected as dredged and grabbed samples (31) from surficial sediments along seven transects (Marshall et al., 1998), from the sea floor off Fraser Island during a scientific survey cruise carried out in 1991 jointly by the Australian Geological Survey Organization (AGSO) and Japanese National Oil Corporation (JNOC). According to Steneck (1986), the term “algal nodule” includes both coated pebbles/cobbles (b 50% coralline red algae) and rhodoliths (>50% corallines) (Bosellini and Ginsburg, 1971; Bosence, 1983; Peryt, 1983). The nodules were actively growing when collected, as shown by their reddish colours characteristic of living coralline algae. The pigments responsible for the red colour rapidly decay after algal death, resulting in whitish coralline skeletons typical of fossil rhodoliths. The polarity of the last growth phase can be recognised by the location of coloured living corallines on the algal nodule surface. Although rhodoliths can be moved by currents affecting the shelf, algal nodules are considered to be essentially in situ growths (Marshall et al., 1998) and re-deposition of shallow-water rhodoliths in deeper settings can be discarded. The nodule internal structure, their taxonomic composition and borings affecting the algal nodules have been observed in 280 ultra-thin sections (about 10 μm in thickness). The outer surface and sectioned

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Table 1 List of examined samples and their depth distribution (in meters). GS, grab sample; DR, dredged sample; F, sedimentary facies (after Marshall et al., 1998); R, rhodolith-coral gravelly facies; Q, quartz fine sand facies; Cf, carbonate fine sand facies. See Fig. 2 for sample location. Sample

Area

Depth

F

Setting

DR008 DR008-2 DR008-6 GS071 GS089 DR007 DR007 drum 48 DR007-1 DR007-10 GS093 DR002 DR002-7 DR019-017 DR019-16 DR019-21 DR019-22 DR019 GS079 GS092 GS092 GS018 DR018 DR018 GS086 GS097 DR021 GS085 GS070 GS070 GS091 GS091

2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2

28 28 28 28 40 43 43 43 43 46 52 52 54 54 54 54 54 57 57 57 60 60 60 68 87 92 94 106 106 117 117

R R R R Q R R R R R R R R R R R R R R R R R R R R R R Cf Cf R R

Gardner Bank Gardner Bank Gardner Bank Gardner Bank Gardner Bank Gardner Bank Gardner Bank Gardner Bank Gardner Bank Gardner Bank Gardner Bank Gardner Bank South Gardner South Gardner South Gardner South Gardner South Gardner South Gardner South Gardner South Gardner South Gardner South Gardner South Gardner Shelf edge Shelf edge Shelf edge Shelf edge Shelf edge Shelf edge Shelf edge Shelf edge

et al., 2012), was also assessed. BI= 0 corresponds to no bioerosion, whilst BI= 6 represents complete bioerosion with undistinguishable inner features due to repeated overprinting. The studied material is deposited at the Institute of Geology and Paleontology, Graduate School of Science, Tohoku University and at the Departamento de Paleontología y Estratigrafía, Universidad de Granada, Spain.

4. Results

Bank Bank Bank Bank Bank Bank Bank Bank Bank Bank Bank

and polished surfaces of 80 algal nodules were observed with a binocular microscope as well. Bioeroder traces have been identified at ichnogenus level (after Bromley and D'Alessandro, 1983, 1984, 1989; Kelly and Bromley, 1984; Perry, 1996; Edinger and Risk, 1996). A semi-quantitative estimation of abundance of traces has also been made. The Bioerosion Index (BI) that indicates the extent to which the primary coralline thallial features are still observable and the borings are overprinted (Bassi

