Paleoenvironment and paleoecological interpretation

According to facies analysis and fossil content, the early–middle Miocene sedimentary succession of Punta Foghe was deposited in a shallow inner sublittoral environment with moderate energy conditions affected by high-energy events.

Agassiza is well represented in facies 2 and 5, indicating shallow settings with sandy sediments. Currently, this genus includes two extant species, both of which are restricted to tropical seas, Agassizia scobiculata Valenciennes, Reference Valenciennes and du Petit-Thouars1846 occurs from littoral to shallow sublittoral depths, while A. excentrica Agassiz, Reference Agassiz1869 is more common at greater depths, from sublittoral to bathyal zones (Mortensen, Reference Mortensen1951; Chesher, Reference Chesher1972; Serafy, Reference Serafy1979; Kier, Reference Kier1984; Lessios, Reference Lessios2005; Alvarado et al., Reference Alvarado, Solis-Marin and Ahearn2010; Galván-Villa et al., Reference Galván-Villa, Rubio-Barbosa and Martínez-Melo2018; Gondim et al., Reference Gondim, De Moura, Christoffersen and Pereira Dias2018). Agassizia are deposit feeders living infaunally in fine-grained sediments (Mortensen, Reference Mortensen1951; Chesher, Reference Chesher1972; Serafy, Reference Serafy1979; Galván-Villa et al., Reference Galván-Villa, Rubio-Barbosa and Martínez-Melo2018; Gondim et al., Reference Gondim, De Moura, Christoffersen and Pereira Dias2018). Agassizia from the Miocene of Punta Foghe are morphologically very similar to A. scrobiculata, the type species of the genus, which has a small to medium globular test, no anterior sulcus, and an anterior ambulacrum (III) that is narrow and weakly depressed adapically with uniserially arranged small pore pairs bearing small penicillate tube feet. The other ambulacra are petaloid and weakly sunken, with entirely rudimentary pores in the anterior column of the anterior petals. Peripetalous and lateroanal fascioles are present.

The Agassizia species from the Miocene deposits studied herein is interpreted as a shallow infaunal form. Since this echinoid lacked respiratory tube feet in the distal half of the anterior column of the anterior paired petals, it did not have the ability to develop a long respiratory funnel through the sediments to the surface and could not burrow deeply. Agassizia is not common in the Miocene sedimentary sequences of Sardinia. It is reported to occur in association with the scutellid Amphiope within conglomeratic levels of the lower Miocene Mores Formation, which represents littoral environments with moderate energy conditions (Mancosu and Nebelsick, Reference Mancosu and Nebelsick2013). A single test was also found in lower–middle Miocene fine-grained sandstones of Porto Torres associated with a spatangoid-dominated fauna reflecting deeper sublittoral environments (Mancosu and Nebelsick, Reference Mancosu and Nebelsick2017a).

Clypeaster is also common in the deposits at Punta Foghe (from facies 2 to 5). Extant representatives of the genus Clypeaster mostly inhabit soft-bottom areas of shallow continental shelves (e.g., Nebelsick, Reference Nebelsick and Lawrence2020 and references therein). In our study, Clypeaster is represented by different morphotypes similar to those exemplified by C. olisiponensis Michelin, Reference Michelin1861, C. latirostris Michelin, Reference Michelin1861, and C. marginatus Lamarck, Reference Lamarck1816. On the basis of morphological features and comparison with recent analogues (see discussion in Mancosu and Nebelsick, Reference Mancosu and Nebelsick2015, Reference Lokier and Al Junaibi2016, Reference Mancosu and Nebelsick2017b), the Clypeaster olisiponensis morphotype, with a highly domed test with thick and tumid margins and flat oral surface, and the Clypeaster latirostris morphotype, with a lower test and relatively thin margin, are interpreted as epibenthic and semi- to shallow infaunal forms, respectively. These morphotypes occur frequently in the Miocene sedimentary deposits of shallow-water settings (see Mancosu and Nebelsick, Reference Mancosu and Nebelsick2015, Reference Lokier and Al Junaibi2016, Reference Mancosu and Nebelsick2017b and discussion therein). The Clypeaster marginatus morphotype with a low, flattened test and thin margins, is interpreted as a shallowly buried to partially burrowed form. It is common as a minor component in spatangoid-dominated assemblages of moderately deep sublittoral environments (Mancosu and Nebelsick, Reference Mancosu and Nebelsick2015, Reference Mancosu and Nebelsick2017b, Reference Mancosu and Nebelsick2019).

