Bassi et al. Progress in Earth and Planetary Science
https://doi.org/10.1186/s40645-020-00356-w(2020) 7:41

Progress in Earth andPlanetary Science

RESEARCH ARTICLE

Open Access

Boring bivalve traces in modern reef anddeeper-water macroid and rhodolith beds
Davide Bassi1* , Juan C. Braga2, Masato Owada3, Julio Aguirre2, Jere H. Lipps4, Hideko Takayanagi5 andYasufumi Iryu5

Abstract
Macroids and rhodoliths, made by encrusting acervulinid foraminifera and coralline algae, are widely recognized as
bioengineers providing relatively stable microhabitats and increasing biodiversity for other species. Macroid andrhodolith beds occur in different depositional settings at various localities and bathymetries worldwide. Six casestudies of macroid/rhodolith beds from 0 to 117 m water depth in the Pacific Ocean (northern Central Ryukyu
Islands, French Polynesia), eastern Australia (Fraser Island, One Tree Reef, Lizard Island), and the Mediterranean Sea(southeastern Spain) show that nodules in the beds are perforated by small-sized boring bivalve traces(Gastrochaenolites). On average, boring bivalve shells (gastrochaenids and mytilids) are more slender and smaller thanthose living inside shallow-water rocky substrates. In the Pacific, Gastrochaena cuneiformis, Gastrochaena sp., Leiosolenus
malaccanus, L. mucronatus, L. spp., and Lithophaga/Leiosolenus sp., for the first time identified below 20 m water depth,
occur as juvenile forms along with rare small-sized adults. In deep-water macroids and rhodoliths the boring bivalves
are larger than the shallower counterparts in which growth of juveniles is probably restrained by higher overturn rates
of host nodules. In general, most boring bivalves are juveniles that grew faster than the acervulinid foraminiferal andcoralline red algal hosts and rarely reached the adult stage. As a consequence of phenotypic plasticity, small-sized
adults with slow growth rates coexist with juveniles. Below wave base macroids and rhodoliths had the highest
amounts of bioerosion, mainly produced by sponges and polychaete worms. These modern observations provide
bases for paleobiological inferences in fossil occurrences.
Keywords: Rhodoliths, Macroids, Bioerosion, Phenotypic plasticity, Bivalves, Pacific Ocean, Mediterranean Sea, Recent

1 Introduction
Macroids and rhodoliths form extensive beds in marine
waters from shallow subtidal and coral reef areas down
to outer platforms (e.g., Foster 2001; Amado-Filho et al.
2012; Foster et al. 2013). Macroids are coated grains, larger than 10 mm, made up of encrusting metazoans or
protozoans (Hottinger 1983). Coralline red algae aredominant components of free-living nodules which are
named rhodoliths (Bosellini and Ginsburg 1971). Macroids and rhodoliths form a habitat for many other organisms, from protists to fish and including boring bivalves* Correspondence: bsd@unife.it
1
Dipartimento di Fisica e Scienze della Terra, Università degli Studi di Ferrara,
Via Saragat 1, I-44122 Ferrara, Italy
Full list of author information is available at the end of the article

that inhabit the nodules themselves, and they contributeto the benthic primary productivity. The nodules canrecord the biodiversity of the inhabiting boring organisms (e.g., Littler et al. 1991; Foster 2001; Mallela andPerry 2007; Mueller et al. 2014; Adey et al. 2015). Modern nodules therefore can provide a basis for understanding activities of ancient bioeroding organisms inenvironments where they occur. This paper documents
the boring bivalves and their traces found in modern
macroids and rhodoliths at six sites, from shallow coral
reef to deep-water environments, in the Pacific Ocean
and Mediterranean Sea, down to depths of 117 m. This
provides a basis for the interpretation of fossil
occurrences.

© The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License,
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Bassi et al. Progress in Earth and Planetary Science(2020) 7:41

Fossil traces are evidence of the activity of once-livingorganisms, grouped in different ethological categories(Seilacher 1964; Ekdale et al. 1984; Bromley 1996). Theseborings (domichnia) include both bioturbation andbioerosion structures (Ekdale et al. 1984; Taylor andWilson 2003; Gibert et al. 2004). Bioerosion structures,widespread in carbonate stable substrates, are also common in mobile hard substrates represented by macroids
and rhodoliths (Bosence 1985; Matsuda and Iryu 2011;
Baarli et al. 2012).
Fossil traces have so far been useful tools in palaeoenvironmental analysis for two reasons: (a) they have good preservation potential, and (b) many individual ichnotaxa,
ichnocoenoses, and involved taphonomic signatures exhibit
reasonably well-constrained environmental distributions(Perry and Bertling 2000; Perry and Hepburn 2008;
Checconi et al. 2010; Bassi et al. 2013). However, mostknowledge regarding the environmental distribution of boring ichnotaxa and their producers comes from shallowwater coral reefs and rocky shores but little is known about
those from deeper settings (Kleemann 1980; Perry 1998;
Gibert et al. 2012; Perry et al. 2012; Aguirre et al. 2017a).
Common and abundant macroborer ichnospecies of
Gastrochaenolites Leymerie have been described fromintertidal rocky settings (e.g., Kelly and Bromley 1984;
Bromley and D’Alessandro 1987; Edinger and Risk 1994;
Wilson and Palmer 1998; Ekdale and Bromley 2001;
Donovan 2002; Kleemann 2009). Little is known about
boring gastrochaenids (Gastrochaenidae) and mytilids(Mytilidae) inhabiting macroids and rhodoliths in deeper
settings. These boring bivalves, both in organic and inorganic substrates, are exposed to different restrictions intheir growth (e.g., Owada 2015; Bagur et al. 2013, 2014;
Márquez et al. 2017). These restrictions are phenotypic
responses to the environmental conditions. Organismsthat grow in different environmental conditions may exhibit behavioral, morphological, ichnological, andphysiological differences (e.g., Hollander et al. 2006).
Gastrochaenolites ichno-specimens and related preserved boring bivalves are analyzed in present-day shallow- to deep-water macroids and rhodoliths. Six examplesof macroid and rhodolith beds from 0 to 117 m water
depth in the Pacific Ocean and the Mediterranean Sea
were studied (Table 1): southern Japan (northern Central

Page 2 of 17

Ryukyu Islands), eastern Australia (Fraser Island, One
Tree Reef, Lizard Island), French Polynesia (Moorea), andsoutheastern Spain (Cabo de Gata). We compare the bivalve borings and their makers and the growth and taphonomic characteristics of the macroids and rhodoliths inorder to decipher the complex interplay between the boring bivalves and their host. Shell-shape diversity of theidentified boring bivalves, together with morphological diversity of the ichnospecimens and taphonomic observations, indicate that (1) the mean shell sizes of the boringbivalves are slenderer and smaller than those growing inside shallow-water rocky substrates, and (2) deep-water (>40 m) boring bivalves grow faster than their hosts. As aconsequence of phenotypic plasticity, small-sized adults
with slow growth rates might coexist with juveniles.