Algal nodules were collected from 28 to 117 m depths (Table 1). Following the division made by Lund et al. (2000) of living algal nodules off Fraser Island, the identified ichnocoenoses are separated in ‘shallow’ water (60 m and less) and ‘deep’ water (down to 117 m). The traces present within algal nodules can be assigned to five different ichnotypes according to their morphology (Fig. 3). These traces comprise one ichnotaxon attributed to the activity of bivalves (Gastrochaenolites), one to sponges (Entobia) and three to polychaetes/ sipunculids and barnacles (Trypanites, Trypanites/Maeandropolydora network, and Rogerella). Microtraces comparable to those produced by microborers such as fungi, algae, bacteria and/or sponges are also present. The largest borings are those of bivalves that produce the ichnogenus Gastrochaenolites, known today to be excavated by the mytiloid Lithophaga and the myoids Gastrochaena and Hiatella (Kelly and Bromley, 1984). The studied specimens often have articulated bivalves preserved inside them (Figs. 3–4). Gastrochaenolites in the study samples is ellipsoidal in shape with the main axis usually perpendicular to the hard-substrate surface and ranges from 2 to 4 mm in diameter at its widest cross-sections. The apertural region of the boring, which is circular and generally abraded, is narrower than the main chamber. The main chamber of Gastrochaenolites can be identified some millimeters deep in the algal nodules (Fig. 4), with its tubes reaching/keeping up the last nodule growth stage, with no preference for exposed or cryptic surfaces. Gastrochaenolites does not occur in algal nodules smaller than 3 cm. The ichnogenus Entobia is produced by etching sponges (Bromley and D'Alessandro, 1984, 1989; Figs. 4–5). These borings, occurring abundantly from shallow algal nodules to deep water rhodoliths, show single or multiple, wide (2–4 mm in width) chambers with an irregular rounded–ovoid shape. Narrow apertures (0.2–0.5 mm in diameter) are either connected to other chambers or to the outer

Fig. 3. Ichnotaxa identified in the rhodolith facies off Fraser Island, eastern Australia. A, Gastrochaenolites isp. in a coralline red algal plant (DR019-21, 54 m). B, Entobia isp. deeply boring a coralline algal thallus (DR019-21, 54 m). C, Gastrochaenolites isp. and Trypanites/Maeandropolydora network (DR021, 92 m). D, Trypanites isp., Gastrochaenolites isp. and Entobia isp. (DR007-drum48, 43 m). E, Rogerella isp. (DR019, 54 m). See Fig. 2 and Table 1 for geographic and bathymetric location of samples.

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Fig. 4. Slab surfaces of algal nodules showing complex boring patterns and morphologies bioerosion traces from the ‘shallow’ water ichnocoenosis (see text for details). A, sample DR008, 28 m. B–G, sample DR007, 43 m. H–K, M, sample DR002, 52 m. L, sample DR019, 54 m. E, Entobia; G, Gastrochaenolites; T, Trypanites; T/M, Trypanites/Maeandropolydora; R, Rogerella. See Fig. 2 for geographic location of samples.

surface of the rhodoliths. Small and short apertural canals were very rarely identified. The most common boring ichnotaxon in the studied rhodoliths is the long cylindrical Trypanites produced by boring polychaetes (Bromley, 1992, 1994; Figs. 4–5). This trace is a simple boring with a single aperture, consisting of a cylindrical tube, generally perpendicular to the substrate surface, with an almost constant diameter and a rounded termination. The tube ranges in size from 1 to 4 mm in diameter and 3 to ca. 15 mm in length. The coralline host of Trypanites sometimes grows over the opening of the boring. Trypanites is abundant on the undersides and in cavities of the Fraser Island algal nodules. The straight borings of Trypanites often constitute a complex network with branched tubular borings characteristic of Maeandropolydora. Such networks are here included in the Trypanites/Maeandropolydora trace group (Figs. 4–5). The Trypanites/Maeandropolydora network, produced by boring polychaetes (Bromley and D'Alessandro, 1983), consists of tubular galleries, irregularly convoluted, sometimes looping round and coming into contact with themselves or intercepting other similar