In Facies 5, the echinoid assemblage also includes Echinocyamus, Koehleraster, and the brissid spatangoid Plagiobrissus. Modern representatives of Plagiobrissus, such as P. grandis (Gmelin, Reference Gmelin and Gmelin1791) are mainly shallow-water forms, although it has been recorded at a depth of 200 m or more (Mortensen, Reference Mortensen1951; Serafy, Reference Serafy1979). Plagiobrissus grandis lives buried in shallow-water sandy areas (Chesher, Reference Chesher1969; Serafy, Reference Serafy1979; Hendler et al., Reference Hendler, Miller, Pawson and Porter1995; Gondim et al., Reference Gondim, De Moura, Christoffersen and Pereira Dias2018 and references cited therein) and typically burrows to a depth of 50 mm (Kier and Grant, Reference Kier and Grant1965). Plagiobrissus is very rare in the sedimentary succession of Punta Foghe as well as in other Miocene fossil deposits of Sardinia. In the Montiferru area, it is found associated with the Clypeaster marginatus morphotype in fine-grained sandstones.

Extant representatives of the genus Echinocyamus, including E. pusillus (Müller, Reference Müller1776) from the Mediterranean and Atlantic Ocean, show a wide ecological distribution ranging from shallow waters down to 1,250 m depth (Mortensen, Reference Mortensen1948b; Ghiold, Reference Ghiold1982; Grun et al., Reference Grun, Sievers and Nebelsick2014). Echinocyamus pusillus commonly occurs nearshore at depths from 2 to 50 m (Tortonese, Reference Tortonese1965; Zavodnik, Reference Zavodnik2003). It inhabits coarse sandy to pebbly substrates in areas exposed to extensive wave and tidal current activity but is also in medium sands bordering seagrass meadows (Telford et al., Reference Telford, Harold and Mooi1983; Telford, Reference Telford, Keegan and O'Conner1985; Grun et al., Reference Grun, Sievers and Nebelsick2014). Another species, Echinocyamus crispus Mazzetti, Reference Mazzetti1893, lives in poorly sorted fine sands with seagrass in depths between 20 and 30 m in the Red Sea (Nebelsick, Reference Nebelsick1992a, Reference Nebelsickb; Nebelsick and Kowalewski, Reference Nebelsick and Kowalewski1999).

Echinocyamus is common if not locally abundant in the Miocene of Sardinia and occurs in littoral, shallow, and deep sublittoral settings, commonly co-occurring with spatangoid echinoids (Mancosu and Nebelsick, Reference Mancosu and Nebelsick2016, Reference Mancosu and Nebelsick2017a, Reference Mancosu and Nebelsick2019).

The single specimen of Koehleraster recognized herein shows morphological affinities to the recent echinoneoid Koehleraster abnormalis (De Loriol, Reference De Loriol1883), the ecology of which is poorly known. Koehleraster (previously considered synonymous with the genus Echinoneus) occurs in the Indo-Pacific (Ghiold, Reference Ghiold1989; Arachchige et al., Reference Arachchige, Jayakody, Mooi and Kroh2019) from the intertidal to 85 m (Mortensen, Reference Mortensen1948a; Lane et al., Reference Lane, Marsh, VandenSpiegel and Rowe2000). It is reported to inhabit sands under coral heads in lagoonal seagrass flats and under boulders in shallow sublittoral environments (Sloan et al., Reference Sloan, Clark and Taylor1979; Lane et al., Reference Lane, Marsh, VandenSpiegel and Rowe2000). Koehleraster occurs rarely within the Miocene sequences of Sardinia in shallow and moderately deep sublittoral settings (see Mancosu and Nebelsick, Reference Mancosu and Nebelsick2017a, Reference Mancosu and Nebelsickb).

