Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: A hypothesis.

Brachiopods were thought to have dominated deep-sea hydrothermal vents and hydrocarbon seeps for most of the Paleozoic and Mesozoic, and were believed to have been outcompeted and replaced by chemosymbiotic bivalves during the Late Cretaceous. But recent findings of bivalve-rich seep deposits of Paleozoic and Mesozoic age have questioned this paradigm. By tabulating the generic diversity of the dominant brachiopod and bivalve clades-dimerelloid brachiopods and chemosymbiotic bivalves-from hydrocarbon seeps through the Phanerozoic, we show that their evolutionary trajectories are largely unrelated to one another, indicating that they have not been competing for the same resources. We hypothesize that the dimerelloid brachiopods generally preferred seeps with abundant hydrocarbons in the bottom waters above the seep, such as oil seeps or methane seeps with diffusive seepage, whereas seeps with strong, advective fluid flow and hence abundant hydrogen sulfide were less favorable for them. At methane seeps typified by diffusive seepage and oil seeps, oxidation of hydrocarbons in the bottom water by chemotrophic bacteria enhances the growth of bacterioplankton, on which the brachiopods could have filter fed. Whereas chemosymbiotic bivalves mostly relied on sulfide-oxidizing symbionts for nutrition, for the brachiopods aerobic bacterial oxidation of methane and other hydrocarbons played a more prominent role. The availability of geofuels (i.e. the reduced chemical compounds used in chemosynthesis such as hydrogen sulfide, methane, and other hydrocarbons) at seeps is mostly governed by fluid flow rates, geological setting, and marine sulfate concentrations. Thus rather than competition, we suggest that geofuel type and availability controlled the distribution of brachiopods and bivalves at hydrocarbon seeps through the Phanerozoic.

Introduction

The idea of bivalves replacing brachiopods as the dominant benthic filter feeders over the course of the Phanerozoic is one of the oldest macroevolutionary patterns discussed in paleontology [1-3]. Originally observed in the rich fossil record of shallow marine environments, a similar pattern was also seen at deep-sea hydrothermal vents and hydrocarbon seeps [4]. These ecosystems differ radically from all others in being based on chemosynthetic primary production rather than photosynthesis [5]. The evolution of the chemosynthesis-based faunal communities may therefore be buffered from mass extinctions and other disruptions of photosynthesis-based food chains [6-8] and may instead be driven by events affecting the discharge of the reduced chemicals (referred to as geofuels hereafter) that fuel the chemosynthesis-based food chain [9]. The animals that dominate chemosynthesis-based ecosystems show extensive physiological adaptations, commonly involving a symbiosis with chemotrophic bacteria, resulting in faunal communities with a low diversity but high abundance of highly specialized animals [10, 11].

A first compilation of Phanerozoic vent and seep sites with brachiopods and/or bivalves indicated a pattern of a Paleozoic to middle Mesozoic dominance of brachiopods in these ecosystems, and the chemosymbiotic bivalves became dominant from the Late Cretaceous onward [4]. Subsequent research confirmed a number of Paleozoic and early Mesozoic seep deposits dominated by brachiopods, including Septatrypa in the Silurian [12], Dzieduszyckia in the Devonian [13], Ibergirhynchia in the Carboniferous [14], Halorella in the Triassic [15], and Sulcirostra and Anarhynchia in the Jurassic [16-18], supporting this hypothesis. However, also discovered were seep deposits at which inferred chemosymbiotic bivalves were a major faunal element, including the modiomorphid genus Ataviaconcha at Silurian and Devonian sites in Morocco [19, 20] and kalenterid and anomalodesmatan genera at Triassic sites in Turkey [21, 22]. These findings challenge the claim of predominantly brachiopod-dominated pre-Cretaceous vents and seeps, and raise the questions why some sites were dominated by brachiopods and others by bivalves.