borings. The gallery diameter ranges from 0.3 to 1.5 mm and the length from 1.5 to 12 mm. The trace network is developed freely in all directions within thick coralline algal thalli, while the network is parallel and superficial within thin ones, which often alternate with other encrusting organisms (mainly bryozoans and serpulids). Acrothoracican/thoracican barnacle borings of the ichnogenus Rogerella are relatively rare in the off-Fraser Island algal nodules. They are only found on the outer coralline surface in the last algal nodule growth stage (Figs. 3–4). When present, they are abundant, but they have been recorded on less than 2% of the nodules we examined. The identified barnacle borings, locally associated with the producing barnacle, range from 1.5 to 2 mm in length, 0.50 to 1 in width, and up to 2 mm in depth. 4.1. ‘Shallow’ water ichnocoenosis Coralline algae in the studied samples at 60 m water depth and shallower are different in taxonomic composition, diversity and

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Fig. 5. Slab surfaces of studied rhodoliths showing complex boring patterns and the morphologies of bioerosion traces from ‘deep’ water ichnocoenosis (see text for details). A–B, E, sample DR018, 60 m. C–D, sample DR021, 92 m. E, Entobia; G, Gastrochaenolites; T, Trypanites; T/M, Trypanites/Maeandropolydora. For the geographic location of the samples see Fig. 2.

growth-forms from those in deeper samples (for details see Lund et al., 2000). Coralline nodules can be algal-coated pebbles and cobbles, and rhodoliths. Nodules show a wide size range (from ca. 10 to 90 mm) in all sample sites and within a single locality. Nodule shapes range from spheroidal to ellipsoidal to discoidal and very discoidal, highly depending on size and shape of nuclei. At 52 m (sample DR002), the encrusting foraminifer Acervulina contributes with coralline red algae to make up algal nodules. The ichnocoenosis is represented by all the identified ichnotaxa (EGTM: Entobia, Gastrochaenolites, Trypanites, Maeandropolydora; Rogerella) which can occur as abundant (Table 2, Fig. 6). Gastrochaenolites occurs in all the studied nodules as common to abundant, whereas Entobia and Trypanites are locally rare. Rogerella is less common and has been identified mostly at 28 m, the shallowest sample site (samples DR008, GS071). It is rare to abundant on the outer surfaces of algal nodules. The rare occurrence of Rogerella in sample DR019 at 54 m is noteworthy. At 60 m (sample DR018-13, DR018-14) the ichnoassemblages are constituted by all the ichnotaxa identified except Rogerella, being Gastrochaenolites the most characteristic ichnotaxon (Fig. 6). No relationship of ichnoassemblage diversity with rhodolith shape has been recognized. Rhodoliths smaller than ca. 2 cm with lumpy growth-forms never bear borings. The BI is 2 in the shallower algal nodules.

4.2. ‘Deep’ water ichnocoenosis Algal nodules deeper than 60 m are all rhodoliths. They are less variable in size than those in shallower depths, with maximum dimensions ranging from ca. 20 to 50 mm. As in the shallower algal nodules, the shapes range from spheroidal to ellipsoidal, discoidal and very discoidal. Coralline thalli in deep-water rhodoliths are significantly thinner than the ones building the shallow-water nodules (Lund et al., 2000). In deep rhodoliths, Trypanites is common and can be abundant as Trypanites/Maeandropolydora network (TM ichnocoenosis). Entobia is abundant at 92 m (sample DR021) and rare at 117 m (GS017). Gastrochaenolites is rare (only occurs at the 92 m, sample DR021). The deepest studied samples are characterized by abundant Trypanites/ Maeandropolydora networks (87 and 94 m, samples GS097, GS085), common Trypanites and Trypanites/Maeandropolydora networks (from 92 to 117 m; DR021, GS085, GS070, GS091; Table 2). Trypanites and Maeandropolydora are randomly located within the nodules, being localized from the early to the last rhodolith growth stage. The borings are often interpenetrated, cross-cutting previous traces, except Gastrochaenolites which is never subjected to other boring activity. This pattern of bioerosion corresponds to a BI of 3 which, in rare samples, can be 4. As for the ‘shallow’ water ichnocoenosis, no relationship