2 Geographical settings
2.1 Southern Japan: Kikai-jima

This survey area lies southwest of Kikai-jima (Central
Ryukyu Islands; Table 1) at water depths between 61
and 105 m in clear oceanic waters with normal marine
salinities (34–35). The sea floor is characterized by flat
topography and mainly consists of coarse bioclastic carbonate sediments (Arai et al. 2008). Mean seawater annual temperature is ~ 22–24 °C (data from J-DOSS,JODC Data On-line Service System).
Macroids for this study were dredged from the flat sea
floor (Bassi et al. 2012a) during a scientific survey cruise
carried out by R/V Tansei-maru (KT-09-16, Ocean Research Institute, The University of Tokyo). The nodules
consist of various sized macroids, which had been
formerly called rhodoliths in the studies of marine sediments and biota around the Ryukyu Islands (Tsuji 1993;
Matsuda and Nohara 1994; Iryu et al. 1995). The macroids examined were still living when collected. They were
washed and dried before subsequent analysis. Detailed
descriptions of the macroid size and shape are reported
in Bassi et al. (2012a).
2.2 Eastern Australia: Fraser Island, one tree reef, Lizard
IslandThe samples were collected in 1991 on the continental
shelf off Fraser Island in southern Queensland, south of
the Great Barrier Reef (Table 1), during a joint survey

Table 1 Geographic co-ordinates and bathymetric ranges of the sampled areas
Location

LatitudeLongitude

Bathymetric range (m)Kikai-jima

28° 14′ N

129° 50′ E

61–105Fraser Island

24° 50′ S/25° 20′ S

153° 20′/153° 40′ E

28–117

One Tree Reef

23° 30′ S

152° 06′ E< 0.3

Lizard Island

14° 39′ S

145° 27′ E

0.5–12

Moorea17° 29′ S

149° 54′ W

0–30

Cabo de Gata

36° 55′ N

1° 57′ W

2.5–50Bassi et al. Progress in Earth and Planetary Science(2020) 7:41

cruise of the Australian Geological Survey Organization(AGSO) and Japanese National Oil Corporation (JNOC).
This area is at the transition from tropical to temperate
carbonate deposition (e.g., Marshall et al. 1998; Boydet al. 2008; Schröder-Adams et al. 2008).
Offshore Fraser Island algal nodules are common in
the rhodolith-coral gravelly facies in the mid-shelf (~45–100 m) water depths and their abundance decreases
both to the outer shelf down to 120 m and to the sandy
inner shelf (Marshall et al. 1998; Lund et al. 2000; Fig.
2). Rhodoliths were picked from 31 dredged and grabbed
samples along the surveyed depth range.
One Tree Reef is one of the coral reefs in the Capricorn Group in the southern Great Barrier Reef Province(Davies et al. 1976; Table 1). This is a mesotidal region(average tidal range in One Tree Reef is 1.5 m) with predominant southeasterlies (Choukroun et al. 2010). The
studied rhodoliths in One Tree Reef extend in the intertidal to shallow subtidal zones of the coralgal rim at theleeward side of the reef. The samples were collected inless than 0.3 m below mean low sea level in October
1992.
Lizard Island is a group of five small granite islands
surrounded by coral reefs in the northern Great Barrier
Reef (Table 1). Rhodoliths were sampled from shallow
subtidal (0.5 to 12 m water depth) sites in the fringing
reefs from both eastern and western sides by snorkelingand scuba diving in November 1992.
2.3 French Polynesia: Moorea

Moorea, the second youngest volcanic island (~ 1.2 to 2Ma) within the Society Islands (Table 1), is located 20
km west of Tahiti, has a barrier coral reef intersected bypasses, which separate a lagoon from the open ocean(Fajemila et al. 2015, 2020). Water circulation is winddriven swells that break on the barrier and force mostly
unidirectional water into the lagoon from where it thenexits through the reef passes (Hench et al. 2008).
Rhodoliths occur in various sites around the island.
The rhodoliths used in this study were collected on
northwestern Moorea from a carbonate sand in ashallow-water (less than 2 m) channel. This channel separates two motus (shallow islands) at the edge of the lagoon adjacent to the western shore of Motu Tiahura(Table 1). Current speed is up to 6.8 m/s in the samplingsite most distant from the motu shore. The rhodolith
bed’s extent is greater than 150 × 30 m parallel to Motu
Tiahura, with rhodoliths usually separated from one another by a few centimeters to a meter.
2.4 Southeastern Spain: Cabo de Gata

The sampled rhodolith beds occur at Rocas del Plomo off
Cala del Plomo in Cabo de Gata (Almería, southeastern
Spain; Table 1). The rhodoliths mainly grow on bioclastic

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gravels around volcanic rocks jutting out on the shelf between 2.5 and 50 m water depth. Shorewards of rhodolith
beds the sediment is siliciclastic sand with bioclasts while
seawards the gravels change to bioclastic muddy sand withdispersed open branching rhodoliths. Waters are oligotrophic to mesotrophic and rhodoliths are only sporadically affected by storm waves. Rhodoliths were collected by
dredging from a small boat (AMA 7, Junta de Andalucía)
and scuba diving from 2002 to 2004.