The remains of large oysters and Spondylus, which are commonly associated with clypeasteroid echinoids, are consistent with other Miocene shallow-water depositional settings of Sardinia (Mancosu and Nebelsick, Reference Mancosu and Nebelsick2017b). Throughout the section, the presence of coralline algae points to the photic zone, as does the presence of the larger benthic foraminifera Heterostegina and Amphistegina, which are symbiotrophs and today occur in tropical and warm-temperate seas (e.g., Reiss and Hottinger, Reference Reiss and Hottinger1984; Betzler et al., Reference Betzler, Brachert and Nebelsick1997; Langer and Hottinger, Reference Langer and Hottinger2000; Eder et al., Reference Eder, Hohenegger, Torres-Silva, Briguglio, Birkeland, Coles and Spies2016). Heterostegina is found to prefer hard substrates in clear water (Reiss and Hottinger, Reference Reiss and Hottinger1984) and may reach >100 m depths, with the optimal range between 40 and 70 m (Hottinger, Reference Hottinger1983, Reference Hottinger1997; Hohenegger, Reference Hohenegger1994). In the Oligo–Miocene, it is reported to inhabit high-energy forereef environments (BouDagher-Fadel et al., Reference BouDagher-Fadel, Lord and Banner2000) at depths of 20–30 m (Banner and Hodgkinson, Reference Banner and Hodgkinson1991). Living Amphistegina is adapted to high-energy conditions, although this species also occurs in mud-free sands in areas of seagrass or coralline algae and in reefal areas to depths of 35 m (McKee et al., Reference McKee, Oriel, Ketner, MacLachlan, Goldsmith, MacLachlan and Mudge1959). Amphistegina is found in depths not exceeding 130 m (Hallock, Reference Hallock and Sen Gupta1999), but its main depth range is reported to be 5–20 m (Murray, Reference Murray1973).

The taphonomic and sedimentary signatures are consistent with a shallow-water setting with moderately energetic conditions, with sporadic high-energy events and related episodes of rapid sedimentation. Differences in the state of preservation between the spatangoid Agassizia and the clypeasteroid Clypeaster can be recognized. Agassizia remains occur almost exclusively as complete pristine tests, though lacking spines. By contrast, Clypeaster is present in a spectrum of preservation states ranging from well-preserved specimens to highly fragmented remains with evidence of encrustation and bioerosion. Multiple circular holes represent postmortem colonization by endolithic organisms.

During high-energy events, remnants of freshly dead spatangoids, as well as spatangoids living within their shallow burrows, could be scoured out and, after limited transport, be smothered by a thick layer of sediment. This led to excellent surface preservation on both complete tests and larger fragments. Agassizia remains lying on the surface for a prolonged time, being thin and fragile, were readily fragmented and destroyed. By contrast, Clypeaster specimens, with their thick and robust tests, experienced longer surface residence times and were exposed to biostratinomic processes, including fragmentation and bioinfestation. This resulted in the preservation of small, abraded, encrusted, and bioeroded fragments along with well-preserved, complete test remains. The accumulation of LBF, with densely packed complete and fragmented shells showing imbrication, is consistent with episodes of high-energy conditions.

The carbonate succession studied herein pertains to the lower portion of the thick sedimentary succession cropping out along the coast of the Montiferru area (see Mancosu and Nebelsick, Reference Mancosu and Nebelsick2019). The echinoid fauna represents somewhat shallower sublittoral environments than those described by Mancosu and Nebelsick (Reference Mancosu and Nebelsick2019), which are characterised by a more diversified echinoid fauna, including some spatangoid taxa, typical of the fine-grained facies of outer sublittoral environments.

Predation in spatangoid taphonomy and paleoecology

Drill holes on Agassizia tests are interpreted as the result of predation by cassid gastropods. The attribution is supported by the general shape and size of the bore holes and the well-documented gastropod–echinoid interactions as found in living populations of both regular and irregular echinoids, including spatangoids (e.g., Moore, Reference Moore1956; Hughes and Hughes, Reference Hughes and Hughes1971, Reference Hughes and Hughes1981; Hughes, Reference Hughes1986; Gerace and Lindsay, Reference Gerace, Lindsay and Gerace1992; Lindsay, Reference Lindsay, Elliott, Craig Edwards and Godfrey1996; Tewfik and Scheuer, Reference Tewfik and Scheuer2013; Grun, Reference Grun2017; Tyler et al., Reference Tyler, Dexter, Portell and Kowalewski2018).