D. Bassi et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 369 (2013) 58–66 Table 2 Distribution of different types of traces produced by macroendolithic borers in the studied algal nodules. All these macroborers operate through multiple phases of bioerosion, resulting in a high degree of substrate (algal nodules) alteration. E, Entobia (sponge traces); G, Gastrochaenolites (bivalve traces); T, Trypanites (sipunculan traces); T/M, Trypanites/Maeandropolydora (sipunculan/polychaete trace network); R, Rogerella (barnacle traces); A, abundant; C, common; R, rare; no entry, absent. See Fig. 2 for sample location. Sample

Depth (m)

DR008 DR008-2 DR008-6 GS071 GS089 DR007 DR007 drum 48 DR007-1 DR007-10 GS093 DR002 DR002-7 DR019-017 DR019-16 DR019-21 DR019-22 GS079 GS092 DR018-13 DR018-14 GS086 GS097 DR021 GS085 GS070 GS091

28 28 28 28 40 43 43 43 43 46 52 52 54 54 54 54 57 57 60 60 68 87 92 94 106 117

E

G

T

C

A A C

R C C

A A A A

A A A

C A

C C

A A

A A

A R R A

R

R A A

R

C R C R R A A A A R C A C C A R A A C C C R

T/M R A C C A A R A A A A C C C R R R

R

A R

R

A A A A R C

of ichnoassemblage diversity with rhodolith shape was recognized. Rhodoliths smaller than ca. 2 cm in diameter with encrusting growth-forms never bear Entobia or Gastrochaenolites. These two ichnogenera do not occur in the early growth stages of the larger rhodoliths. 5. Discussion The ichnocoenoeses described here occur in the algal nodules that were analysed in detail by Lund et al. (2000). These authors found that shallower algal nodules have larger mean size with higher standard deviation than the deeper ones, while there are no changes in nodule shape along depth gradients. All the identified ichnotaxa are present up to abundant along the studied transects in shallow-water nodules, which bear a higher

Fig. 6. Slab surfaces of studied small rhodoliths with encrusting growth-forms showing complex boring patterns and the morphologies of bioerosion traces from ‘deep’ water ichnocoenosis (see text for details). A–C, sample GS086, 68 m. D–F, sample GS097, 87 m. T, Trypanites (arrow heads); T/M, Trypanites/Maeandropolydora (arrows). For the geographic location of the samples see Fig. 2.