3 Methods/experimental
Macroid and rhodolith shapes were assessed as sphericity index (see Sneed and Folk, 1958; Graham andMidglay 2000) by measuring the short, intermediate, andlong axes of each specimen (e.g., Bosence 1983a). Taxonomic composition, nature of the nucleus, inner arrangement, and constructional voids, and outer growthforms (e.g., Bassi et al. 2012b; Aguirre et al. 2017b) wereanalyzed on polished slabs and in thin sections (n = 300,
~ 10 μm in thickness). The thin sections were made after
embedding the macroid and rhodolith specimens inepoxy resin in a vacuum chamber. The embedded specimens were sectioned along the plane including the center of the specimen. The identified ichnogenera are
based on descriptions and illustrations of Bromley andD’Alessandro (1983, 1984, 1989), Kelly and Bromley(1984), Edinger and Risk (1997), and Perry (1996). The
ichnotaxa identified in the Kikai-jima and Fraser Island
beds have been described and illustrated in Bassi et al.
(2011, 2012a). The abundance of bioerosion traces wassemi-quantitatively estimated using a binocular microscope (Nebelsick et al. 2011). Boring bivalves were identified according to shell shapes and microstructures ofisolated specimens collected from nodules (Owada andHoeksema 2011). Shell microstructures were observed
under scanning electron microscope JEOL JCM-5000
with an accelerating voltage of 15 kV (Department of
Biological Sciences, Kanagawa University; Owada 2009;
Owada and Hoeksema 2011). Bivalve length and height
were assessed along and across the nearly straight ligament, which is the axis of shell opening. These measurements along with the boring traces were evaluated witha digital vernier caliper. The length of the Gastrochaenolites chamber was determined by measuring a very thiniron wire inserted in the burrow.
In macroids and rhodoliths, bioeroding organisms operating with chemical or physical processes destroy the
inner nodule structure. The bioerosion index (BI) is an
estimation of the degree of bioerosion which ranges
from no bioerosion (BI 1) to complete bioerosion (BI 6;
undistinguishable arrangement of the inner coated grain;
Bassi et al. 2012a). The BI was assessed on macroid
polished slabs. BI is similar to the bioturbation index
which estimates the percentages of restructuring inBassi et al. Progress in Earth and Planetary Science(2020) 7:41

clastic- or limey-bedded sedimentary deposits by organisms (Taylor and Goldring 1993).
The studied material from Kikai-jima and Fraser Island
is deposited at the Institute of Geology and Paleontology,
Graduate School of Science, Tohoku University, while
additional material from Fraser Island, and samples fromOne Tree Reef/Lizard Island, Moorea, and southeastern
Spain are stored at the Departamento de Paleontología yEstratigrafía, Universidad de Granada, Spain. Additional
material from Moorea is stored in the Museum ofPaleontology, University of California. Isolated boring bivalve specimens are housed at the Department of Biological Sciences, Faculty of Science, Kanagawa University.

4 Results and discussion
4.1 Macroid and rhodolith beds

The samples collected in Kikai-jima consist of macroids
with minimum and maximum diameters respectively 2.0
cm and 10.4 cm in size (n = 75, mean 6.4 cm, standard
deviation s.d. ± 2.0 cm). Macroids from a single locality
significantly vary in size from ~ 1.2 cm to 13 cm. Coalescentmacroids can be up to 15 cm in size. Spheroidal and subspheroidal shapes dominate the studied samples (Fig. 1).
Samples from 61–71 m water depth show rare subdiscoidal shapes. Inner macroid arrangement consists ofPage 4 of 17

concentrically, commonly asymmetrical, laminated, andsuperimposed Acervulina inhaerens tests associated withsubordinate coralline thalli, serpulids, and bryozoans, andhigh volumes of constructional voids. Encrusting arborescent foraminifera, such as Homotrema and Miniacina, arealso present. The macroid surface shows dominant encrusting foraminifera together with common to rare warty andrare lumpy thin (< 1 mm thick) coralline thalli (Lithothamnion sp., melobesioid indet.; Bassi et al. 2011).
Off Fraser Island in shallow-water settings between 28
and 60 m, rhodoliths comprise algal-coated pebbles andrhodoliths while only rhodoliths were found in deeper settings (> 60 m; see details in Lund et al. 2000). Algal-coatedpebbles, up to 9 cm in diameter, range from spheroidal toellipsoidal to discoidal, with a low percentage of constructional voids. Rhodoliths show a maximum diameter of 4.6
cm and the shape ranges from spheroidal to ellipsoidal,
discoidal, and very discoidal (n = 76; Fig. 1). In shallower
rhodoliths, melobesioids dominate with subordinate lithophylloids and other corallinaceans, sporolithaceans, andpeyssonnelliaceans. Deeper rhodoliths, ranging from ~ 2
to 5 cm in maximum diameter (n = 22), are composed ofdominating sporolithaceans, melobesioids, and peyssonneliaceans (Lund et al. 2000). Rhodoliths show a high percentage of constructional voids.

Fig. 1 Macroid and rhodolith sphericity in the studied beds from Kikai-jima, Fraser Island, One Tree Reef/Lizard Island, Moorea, and Cabo de Gata.
The sampled bathymetric range of the studied beds is also reported (colored depth intervals). No variation in sphericity with increasing depth
is observed

Bassi et al. Progress in Earth and Planetary Science(2020) 7:41

One Tree Reef/Lizard Island rhodoliths, up to 15 cm indiameter (with mean, minimum, and maximum diametersrespectively 4.6 cm (n = 7, s.d. ± 1.1 cm), 3 cm, and 6.3 cm
in size), consist of coralline algae around coral fragments.
The coral nuclei are usually larger than the algal cover,which comprises thick encrusting, lumpy to fruticose thalliof Porolithon gr. P. onkodes (Heydrich) Foslie, Hydrolithonboergesenii (Foslie) Foslie, and various minor amounts of
Lithophyllum gr. L. kotschyanum Unger, Lithophyllum gr.
L. pustulatum (Lamouroux) Foslie, Spongites sp., andNeogoniolithon sp. (Figs. 2 and 3).
The Moorea rhodoliths, ranging in size from 2.7 to
9.2 cm (n = 29, mean 4.5 cm, s.d. ± 1.3 cm), have a wide
variety of shapes (Fig. 1). They typically consist of several
thick coralline algal thalli encrusting coral fragments(Fig. 4). In many cases, the coral nucleus is larger than
the algal covering and controls the nodule shape. Other
rhodoliths are mainly made up of coralline algae and are
sub-spheroidal to sub-discoidal/sub-ellipsoidal in shape,with a low constructional void percentage. Coralline
growth forms tend to be encrusting in the inner part of
the algal covering and pass outwards to warty/lumpy
and fruticose. Thick encrusting to lumpy thalli of Porolithon gr. P. onkodes (Heydrich) Foslie are the most common components, followed by branching growths of
Neogoniolithon sp. and Lithophyllum gr. L. kotschyanum
Unger. Hydrolithon boergesenii (Foslie) Foslie and Lithophyllum gr. L. prototypum (Foslie) Foslie also occur as
minor elements.