Hughes (Reference Hughes1986) described in detail the hunting technique used by the cassid Galeodea echinophora (Linnaeus, Reference Linnaeus1758) to prey on the infaunal spatangoid Echinocardium cordatum. After detecting a buried urchin by olfaction, the gastropod attacks the infaunal prey, extending its proboscis down through the sediment. Although on some occasions the prey remains buried throughout the attack and is consumed entirely within the sediment, more often, an Echinocardium rises to the sediment surface by vigorously moving its spines and tube feet. The predator crawls upon its prey, engulfing the echinoid with its foot, partly removing the spines, and drilling into the test using its radula and sulfuric acid, whereby a circular puncture wound is produced. The remaining central disc is then pushed into the test's cavity to produce the bore hole. The gastropod extends its long proboscis throughout the interior of the test to consume the internal tissues (Hughes and Hughes, Reference Hughes and Hughes1981; Hughes, Reference Hughes1986). Cassids generally bore a single hole into the urchin test, although in some cases two or more gastropods attack the same urchin, either simultaneously or sequentially, thus producing several bore holes (Hughes, Reference Hughes1986). The cassids Cassis madagascariensis Lamarck, Reference Lamarck1822 and Semicassis granulata (Born, Reference Born1778) use a similar mode of attack while foraging for buried spatangoids (see Moore, Reference Moore1956; Hughes and Hughes, Reference Hughes and Hughes1981).

Statistical analyses performed herein indicate no evidence of size selection by predators. As discussed by Grun (Reference Grun2017), cassid predators rarely exhibit size preference, and where selection is present, a statistically distinguishable distribution of drilled and undrilled echinoid specimens is expected (Nebelsick and Kowalewski, Reference Nebelsick and Kowalewski1999).

Comparison of test length distributions between drilled (mean 16.83 mm; median 17.06 mm) and undrilled tests (mean 15.53 mm; median 15.12 mm) of Agassizia indicates a slight difference that is not statistically significant (t = 1.54; p = 0.12), suggesting that predators did not hunt a distinct size class of prey. Furthermore, as indicated by drill-hole dimensions, predator size is only weakly correlated with prey test size (r = 0.11; p = 0.49) (Fig. 8.6), indicating that distinct size ranges of cassid predators did not select for a specific prey size. Agassizia lived shallowly burrowed within the sediment and occurred in large numbers. It is thus likely that the cassid predator preyed upon randomly encountered echinoids.

In contrast to prey size, a clear drilling stereotypy is recognized, with the prey attacked mainly at the upper, aboral surface (74.28%) (Fig. 9.1). Handling by the predator in a preferred anterior–posterior orientation is, however, not present (Fig. 9.3). This is consistent with observations of the distribution of drill holes in the test of extant Echinocardium, as the holes are also found mainly on the aboral side of the test (Hughes, Reference Hughes1986).

Drilling predation by cassid gastropods may be an important factor influencing the preservation of spatangoid echinoid tests (see Tyler et al., Reference Tyler, Dexter, Portell and Kowalewski2018). Potential predation-related biases should be considered in estimating drilling frequency in relation to predation intensity and size and site selectivity. Cassid predators that prey on spatangoids within the sediment can enhance the preservation of the tests. In addition, cassids create an enlarged opening and remove internal soft tissue, including the peristomial and periproctal membranes, thus accelerating sediment infill and burial of the test (Tyler et al., Reference Tyler, Dexter, Portell and Kowalewski2018).

By contrast, if echinoid tests are weakened by drill holes, they would be more easily destroyed by mechanical, chemical, and biological processes, leading to the underestimation of drilling frequencies. In the case of Meoma ventricosa (Lamarck, Reference Lamarck1816), the high percentage of drilled tests (96.8%) suggests that drill holes did not weaken the test sufficiently to lead to preferential breakage of drilled specimens (Tyler et al., Reference Tyler, Dexter, Portell and Kowalewski2018). This was also observed by Nebelsick and Kowalewski (Reference Nebelsick and Kowalewski1999) for Echinocyamus and Fibularia from the Red Sea. Drilling predation may also introduce a size bias when large holes occur on small tests (Grun and Nebelsick, Reference Grun, Nebelsick, Zamora and Rabano2015), which are more easily destroyed, and when large predators destroy the test of a much smaller prey during the hunting process (Grun et al., Reference Grun, Sievers and Nebelsick2014).