63

ichnodiversity than the deeper ones. The shallowest studied algal nodules are characterized by EGTM ichnocoenosis. Rogerella, an acrothoracican/thoracican barnacle boring, occurs as abundant at 28 m and as rare at 54 m water depth. This ichnogenus has been up to now recorded from lagoon to intertidal zones in reefs in less than 25 m (Gingras et al., 2004; Perry and Hepburn, 2008; Montaggioni and Braithwaite, 2009). In the fossil record, this ichnogenus has only been reported from crinoid ossicles in coral-sponge reefs (Middle Jurassic, Wilson et al., 2010; see also Codez and de Saint-Seine, 1958). In samples deeper than 60 m, abundant to common Trypanites and Trypanites/Maeandropolydora network dominate the TM ichnocoenosis down to 117 m depth. Entobia is rare at 68 and 117 m, whilst it occurs as abundant associated with rare Gastrochaenolites at 92 m depth. Therefore, below 60 m there is a clear change from the EGTM ichnocoenosis to TM ichnocoenosis (Figs. 7–8). Shallow-water EGTM ichnocoenosis has been reported from tropical and non-tropical settings, mainly from settings shallower than 30 m, being most records shallower than 10 m (Mediterranean area, Bromley and D'Alessandro, 1989; Bromley and Asgaard, 1993; Atlantic Ocean, Madeira, Johnson et al., 2011; Gulf of Mexico, Blanchon and Perry, 2004; above 30 m in reef systems, Perry and Hepburn, 2008; Montaggioni and Braithwaite, 2009). Recent studies identified EGTM ichnocoenosis in deeper sites (Bassi et al., 2011). The near disappearance of bivalve borings in the ‘deep’ ichnocoenosis is in good agreement with the distributional patterns emerged in recent studies of boring molluscan communities performed on eastern Australia coasts. In eastern Australia and Tasmania, boring bivalves such as Gastrochaena spp., Lamychaena spp. and Rocellaria spp., which produce the ichnogenus Gastrochaenolites, thrive from subtidal to offshore settings boring on corals and limestones (Kleemann, 1990, 1995, 1998; Carter et al., 2008). At northernmost New South Wales, Australia, Smith (2011) found that the density of the endolithic bivalve Lithophaga lessepsiana increases with increasing distance from the coast, down to ca. 10 m depth. In the Queensland area, Wilson (1979) identified nine boring bivalve species from intertidal, through back-reef to offshore settings. The highest diversity is above ca. 30 m depth. Only one species, Lithophaga teres, shows a wide bathymetric range, from intertidal zone down to 66 m, in “calcareous lithothamnion nodules” (Wilson, 1979, p. 440). These patterns have been explained, at least in part, by the great influence of the East Australian Current (EAC) offshore (Smith, 2011). These studies report on diversity and densities of boring bivalves inhabiting coral colonies and limestones. Although evaluations cover only one of the many organisms responsible for bioerosion (Hutchings, 1986; Taylor et al., 2003; Perry and Hepburn, 2008), they nevertheless provided the opportunity to examine predictions made by previous workers that higher nutrient levels (and consequently higher planktonic production) and lower water temperatures, such as those found in high latitude sites, can lead to increased densities of endolithic bioeroders (Highsmith, 1981; Hallock and Schlager, 1986; Glynn, 1997). The upwelling off Fraser Island is a key ecological feature of the Temperate East Marine Region that separates the warm, nutrientpoor waters of the Coral Sea from the cold, nutrient-rich waters of the Tasman Sea (Australian Dept. of Sustainability, 2011; Malcolm et al., 2011). Upwelling and associated nutrient enrichment events are observed along the east coast of Australia and various driving mechanisms were discussed by Roughan and Middleton (2002). The middle to outer shelf off Fraser Island is likely to be subjected to this upwelling (Australian Dept. of Sustainability, 2011, fig. 2.2), and it probably promotes the development of bioeroders. However, the upwelling influence cannot explain the differences in diversity and density found in the identified ichnocoenoses, as its affects the middle shelf waters at any depth. The EGTM ichnocoenosis has been recognised in macroid beds off Kikai-jima (Central Ryukyu Islands, Japan) occurring within forereef environments in discontinuous belts from 60 m down to about

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Fig. 7. Distribution of ichnogenera and their relative abundance in the studied samples. See Fig. 2 and Table 2 for sample location. The average proportion of coralline red algal families and subfamilies in the studied samples is from Lund et al. (2000, Fig. 5). The EGTM ichnocoenosis occurs at 60 m and shallower depth, whilst the TM ichnocoenosis extends down to 117 m. E, Entobia; G, Gastrochaenolites; T, Trypanites; T/M, Trypanites/Maeandropolydora; R, Rogerella; r, rare; c, common; a, abundant.