Page 5 of 17

Rhodoliths in southeastern Spain are mainly fruticose
and boxwork structures (from 2.3 to 4.9 cm in size,
mean 3.3 cm, s.d. ± 0.7 cm, n = 18; Fig. 1), developedaround relatively small bioclastic nuclei (Figs. 5 and 6).
Monospecific fruticose rhodoliths can be formed by
Lithophylllum gr. L. racemus (Lamarck) Foslie, Phymatolithon gr. P. calcareum (Pallas) Adey and McKibbin,
Lithothamnion valens Foslie, Lithothamnion minervae
Basso, Lithothamnion gr. L. corallioides (Crouan andCrouan) Crouan and Crouan, and Spongites fruticulosus
Kützing. Complex, multispecific rhodoliths with boxwork structure can include combinations of any of these
species and other Lithophyllum, Lithothamnion, Mesophyllum, Phymatolithon, and Sporolithon species, as well
as Peyssonneliacean algae. Below 40 m they are mainly
small loose-branching rhodoliths made of L. gr. L. corallioides and P. gr. P. calcareum.
4.2 Distribution and relative abundance of the ichnotaxa

Five ichnogenera were identified: Entobia Bronn, Gastrochaenolites Leymarie, Trypanites Mägdefrau, Maeandropolydora Voigt, and Rogerella de Saint-Seine, the latterpresent only off Fraser Island. Trypanites/Maeandropolydora is used when distinguishing ichnocharacters are
not preserved. Micro-endolithic traces also occur. The
borings often match exactly the shape of the boring
endolithic invertebrate (Fig. 6), although similar borings
are sometimes produced by different organisms. The
bioerosion structures are distributed in two tiers relative

Fig. 2 Outer rhodolith surfaces from intertidal and shallow subtidal settings in One Tree Reef and Lizard Island showing the range in size andgrowth forms (en, encrusting; w, warty)Bassi et al. Progress in Earth and Planetary Science(2020) 7:41

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Fig. 3 Slab surfaces of One Tree Reef and Lizard Island rhodoliths showing the bioerosion traces. Note the growth break between the bioeroded
nucleus (bn) and the fruticose/lumpy stage (fr, lu). E, Entobia; G, Gastrochaenolites; T, Trypanites

to the substrate surface: shallow and deep. All the ichnotaxa occur as rare to abundant (Fig. 7).
In the studied sites, the bioerosion index (BI) ranges
from 1 to 4, being higher in the deeper water settings(Fig. 7). The shallowest studied rhodoliths show BI 1
(i.e., One Tree Reef/Lizard Island, Moorea; Fig. 7). From
~ 3 to ~ 10 m water depth, rhodoliths have a BI of 1
with a single case of B2 in Cabo de Gata. Below 10 m to
60–70 m water depth, macroids and rhodoliths show BI
2 (Kikai-jima, Fraser Island, Cabo de Gata). BI 3 wasrecognized in macroids and rhodoliths down to ~ 115 m(Kikai-jima, Fraser Island), with locally BI 4 in the deepest samples (below 90 m).
4.3 Gastrochaenolites: size, location, and boring bivalves

In general, the identified Gastrochaenolites specimens are
3.5–16.7 mm in length. Length of Gastrochaenolites ichnospecimens shows a significant correlation with bathymetry (correlation coefficient R = 0.44, p < 0.001; Fig. 8a).
On the other hand, a very weak but statistically significant

Fig. 4 Slab surfaces of Moorea algal nodules (< ~ 2 m water depth) showing encrusting (en) and fruticose (fr) coralline growth forms and theboring bivalve traces (G, Gastrochaenolites). Within the algal nodules, serpulids and encrusting/arborescent foraminifera (min, Miniacina; hr,
Homotrema) are present. Note that most of the nodules consist of coral fragments

Bassi et al. Progress in Earth and Planetary Science(2020) 7:41

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Fig. 5 Slab surfaces of rhodoliths from Cabo de Gata showing complex boring patterns and bioerosion traces from 24.5, 30, 40, and 50 m water
depth. Symbol points out the split rhodoliths (see Fig. 6). E, Entobia; G, Gastrochaenolites; en, encrusting; lu, lumpy; fr, fruticose; bn,
bioeroded nucleus

correlation (R = 0.16, p < 0.05) was observed between
macroid/rhodolith size and depth (Fig. 8b). There is no
significant correlation between macroid/rhodolith size andGastrochaenolites length (R = 0.06, p > 0.05).
In our samples, remains of the bivalve producers of
Gastrochaenolites may still be found in situ inside mostof the related perforations. However, some boring bivalves
do not preserve enough diagnostic shell characters for
species determination. The identified boring bivalves belong to four genera (Gastrochaena, Gregariella, Leiosolenus, Lithophaga) and eleven species (Table 2). Whendiagnostic shell characters for distinguishing the genera

Fig. 6 Slab surfaces of two splitted rhodoliths showing their inner arrangement and the trace fossils; Cabo de Gata. Each rhodolith was cut in
two parts through its center. Note that the Gastrochaenolites specimen (G; comparable to G. lapidicus Kelly and Bromley; dashed lines) stillcontains its producer boring bivalve (Gastrochaena sp.), which grew in encrusting (en) and lumpy (lu) coralline growth forms. The rhodolith shapeis not influenced by the boring-bivalve shapeBassi et al. Progress in Earth and Planetary Science(2020) 7:41

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Fig. 7 Distribution of the ichnogenera, their relative abundance in the studied areas, and the bioerosion index (BI). The distribution of samples isplotted according the different sampling methods (see text for details). The sampled bathymetric range of the studied beds is also reported(depth intervals are dark gray for macroids and gray for rhodoliths). E, Entobia; G, Gastrochaenolites; T, Trypanites; T/M, Trypanites/
Maeandropolydora; R, Rogerella; r, rare; c, common; a, abundant