A further complication in this context is that the feeding strategy (or strategies) of vent and seep-inhabiting brachiopods is essentially unknown. The large size of certain species and brachiopod dominance at some sites may intuitively suggest that they were chemosymbiotic [18, 23, 24]. However, brachiopods are virtually absent from extant vents and seeps, and the few known examples are filter feeder that take advantage of the hard substrate provided by authigenic carbonates exposed at some seeps [25]. Furthermore, the general brachiopod bauplan lacks certain features, such as gills and a closed cardio-vascular system, which are important for hosting chemosymbionts in bivalves or tube worms [26, 27] and make brachiopods ill-suited for coping with the toxicity of hydrogen sulfide. Furthermore, the brachiopods that formed mass occurrences at ancient seeps are not drawn randomly from the brachiopod tree of life but instead belong, with one exception, to a single clade: the Dimerelloidea [28]. The one exception is the genus Septatrypa from a Silurian seep deposit in Morocco [12], which belongs to a different rhynchonellate order than the dimerelloids. Because insights into the feeding strategy of seep-dominating brachiopods are only available for the dimerelloids (see below), our study focuses exclusively on members of this clade. One intriguing feature of many seep deposits dominated by dimerelloids is the sheer abundance of the brachiopods, which by far exceeds the abundance of chemosymbiotic bivalves at fossil seep deposits ([13, 15, 17, 29], own observations).

Here we present the hypothesis that dimerelloid brachiopods and chemosymbiotic bivalves coexisted at hydrocarbon seeps during the Paleozoic and Mesozoic by partitioning the locally available geofuels. We propose that the presence, absence, or relative abundance of each clade at a given site was largely controlled by the chemical composition of the seep fluids (the proportions of sulfide, methane, and/or oil), which in turn was influenced by seepage intensity and perhaps seawater sulfate concentrations. Our hypothesis is based on (i) a tabulation of the diversity of the ecologically dominant bivalve and brachiopod genera at seeps through the Phanerozoic; (ii) recent improvements in geochemically assessing the composition of fluids and the intensity of fluid flow at ancient seeps; and (iii) a set of derivations and assumptions on the paleoecology of the dominant brachiopod and bivalve clades at ancient hydrocarbon seeps.

Approach

Compilation of generic diversity of bivalves and brachiopods

Modern seep communities are characterized by the low diversity but high abundance of a few taxa that are able to take advantage of the unique food resources at seeps [5, 30]. Thus our compilation of brachiopod and bivalve diversity at seeps includes only the ecologically dominant clades instead of the full range of genera known from fossil seep deposits to avoid the results being blurred by chance occurrences or by local taxa fortuitously taking advantage of the abundance of food at a seep site (known as ‘vagrants’ or ‘background taxa’, cf. [31] Sibuet and Olu, 1998). Among bivalves, only chemosymbiotic or in the case of extinct taxa, inferred chemosymbiotic taxa, were included. Although chemosymbiotic bivalves may occasionally be rare, in general they dominate seep deposits numerically (cf. [9] Kiel, 2015; [32] Campbell, 2006).

Among brachiopods, only dimerelloid genera reported from geochemically confirmed seep deposits are included because (i) with a single exception (see below), only dimerelloids occurred at ancient seeps in rock-forming quantities; all other brachiopods reported from ancient seeps (including various terebratulids, i.e. [33-37]) represent minor faunal elements that most likely took advantage of exposed hard substrate [28], and (ii) the feeding strategies of brachiopods at ancient seeps remain unclear except for the dimerelloids, for which some clues are available [38]. The only exception to (i) is Septatrypa, which occurs in rock-forming quantities in a Silurian seep deposit from Morocco [12]. This genus belongs to a different rhynchonellate order than the dimerelloids, hence we refrain from extending the feeding strategy inferred from the Cretaceous dimerelloid Peregrinella to this Silurian genus.

The dataset includes 42 bivalve and seven brachiopod genera; their stratigraphic distributions, life habits (epifaunal, semi-infaunal, and infaunal), and all relevant references are shown in Table 1. To assess a potential sampling bias, we also compiled the number of seep-bearing rock units at which these taxa were found (Table 2), as done in a previous quantitative study on seep faunas [8].

Table 1

Dimerelloid brachiopod genera and (inferred) chemosymbiotic bivalve genera in ancient hydrocarbon-seep deposits.

New brachiopod and bivalve genera established since Mike Sandy’s review of dimerelloid brachiopods as seep-inhabitants in 1995 [23] are marked by an asterisk (*); see section ‘Diversity pattern’ for reasoning.