100 m water depth (Bassi et al., 2011, 2012). In the Kikai-jima macroids Entobia has a great dominance associated with a high abundance of Trypanites and Maeandropolydora throughout the macroid growth stages, while Gastrochaenolites is common in the late growth stages of the larger macroids. In smaller macroids, however, the overall abundance of Entobia and Trypanites is more pervasive. In the EGTM ichnocoenosis, only Gastrochaenolites seems to be excluded from the smaller-sized nodules. Off Fraser Island, the smaller size of the algal nodules deeper than 60 m can explain the virtual absence of Gastrochaenolites in the deeper TM ichnocenosis. The overlap of depth range of the EGTM ichnocoenosis off Kikai-jima with the one of the TM ichnocenosis off Fraser Island suggests that water depth itself does not directly controls the bioeroder assemblages. Bioerosion rates are also affected by additional factors such as energy regime (Tribollet et al., 2002) and sedimentation (Hutchings et al., 2005). The effects of the annual and seasonal variability of the EAC (Hill et al., 2008) on coastal ecology are diverse and so far largely unknown (Suthers et al., 2011). The energy regime cannot be ruled out as ecological factor influencing the identified ichnocoenoses. The accelerator mass spectrometry (AMS) 14C ages of algal nodules off Fraser Islands show that they have been growing for centuries with a very low growth rates (Marshall et al., 1998), and an intermittent growth could not been excluded (Iryu in Tusji et al., 1994a, p. 205). These data testify that the shelf is characterized by a low sedimentation rate down to 117 m. This can explain the occurrence of Entobia, the ichnogenus produced by etching sponges which are inhibited even by low levels of sedimentation (Bromley, 1994). The EGTM ichnocoenosis off Kikai-jima also develops under low sedimentation rate (Bassi et al., 2011, 2012). In this area, tide-induced currents and very low sedimentation rates (Tsuji, 1993; Arai et al., 2008) promote the proliferation of encrusting foraminifer acervulinids, coralline red algae, boring sponges and bivalves. Trypanites-type borings are generally produced by polychaetes but sipunculacean worms and acrothoracican barnacles can also generate similar borings (Ekdale et al., 1984). It is very difficult to distinguish whether Trypanites-like traces have been made by polychaetes/sipunculaceans or barnacles, the latter being indicative of shallower water settings (Brickner et al., 2010). In our case study, Trypanites and the Trypanites/Maeandropolydora network are dominant ichnotaxa both in shallow and deeper water ichnocoenoses.

These structures, made during the lifetime of the host algal nodules and located from the nucleus to the external surface of algal nodules, show no particular orientation patterns, and are arranged in a manner suggesting that their grouping is not conditioned by the life position (upright) of the algal nodules. For polychaetes, common suspension feeders, there is a double advantage to establish themselves on free-living algal nodules. Firstly, they can position themselves on a solid and firm substrate and, secondly, this position allows them to catch suspended particles from the water and keep up feeding even during the occasional nodule overturning (Riisgård and Larsen, 2010). The degree of bioerosion performed by epibionts and endobionts on algal nodules/rhodoliths is determined by the time during which nodules remain within the reach of colonization (residence time). Bioeroder settlement could be controlled by substrate particle size, as size would likely affect rate of nodule overturning and, concomitantly, the survivability of colonizing organisms (Adey and Macintyre, 1973; Bosence, 1983). In the studied algal nodules, Lund et al. (2000) found that in waters shallower than 60 m the nodules are bigger and show a higher variation in size than the deeper ones. Such a decreasing trend in nodule size with water depth corresponds to the decrease in ichnodiversity from the EGTM ichnocoenosis to the TM ichnocoenosis (Table 2, Fig. 7). Moreover, since rhodoliths smaller than ca. 2 cm in diameter with encrusting growth-forms never bear Entobia or Gastrochaenolites, they would offer no suitable settlement sites for larvae of these boring organisms. Rhodoliths similar in size but with lumpy growth-forms do not bear borings at all. The BI fairly increases with water depth indicating a higher bioerosion intensity, perhaps related to a lower growth rate of deeper rhodoliths. The AMS 14C ages of algal nodules suggest long times for nodule growth all over the mid shelf (Iryu in Tsuji et al., 1994a; Marshall et al., 1998) but the growth rate is probably lower in the smaller deeper rhodoliths. The presence of Gastrochaenolites with an oriented pattern (i.e. with the siphonal openings oriented towards the upper nodule surface; Figs. 4–5), means that settlement took place when the host substrate (the nodule) was already stabilized in its last growing phase and did not undergo further overturning. Entobia is settled from the nucleus to the last rhodolith growth stage. The distribution and patterns in clionid borings observed implies that they were produced during nodule