Leiosolenus and Lithophaga (family Mytilidae) are not preserved, Lithophaga/Leiosolenus sp. is used. The bivalves
are represented by adults of small sizes and juveniles withapproximately the same size ranges of the small
adults. Juveniles and adults were distinguished according to the size ranges reported in literature as well ascomparing the growth increments marked by thegrowth lines (Carter 1978; Savazzi 1999; Carter et al.
2008; Owada and Hoeksema 2011).
In Kikai-jima, Gastrochaenolites commonly occurs in
the outer parts of the larger macroids, but below 85 m
water depth Gastrochaenolites occur both in the innerand outer parts. Boring bivalves, represented by juvenile

specimens of Lithophaga spp. and Lithophaga/Leiosolenus sp. (Table 2, Fig. 9), are chemical borers (e.g.,
Savazzi 1999). These macroids are subspheroidal inshape and about 8 cm in diameter.
Off Fraser Island Gastrochaenolites generally occurs
perpendicular to the rhodoliths’ outer surface. They canalso occur just beneath or some millimeters below the surface where they are overlain by encrusting coralline algal
thalli (Fig. 10). This ichnotaxon does not occur in rhodoliths smaller than 3 cm; rare boring bivalves were preservedin the holes. In the shallower water rhodoliths (see Bassi
et al. 2013), the identified boring bivalves are juvenile individuals of Gastrochaena cuneiformis Spengler, Leiosolenus

Bassi et al. Progress in Earth and Planetary Science(2020) 7:41

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Fig. 8 Plots of (a) length of Gastrochaenolites ichnospecimens and water depth (R = 0.44, p = 0.001, total n = 57; Fraser Island n = 21; Kikai-jima, n= 11; Cabo de Gata, n = 12; Moorea, no = 7; One Tree Reef/Lizard Island, n = 6), (b) Macroid and rhodolith sizes and water depth (R = 0.16, p =0.0145, n = 234) from the six study cases. The sampled bathymetric ranges of the studied beds are also reported for each studied locality (verticalbars). OTR/LI, One Tree Reef/Lizard Island

Table 2 Distribution of the identified gastrochaenid (g, Gastrochaenidae) and mytilid (m, Mytilidae) bivalve taxa in the studied
macroid and rhodolith beds
Kikai-jima
Depth (m)74–76.5

Fraser Island
43

54

Gastrochaena cuneiformis (g)75–96.9

100–105.3

43

X

X

Gastrochaena cf. turbinatus (g)

X

60

92

< 10

30–40

X

Gregariella petagnae (m)XLei. malaccanus (m)XLei. mucronatus (m)

X
X

X
X

Leiosolenus sp. (m)X

Lith./Lei. sp. (m)X

Lithophaga sp. (m)Lithophaga sp. (m)Cabo de Gata

X (rare)Gastrochaena sp. (g)Leiosolenus sp. (m)OTR/LI, Moorea

X
X

OTR One Tree Reef; LI Lizard Island; Lei. Leiosolenus; Lith. Lithophaga

XBassi et al. Progress in Earth and Planetary Science(2020) 7:41

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Fig. 9 Boring mytilid bivalves from deep-water macroids off Kikai-jima, Japan. a Leiosolenus sp., inner and outer shell surface. b, c SEM photos
illustrating shell microstructures of Lithophaga sp. (b) and Leiosolenus sp. (c). HO, homogeneous structure; SN, sheet nacreous; ISP, irregular simple
prisms; ISpP, irregular spherulitic prisms

malaccanus (Reeve), L. mucronatus (Philippi), and Leiosolenus spp. Leiosolenus malaccanus (up to 2.5 cm in length)and L. mucronatus (up to 1.2 cm in length) also occur asadults. The boring bivalves Lithophaga/Leiosolenus sp. and
Lithophaga sp. were identified in the deep-water rhodoliths(Table 2).
In the shallow-water One Tree Reef, Lizard Island, andMoorea rhodoliths, Gastrochaenolites is rare to common. Very small ovate main chambers with a very longneck region, circular in cross section throughout, occur

in the rhodolith nuclei (generally a coral fragment), andthe long necks (tubes) reach up to the last growth stage
constructed by coralline thalli (Figs. 4, 5, and 6). These
ichnospecimens show similarities to G. turbinatus Kelly
and Bromley, 1984. No boring bivalves were foundwithin the traces (compare with Kleemann 1995).
Gastrochaenolites was recognized throughout the Cabode Gata rhodolith beds being abundant at 30 to 40 m
water depth. Some ichnospecimens show smooth, elongate ovate chambers circular in cross section with a

Fig. 10 Thin section photomicrographs showing Gastrochaenolites (G), Trypanites (T), and Trypanites/Maeandropolydora (T/M) in rhodoliths off Fraser Island.
a Cylindrical tubes of Trypanites bore successive coralline thallial growth increments. b Encrusting coralline thallus (arrow) overlying Gastrochaenolites

Bassi et al. Progress in Earth and Planetary Science(2020) 7:41

distinct neck region (Figs. 5 and 6). These characteristicsof the ichnospecimens are comparable to G. lapidicus
Kelly and Bromley, 1984. Gastrochaenolites specimens
commonly contain the producing boring bivalves, which
are Gregariella petagnae (Scacchi), possible juvenile
forms, and Gastrochaena sp. The studied specimensshow keel shells in shape (~ 7 mm in length), hairs on
the shell surface, and prominent dysodont teeth in theanterior and posterior margins. These characters are
considered diagnostic of Griegariella petagnae (Huber,2010). The siphons of large boring Gastrochaena sp. canbe encrusted by very thin coralline thalli (Fig. 6). The
shape of a rhodolith with a bivalve boring in the nucleus
is not influenced by the boring-bivalve shape (Figs. 5
and 6).
4.4 Ecological evidence and constraints in
Gastrochaenolites bathymetric distribution

In the studied macroids and rhodoliths, the occurrenceof boring bivalves and related traces (Gastrochaenolites)
is constrained by their ecology. These constraints, ranging from the relationship with other boring andencrusting organisms (i.e., associated ichnotaxa andbioerosion index BI) through the sizes of the bivalves
and the host (i.e., macroids and rhodoliths) to the natureand stability of the substrate, can be assessed even infossil material.
In our samples, Gastrochaenolites is rarely affected byother traces if it kept up with the growth of the outernodule surface (Moorea, Cabo de Gata; Figs. 4 and 5).
By contrast, if Gastrochaenolites is buried in the nodule,
its last and upper part can be perforated by other borings (Kikai-jima, fig. 6 in Bassi et al. 2012a; One Tree
Reef/Lizard Island, Fig. 3). Gastrochaenolites producers,
when still alive, therefore, do not have any active competitor for space (e.g., Carter 1978).
In the settings above 10 m water depth, Gastrochaenolites is rare to common (e.g., One Tree Reef/Lizard Island, Moorea) and becomes abundant along with
Entobia below 20 m (Cabo de Gata) and 30 m water
depth (Fraser Island; Fig. 7). Our studied cases show thatthe bioerosion increases below ~ 40 m water depth as
evidenced by the BI. High BI (i.e., 3–4) at 40–50 m water
depth in the Cabo de Gata rhodoliths and below 60 m
water depth in the Kikai-jima macroids and Fraser Island
rhodoliths (Fig. 7) indicate high bioerosion intensity, related to a lower macroid and rhodolith growth rate andto long-lasting exposure on the sea floor. Influence ofhigh boring speed and population density cannot be
ruled out as bioerosion factors. On the Brazilian shelf inhigh nutrient settings, delayed burial favors intense boring of rhodoliths (Brasileiro et al. 2018). In high-energy
intertidal and reef-crest/shallow reef-front settings,
macroboring assemblages are typically dominated byPage 11 of 17