NEOGENE
Dimerelloid brachiopods:	none.
Infaunal bivalves:	Acharax [39], Anodontia [40], Channelaxinus* [41], Cubatea* [42], Elliptiolucina*, Elongatolucina* [43], Isorropodon [44], Lucinoma, Meganodontia* [41], Megaxinus [45], Myrteopsis, Nipponothracia*, Pegaphysema [43], Pliocardia [46], Solemya [47], Thyasira [48].
Semi-infaunal bivalves:	Archivesica [41], Callogonia [49], Calyptogena [50], Conchocele [42, 47], Gigantidas* [51], Notocalyptogena* [52], Pleurophopsis (= Adulomya) [42, 53, 54].
Epifaunal bivalves:	Bathymodiolus [41, 51].
PALEOGENE
Dimerelloid brachiopods:	none.
Infaunal bivalves:	Acharax [42, 55], Amanocina*, Cubatea*, Elliptiolucina*, Elongatolucina* [43, 56], Epilucina [57], Lucinoma [58], Maorityas [59], Nipponothracia* [43], Nucinella [55], Nymphalucina [43], Pliocardia [42], Rhacothyas* [33], Solemya [60], Thyasira [59].
Semi-infaunal bivalves:	Conchocele [59], Hubertschenckia [44], Pleurophopsis [42].
Epifaunal bivalves:	Bathymodiolus, Idas, Vulcanidas* [60].
LATE CRETACEOUS
Dimerelloid brachiopods:	none.
Infaunal bivalves:	Acharax [61], Amanocina* [43], Cubatea* [43], Miltha [61], Myrtea [61], Nucinella [62], Nymphalucina [43], Solemya [63, 64], Tehamatea* [43], Thyasira [48, 59].
Semi-infaunal bivalves:	Caspiconcha* [65, 66], Conchocele [59, 63].
Epifaunal bivalves:	none.
EARLY CRETACEOUS
Dimerelloid brachiopods:	Peregrinella [29, 38].
Infaunal bivalves:	Acharax [67], Amanocina* [43], Cretaxinus* [68], Cubatea* [43], Nucinella [67–69], Solemya [64, 68, 70], Tehamatea* [43], Thyasira [59].
Semi-infaunal bivalves:	Caspiconcha* [65].
Epifaunal bivalves:	none.
JURASSIC
Dimerelloid brachiopods:	Anarhynchia [18], Cooperrhynchia [71], Sulcirostra [17].
Infaunal bivalves:	Acharax [67], Beauvoisina* [43], Nucinella [68], Solemya [68], Tehamatea* [37].
Semi-infaunal bivalves:	Caspiconcha* [65].
Epifaunal bivalves:	none.
TRIASSIC
Dimerelloid brachiopods:	Halorella [15, 21].
Infaunal bivalves:	Nucinella [15], Aksumya* [22].
Semi-infaunal bivalves:	Terzileria*, Kasimlara* [22].
Epifaunal bivalves:	none.
CARBONIFEROUS
Dimerelloid brachiopods:	Ibergirhynchia* [72].
Infaunal bivalves:	‘solemyid’ [14].
Semi-infaunal bivalves:	none.
Epifaunal bivalves:	none.
DEVONIAN
Dimerelloid brachiopods:	Dzieduszyckia [13].
Infaunal bivalves:	Dystactella [20].
Semi-infaunal bivalves:	Ataviaconcha* [20].
Epifaunal bivalves:	none.

Table 2

Seep-bearing rock units or equivalents, sorted into the same geologic time bins as the genera in Table 1; Fm = Formation.