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Fig. 8. Slab surfaces of studied algal nodules and tracings of Gastrochaenolites, Entobia and Trypanites/Maeandropolydora (T/M). A, sample DR007 (43 m); B, sample DR018 (60 m).

growth. During the growth some surfaces were exposed first, colonized by the sponges and then overturned, thus facilitating the settlement sponges on all rhodolith surfaces. Availability of light, water temperature, desiccation, and intensity of grazing by herbivores are the main factors that influence the rates of crustose coralline algal growth (Adey, 1970; Littler and Doty, 1975; Littler and Littler, 1984; Steneck et al., 1991; Figueiredo et al., 2000). In the studied area, Lund et al. (2000) concluded that the coralline-algal assemblage variation with depth is likely due to illuminance decrease, which favours thin coralline plants. Although Gastrochaenolites and Entobia were identified at 92 m, below 68 m small rhodoliths made up of thin coralline thalli are not suitable for boring organisms which need thicker hard-substrate to colonize, and therefore only the less diverse TM assemblage develops. Nonetheless, the primary factors governing macroborer distribution have not yet been clearly differentiated and are presumably interactive, with their relative importance differing from site to site. Taxonomic uncertainties regarding a number of macroboring ichnotaxa mean that it may be difficult to accurately determine the relationship between species and ecological zones (Perry and Hepburn, 2008; Montaggioni and Braithwaite, 2009; Bassi et al., 2011). This restricts the overall use of macroboring imprints as proxies for palaeobathymeric reconstruction (Nebelsick and Bassi, 2000; Bassi et al., 2010, 2011; Checconi et al., 2010). 6. Concluding remarks 1. Five ichnotaxa of borings are found in subtropical algal-nodule beds off Fraser Island, eastern Australia. These beds occur on a very flat inner shelf (extending to a depth of about 45 m), in the middle shelf (45–60 m) and on terrace (down to 117 m), marking the boundary between the middle- and outer-shelf. 2. The ‘shallow’ water ichnocoenosis (at 60 m and shallower) is dominated by Entobia (sponge borings), Gastrochaenolites (bivalve borings), Trypanites and Trypanites/Maeandropolydora network (worm borings) (EGTM ichnocoenosis). Rogerella (acrothoracican/ thoracican barnacle borings) is relatively rare being present only at 28 and 54 m water depth. The ‘deep’ water ichnocoenosis (from 68 to 117 m water depths) is characterised by Trypanites and the Trypanites/Maeandropolydora network (TM ichnocoenosis). Rare Entobia and Gastrochaenolites are locally present. Difficulties in accurately determining a number of macroboring species and ecological zones may restrict the overall use of macroboring imprints as proxies for palaeobathymeric reconstruction. 3. The decrease in ichnodiversity from the EGTM ichnocoenosis to the TM ichnocoenosis corresponds to a decrease in nodule size and coralline thallus thickness with water depth. Below 60 m rhodoliths made up of thin coralline plants are not suitable for boring organisms

which need thicker hard-substrate to colonize. Small rhodoliths with lumpy growth-forms do not bear borings. 4. The higher intensity of bioerosion in the deeper ichnocoenosis might reflect lower growth rates of the smaller, deeper nodules.

Acknowledgements DB gratefully acknowledges the invitation as visiting Professor from the Graduate School of Environmental Studies, Nagoya University, to study the eastern Australian material. Comments from B. Kolodziej and an anonymous reviewer on an earlier draft helped to improve this paper.

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