sponges while boring bivalves decrease below ~ 30 m
water depth (e.g., Perry 1998; Perry and Hepburn 2008).
The recorded Gastrochaenolites specimens show a significant correlation between chamber-length and bathymetry (Fig. 8a). The largest specimens occur in Kikaijima macroids (> 60 m), while the smallest specimens
were recorded in Moorea, One Tree Reef, and Fraser Island rhodoliths. In Cabo de Gata and Fraser Island rhodoliths (< 60 m), large and small individuals occur
throughout. Very weak but statistically significant correlation occurs between nodule size and water depth. However, the absence of correlation between nodule size andGastrochaenolites length suggests that stability of thenodules rather than their size favors boring bivalve
growth.
Boring bivalves need a relatively stable substrate withcurrents to avoid burial. Above the fair-weather wave
base, the overturn rate of the rhodoliths constrains thegrowth of the boring bivalves which, then, may not reachthe adult stage. In the deeper settings, the higher stability of the macroids and rhodoliths, which only occasionally overturn (e.g., Matsuda and Iryu 2011; Bassi et al.
2012a, 2013), allows the juvenile boring bivalves tothrive longer. The absence of correlation between the
nodule size and Gastrochaenolites length confirms that
nodule size does not affect boring bivalve colonizationand growth (e.g., Fig. 6; Fig. 6, Bassi et al. 2012a; Fig. 5aand 5c, Bassi et al. 2013).
The average shell sizes of boring bivalve individuals in
the macroids and rhodoliths are slenderer and smaller
than those growing inside rocky substrates. All our Gastrochaenolites specimens are at least ten times smaller
than the known Gastrochaenolites spp. (Kelly and Bromley 1984; Donovan 2002, 2013; Donovan and Hensley
2006; Santos et al. 2011; Donovan et al. 2014; Silva et al.
2019). This is clear for G. lapidicus identified in the
Spanish rhodoliths collected at 30–40 m water depth(Fig. 6). This ichnospecies has also been identified so far
in clasts and cobbles from palaeoshores (Santos et al.
2011; Donovan 2013). The largest boring bivalves up to~ 85 mm long producing large Gastrochaenolites were
described in shallow-water rocky substrates (Santos et al.
2011; Bagur et al. 2016; Somaya et al. 2018). Although inlarger bivalves and corals Gastrochaenolites spp. show
large sizes (Perry 1998, 2000; Blanchon and Perry 2004;
Domènech et al. 2014), they are much smaller than theichnospecimens found in rocky substrates (Cachão et al.
2011). Different types of substrates generate different restrictions on the growth of Leiosolenus patagonicus individuals (as Lithophaga patagonica in Bagur et al. 2013).
Boring bivalves in larger ostreid shells cause an increase of
the metabolic energy costs to the host which produces
extra conchiolin to seal off the holes (Diez et al. 2014).
Leiosolenus patagonicus changes its phenotype depending

Bassi et al. Progress in Earth and Planetary Science(2020) 7:41

on the oyster’s anti-parasitism responses by physical compression (Márquez et al. 2017). The chemical inducement
or deterrent of acervulinid and coralline species to boringbivalve settlement is unknown.
According to these ecological constraints related to
the nature and stability of the substrate, the boring bivalves and especially their traces (i.e., Gastrochaenolites)
are more likely to be preserved and, hence, are usefulproxies in palaeoecological studies. The distinction of
Gastrochaenolites ichnospecies is based on the chambershape and the occurrence of one or two tubes in theneck region (Bromley and D’Alessandro 1987; Donovan
2013; Bassi et al. 2017). Because the bored substrate nolonger represents a possible diagnostic character of theichnogenus (Donovan and Ewin 2018), the ichnotaxonomy of Gastrochaenolites ichnospecies needs a reassessment which would provide hints to decipher theboring bivalve palaeobiodiversity in common fossil
macroid and rhodolith deposits.
4.5 Boring bivalves and growth rates

The identified boring gastrochaenid and mytilid species
are commonly found at depths shallower than 20 m
(Carter et al. 2008; Owada and Hoeksema 2011; Printrakoon et al. 2016). In our samples, they also occur deeper
than 40 m (Table 2). In particular, Lithophaga spp. andLeiosolenus spp. identified in the Kikai-jima macroids (>75 m) are the deepest-living boring mytilids reported sofar. Adult gastrochaenids and mytilids boring deep-water
macroids and rhodoliths are smaller than their shallowwater counterparts in rocky-shelly substrates as a phenotypic response to size and substrate stability. Lithophaga
and Leiosolenus are monophyletic genera (Owada 2007),
whose species show shell shapes that vary according to
the different thickness of the substrate (Owada 2015).
These variations appear to be an ecophenotypic response
to substrate thickness, although a genetic component ispossible based on the separation of species by depth.
Genetic studies of these species’ populations, however,
have not yet been done. Another alternative hypothesisis that food supply could be a factor in bivalve size.
While the small size of the shallowest (< 10 m; Lizard
Island, One Tree Reef, Moorea) boring bivalves can be
related to nutrient depletion in coral reefs, no oligotrophic conditions prevail in the rest of sampling sites,
and, therefore, nutrient availability does not seem to bea major controlling factor on boring-bivalve size. For the
moment, we accept the first hypothesis of ecophenotypic
response to be most likely pending further information.
The small Gastrochaenolites ichnospecimens represent
both juvenile boring bivalves that could not reach theadult stage and young adults (Fig. 11). Most of the identified boring bivalves were, in fact, live juveniles ofchemical borers (Kikai-jima, Fraser Island, Cabo de Gata;