The random orientation of complete, drilled tests of Agassizia, with respect to the bedding plane and their state of preservation, indicates that predated spatangoids suffered exhumation and limited reworking. The rapid infilling of small to medium tests by fine-grained sediments, that entered through the peristome and periproct as well as via the newly produced bore hole, after all internal soft tissues were fed upon by the gastropod predators, possibly enhanced the preservation potential. The subsequent overturning and redeposition by high-energy events and final burial under thick layers of sediment then led to the preservation of otherwise thin and fragile spatangoid tests.

Predation is considered one of the major selective forces in the evolution of morphological and behavioral characteristics in marine invertebrates, including species distributions, life habits, and population densities (Vermeij, Reference Vermeij1977; Bardhan and Chattopadhyay, Reference Bardhan and Chattopadhyay2003). Morphological innovations and diversification in spatangoids have been related to increasing predation pressure by cassid gastropods (Smith, Reference Smith1984; McNamara, Reference McNamara, David, Guille, Féral and Roux1994; Kanazawa, Reference Kanazawa, Heinzeller and Nebelsick2004, Reference Kanazawa, Reich, Reitner, Roden and Thuy2010; Saitoh and Kanazawa, Reference Saitoh and Kanazawa2019), which diversified during the Eocene (Farrar et al., Reference Farrar, Graves, Petsios, Portell, Grun, Kowalewski and Tyler2020; Petsios et al., Reference Petsios, Portell, Farrar, Tennakoon, Grun, Kowalewski and Tyler2021).

Cassids feed almost exclusively on echinoids (e.g., Hughes and Hughes, Reference Hughes and Hughes1971, Reference Hughes and Hughes1981; Tewfik, Reference Tewfik, Acosta and LeRoy Creshwell2014; Tyler et al., Reference Tyler, Dexter, Portell and Kowalewski2018), opportunistically preying on the locally most abundant species (see Tewfik and Scheuer, Reference Tewfik and Scheuer2013 and references therein) and exerting high predation pressures on echinoid populations (e.g., Gladfelter, Reference Gladfelter1978; Engstrom, Reference Engstrom1982; McClintock and Marion, Reference McClintock and Marion1993; Lindsay, Reference Lindsay, Elliott, Craig Edwards and Godfrey1996; Tyler et al., Reference Tyler, Dexter, Portell and Kowalewski2018).

Specialized morphology, increased size and test thickness, infaunalization, habitat selection, colonization of fine-grained sediments in both deeper-water settings and gravelly substrates in shallow unstable environments, and related functional and morphological adaptations are interpreted as antipredation strategies adopted by spatangoids (McKinney and McNamara, Reference McKinney and McNamara1991; McNamara, Reference McNamara, David, Guille, Féral and Roux1994; Kanazawa, Reference Kanazawa, Heinzeller and Nebelsick2004, Reference Kanazawa, Reich, Reitner, Roden and Thuy2010; Saitoh and Kanazawa, Reference Saitoh and Kanazawa2019).

An antipredator adaptation that depends on high-density populations is suggested for Agassizia. This echinoid does not appear to possess any specific morphological adaptations to minimize predation risk as it lacks the long and robust aboral defensive spines present, for example, in Lovenia elongata (Gray, Reference Gray and Eyre1845) and Plagiobrissus grandis (Lawrence and Ferber, Reference Lawrence and Ferber1971; Ferber and Lawrence, Reference Ferber and Lawrence1976; Hendler et al., Reference Hendler, Miller, Pawson and Porter1995). Agassizia also lacks the ability to burrow deeply into the sediment. A gregarious behavior for Agassizia is suggested by the high number of preserved tests. This potentially served to counter predation pressures on Agassizia populations by providing safety in numbers, thereby reducing the probability of lethal predatory attacks on each individual.

Safety in numbers, including the dilution effect of living in dense assemblages, is considered relevant in influencing the possibility of becoming prey, as the larger the group of prey animals, the lower the chance that any given individual will become prey (e.g., Foster and Treherne, Reference Foster and Treherne1981; Lehtonen and Jaatinen, Reference Lehtonen and Jaatinen2016). Defensive aggregating behavior in the regular sea urchins Strongylocentrotus and Echinometra reduces the intensity of predation by crabs, lobsters, and sea stars (Bernstein et al., Reference Bernstein, Schroeter and Mann1983; Morishita and Barreto, Reference Morishita and Barreto2011).