Page 12 of 17

Table 2). These juveniles likely start boring after reaching ~ 1.5 mm in length, like shallow-water juveniles ofBarnea manilensis (e.g., < 5 m, Ito 1999). The identified
adults are very small in size compared with the shallowwater counterparts in rocky shelly substrates (Kleemann1984). While the adults of Leiosolenus mucronatus arerather smaller than those of the other species even inshallow-water settings (Kleeman and Maestrati 2012),
the ones of identified Lithophaga spp. are very small insize compared with the shallow-water counterparts inrocky shelly substrates (Kleeman 1984). Comparing thelength of the studied Gastrochaenolites with the previously reported length to growth-rate ratio of gastrochaenid and mytilid boring bivalves (Carter 1978; Bagur et al.
2013; Peharda et al. 2015), our ichnospecimens are likely
to be only up to a few years in age or small-sized adults.
The small-sized adults grew obviously with slower
growth rate than the shallower counterparts. The adaptation to the substrate (macroids and rhodoliths) constrained the bivalve growth rate or, vice versa, thebivalve grew slower to adapt to the substrate.
Gastrochaenids and mytilids perform different chemical boring activity. Adapted to live in rapidly erodedand broken coral margins, gastrochaenids can impede orescape coral overgrowth by elongating their siphonalburrow (Carter 1978). The siphons are especially extensible and retractable, thereby enabling the organism tosurvive coral overgrowth or erosion. A similar strategy
seems to be performed by some boring bivalves inhabiting macroids and rhodoliths (e.g., Gastrochaena sp. in
Cabo de Gata; Fig. 6). The Mytilidae, such as Gregariella, Leiosolenus, and Lithophaga, do not possess siphons (Savazzi 1999).
When the host substrate is fouled by epibionts orovergrows the opening of the borehole, these bivalves
react by boring backward (Savazzi 1999). This backward
migration can be interrupted if the host growing rate isslower than the boring bivalve rate or if macroids andrhodoliths are moved or overturned, as is likely in thestudied case. Because macroids and rhodoliths do notconstantly grow (e.g., Matsuda and Iryu 2011), the juveniles colonized the host surfaces and grew until a subsequent turning or burial of the host. The turning or
burial commonly result in the death of the bivalves.
As in large bivalve shells and corals (Perry and Hepburn 2008; Bagur et al. 2014), boring mytilids colonize
both living and dead macroids and rhodoliths. However,since these bivalves do not elongate their siphonal burrow and they need protection during their growth, bivalves in dead/inactive macroids and rhodoliths may bekilled in a few years. In this case, the preservation of thebivalve shell inside their traces is very rare.
Deep-water (> 20 m) boring bivalve growth rates are
unknown. Shallow-water boring bivalves show highBassi et al. Progress in Earth and Planetary Science(2020) 7:41

Page 13 of 17

Fig. 11 Schematic summary of development and preservation of bivalve borings (Gastrochaenolites) in deep-water macroids and rhodoliths. a
The juvenile bivalve growth rate is as rapid as the encrusting foraminiferal and coralline red algal growth rate. b In young bivalves, growth rate ishigher than the host’s rate; these individuals cannot be embedded by the host and, therefore, die. c No adults are preserved unless phenotypic
plasticity promoted small individuals. General growth curve of age-at-length boring bivalves after Bagur et al. (2013) and Peharda et al. (2015)

variations in growth rates among individuals, during different seasons and with different substrate hardness(Peharda et al. 2015; Bagur et al. 2013; Wizemann et al.
2018). Longevity and growth vary among Lithophaga
species, which thrive in hard carbonate substrates. In
Lithophaga lithophaga living at less than 3 m water
depth in Croatia, ontogenetic ages of shells varied from10 to 54 years with a growth rate ranging from ~ 3.3mm/year (for individuals 10 years old, the youngest one
analyzed in the study) to ~ 1.7 mm/year (50 years old;Peharda et al. 2015). In southwest Argentina, intertidal
rock-boring Leiosolenus patagonicus populations longevity ranged between 6.5 and 15 years with a growth ratefrom ~ 3.6 mm/year (4 years old) to ~ 2.2 mm/year (13years old; Bagur et al. 2013).
Many studies report shallow-water rhodolith growth
rates of < 1 mm/year (Bosence 1983b; De Grave et al.
2000; Frantz et al. 2000; Rivera et al. 2004; Steller et al.
2007; Kamenos et al. 2008). Annual growth rates forrhodoliths from the Santa Catalina Island, California
were calculated at 1.25 ± 0.62 mm/year (Tompkins andSteller 2016). Although some tropical coralline species
grow faster than 1 mm/year (Matsuda 1989), the majority of coralline species have growth rates < 0.4 mm/year(Figueiredo et al. 2012).
Considering a calibrated age of about 3500 cal. year
BP, the deep-water macroids off Kikai-jima have an apparent growth rate of about 0.02 mm/year (Bassi et al.
2019). These macroids did not grow continuously; rather

their growth is commonly intermittent, probably as a result of repeated burial and exposure, as commonly
known from many macroids and rhodoliths in various
settings (e.g., Matsuda and Iryu 2011). This apparent
macroid growth rate is comparable to those for deepwater foraminiferal-algal nodules of 0.02–0.09 mm/year
at 30–60 m depth (Reid and Macintyre 1988) and 0.01–
0.05 mm/year at 61–91 m depth (Littler et al. 1991).
Comparable growth rates have been found for deepwater rhodoliths on the Brazilian Shelf (0.04 mm/year,
Brasileiro et al. 2018).
In shallow-water (< 12 m), rocky and sandy coquina
substrates Lithophaga growth rates of ~ 1.6–3.0 mm/
year (Peharda et al. 2015) are higher than those reported
for our deeper macroids/rhodoliths (0.01–0.05 mm/year). Considering that substrate composition and hardness along with water temperature seem to largely influence boring bivalve growth parameters (Bagur et al.
2014; Peharda et al. 2015), in deep-water macroids andrhodoliths, the boring bivalves likely grow slower than
the shallow-water counterparts, although still higher
than the host’s growth. In the deep-water macroid andrhodolith beds, the identified juvenile boring bivalve
specimens grew as fast as their host just during the early
growth stages (Fig. 11). Since the boring bivalves growfaster than the macroid and rhodolith host, most ofthem died or reached an early adult stage characterized
by a small size due to a slow growth rate. For othermacroids and rhodoliths that might grow faster, theseBassi et al. Progress in Earth and Planetary Science(2020) 7:41

Page 14 of 17

biodiversity, and palaeobathymetry. The use of
Gastrochaenolites ichnospecies as palaeobathymetricindicators must be treated with caution due to thelack of taxonomic and ecological (phenotypic
plasticity) data about present-day deep-water boringbivalves.

problems do not develop. Where deep-water macroids
and rhodoliths might overturn, the juveniles may be
choked and die.

5 Concluding remarks
Six study cases of macroid and rhodolith beds from 0 to
117 m water depth of the Pacific Ocean (northern Central Ryukyu Islands, Fraser Island, One Tree Reef, Lizard
Island, Moorea) and Mediterranean Sea (southeastern
Spain) were analyzed. Distribution of the domichnia
Gastrochaenolites and its producers (i.e., gastrochaenid
and mytilid boring bivalves) were assessed. Four coreconclusions underscore unusual aspects of the studied
macroid and rhodolith beds.
1. The gastrochaenid and mytilid boring bivalves do
not show competition for space with other borers
such as etching sponges and polychaete worms.
The highest bioerosion recorded in the macroids
and rhodoliths below wave base is mainly producedby sponges and polychaete worms.
2. The boring bivalves belong to four genera(Gastrochaena, Gregariella, Leiosolenus,
Lithophaga) and eleven species. For the first time,living individuals of Gastrochaena cuneiformis, G.
cf. turbinatus, Leiosolenus (L. malaccanus, L.
mucronatus, L. spp.; Fraser Island, deeper than 40m), and Lithophaga/Leiosolenus sp. (Kikai-jima,
deeper than 75 m) were found in waters deeper
than 20 m.
3. On average, the boring bivalves are slenderer andsmaller than those growing inside shallow-water
rocky substrates. In free-living nodules, the boringbivalve growth is constrained by the acervulinid
foraminiferal/coralline algal host growth rate and by
the host-overturn and burial rate. In shallow-watersettings, the higher rhodolith-overturning ratecauses juvenile mortality. In deep-water (> 40 m)
higher macroid and rhodolith stability allows theboring bivalves to reach an adult stage.
4. During the juvenile stage, the bivalves can equal thehost growth but, due to their faster growth, rarely
they reach the early adult stage. Although thegrowth rate of deeper gastrochaenids and mytilids ispresumably slower than that of their shallow-water
rocky-substrate counterparts, it is faster than that of
the acervulinid foraminiferal/coralline algal hosts.
As a consequence of phenotypic plasticity, smallsized adults with slow growth rates might coexist
with juveniles.
5. These observations provide a basis forpalaeoecological interpretation of fossil macroid andrhodolith deposits in terms of boring bivalve
morphologic variation, ichno- and palaeo-

Abbreviations
BI: Bioerosion index; E: Entobia Bronn; G: Gastrochaenolites Leymarie;
M: Maeandropolydora Voigt; s.d.: Standard deviation; T: Trypanites Mägdefrau;
R: Rogerella de Saint-Seine
Acknowledgements
Sincere thanks are expressed to the Museum of Natural History and to the
Graduate Program in Earth and Environmental Sciences (GP-EES), Tohoku
University, for inviting DB to Sendai, Japan. JHL thanks the support andencouragement of the Directors of the Gump Biological Research Station(GBRS) of the University of California, Berkeley located on Moorea, Directors
George Roderick and Dr. Neil Davies for permitting JHL to work at theStation, and the station managers Mr. Frank Murphy, Drs. Stephen Strand,
and John Woodward, and the staff of GBRS for logistic and living support.
This work was done under permit No. 568/BCO from Haut-Commissariat de
La Republique en Polynesie Francaise. JHL is grateful for the collection
support from the Museum of Paleontology, Berkeley. This is UC Museum ofPaleontology Publication 3000, and a GBRS contribution in science. This
paper is a scientific contribution of the Project MIUR–Dipartimenti di
Eccellenza 2018–2022 and of the PRIN 2017 RX9XXXY. The authors are
grateful to two anonymous reviewers and the PEPS editor K. Endo for
constructive comments.
Authors’contributions
DB, JCB, and YI proposed and designed the study. JCB, JA, JHL, and YI
conducted the field sampling. DB, JCB, JA, and YI described the macroids
and the rhodoliths. DB identified the ichnospecimens. MO identified theboring bivalves and discussed their ecology. MO and HT illustrated thestudied specimens. All authors interpreted the data and read and approved
the final manuscript.
Funding
This work was supported by the Japan Society for the Promotion of Science
KAKENHI (Grant-in-Aid for Scientific Research), grant number 25247083 to YI.
This investigation was financially supported in part by local research funds(Erasmus+, FAR2012–2017, FIR2016, FIR2018, PRIN 2017RX9XXXY “Biotic
resilience to global change: biomineralization of planktonic and benthic
calcifiers in the past, present and future” and the BioMed Central-Prepay
Membership at the University of Ferrara, DB). JCB and JA were supported by
Junta de Andalucía Research Group RNM 190. JHL thanks the Committee on
Research, the Museum of Paleontology and the Department of Integrative
Biology, UC Berkeley, and the UC Pacific Rim Project for financial support ofhis field and laboratory work.
Availability of data and materials
All data generated and analyzed during this study are included in thispublished article. Please contact the corresponding author regarding data
requests.
Competing interests
The authors declare that they have no competing interests.
Author details
Dipartimento di Fisica e Scienze della Terra, Università degli Studi di Ferrara,
Via Saragat 1, I-44122 Ferrara, Italy. 2Departamento de Estratigrafia yPaleontologia, Universidad de Granada, Campus de Fuentenueva s/n, 18002
Granada, Spain. 3Department of Biological Sciences, Faculty of Science,
Kanagawa University, 2946 Tsuchiya, Hiratsuka City, Kanagawa Prefecture259-1293, Japan. 4Department of Integrative Biology and Museum ofPaleontology, University of California, Berkeley, California 94720, USA.
5
Institute of Geology and Paleontology, Graduate School of Science, Tohoku
University, Aobayama, Sendai 980-8578, Japan.
1Bassi et al. Progress in Earth and Planetary Science(2020) 7:41

Received: 25 September 2019 Accepted: 19 July 2020

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