Site(s)	Rock unit or equivalent	Reference
NEOGENE
Fukaura town	Akaishi Fm	[50]
Ogasawara's slumped block	Aokiyama Fm	[47]
Stirone River seep complex	Argille Azzurre Fm	[73]
LACM loc. 6132, USGS M2790	Astoria Fm	[44]
Akanuda Limestone	Bessho Fm	[74]
Bexhaven, Karikarihuata, Moonlight North, Rocky Knob, Tauwhareparae, Waipiro	Bexhaven Limestone	[51]
Liog-Liog Point	Bata Fm	[75]
Takangshan quarry	Gutingkeng Fm	[76]
Ikegami	Hayama Fm	[77]
Shimo-sasahara, near Yatsuo	Higashibessho Fm	[46]
Oinomikado & Kanehara 1938 loc.	Higashiyama Oil field	[47]
Saitama conglomerate	Hiranita Fm	[78]
Nagasawa & Oyamada's 1996 loc.	Hongo Fm	[47]
Kamada's Honya loc.	Honya Fm	[47]
Cantera Portugalete	Husillo Fm	[42]
Haunui, Ugly Hill, Wanstedt	Ihungia Series	[79]
slumped blocks, YDFAB 1993	Ikedo Fm	[47]
Joban coal field	Kabeya Fm	[80]
Doguchi Bridge	Kawazume Fm	[47]
Izura Kanko Hotel	Kokozura Fm	[49]
Matsudai, Sugawa	Kurokura Fm	[81]
Freeman's Bay, Godineau River, Jordan Hill	Lengua Fm	[42]
Casa Cavalmagra, Case Rovereti, Castellvecchio, Le Colline, Montepetra	Marnoso-arenacea Fm	[41]
Kanie's 1991 juvenile Calyptogena loc.	Misaki Fm	[47]
Morai, Otatsume's 1942 loc.	Morai Fm	[47]
loc. M2 of Shikama & Kase, 1976	Morozaki Group	[47]
Limestone nodule in Kochi	Muroto Fm	[82]
Ozaki 1958 loc.	Naari Fm	[83]
Nadachi Signal Station	Nadachi Fm	[84]
Amano et al 1994 loc.	Nanbayama Fm	[47]
Nakanomata seep deposit	Nodani Fm	[85]
Rekifune seep	Nupinai Fm	[86]
Kanno & Akatsu 1972 loc.	Nupinaigawa mudstone	[47]
Yokohama City	Ofuna Fm	[47]
Kita-Kuroiwa	Ogaya Fm	[74]
Sakurai's 2003 loc.	Ogikubo Fm	[47]
Hayashi's 1973 localities	Ohno Fm	[47]
Ogasawara 1986 Akita loc.	Onnagawa Fm	[47]
Huso Clay Member	Pozon Fm	[87]
Quinault seep	Quinault Fm	[88]
Hayashi & Miura's 1973 loc.	Ryusenji Fm	[47]
Buton asphalt deposit	Sampalokossa Beds	[89]
Matsumoto & Hirata's 1972 Shizuoka loc.	Setogawa Group	[82]
Oshima	Shikiya Fm	[90]
Kawaguchi/Kotto	Shiramazu Fm	[91]
SOFZ—Baths Cliffs fauna	SOFZ	[87]
Joban coal field	Taira Fm	[80]
Kanno & Ogawa 1964 loc.	Takinoue Fm	[92]
Kanno's 1967 Tokyo loc.	Tateya Fm	[47]
Oinomikado & Kanehara's 1938 loc.	Teradomari Fm	[47]
Sasso delle Streghe	Termina Fm	[41]
Abisso Mornig, Casa Carnè, Casa Piantè	Tossignano marls	[41]
Tanaka's Matsumoto City loc.	Uchimura Fm	[47]
Katto & Masuda's 1978 pyrite loc.	Uematsu Fm	[47]
Matsumoto's 1966 & 1971 Shizuoka locs.	Wappazawa Fm	[47]
Kanehara's 1937 loc.	Yunagaya and Shirado Groups	[93]
PALEOGENE
Fossildalen	Basilika Fm	[35]
Buje petrol station	Central Istria flysh	[94]
Diapiric mélange, Joes River	Diapiric melange	[87]
Angela Elmira asphalt mine	Elmira Asphalt	[95]
Bear River (LACMIP loc. 5802)	equivalent of Lincoln Creek Fm	[96]
Belen	Heath shales	[95]
LACMIP loc. 12385, CSUN loc. 1583	Humptulips Fm	[96]
LACMIP loc. 17101	Jansen Creek Member	[60]
Rock Creek Oregon, Vernonia-Timber Road	Keasey Fm	[97]
CR2, UWBM loc. B-7451, LACMIP loc. 5843, LACMIP loc. 16504, SR1-SR4	Lincoln Creek Fm	[60, 98–100]
Bullman Creek, LACMIP loc. 6958, Shipwreck Point	Makah Fm	[58, 59, 101]
Cima Sandstone lentil	Moreno Fm	[102]
Kami-Atsunai railway station	Nuibetsu Fm	[103]
Urahoro concretion	Oomagari Fm	[47]
Palmar-Molinera-Road	Palmar-Molinera	[95]
Huberschenkia-loc. (Yayoi site)	Poronai Fm	[104]
East Twin River, LACMIP locs. 15621, 6295, Whiskey Creek	Pysht Fm	[59, 100, 101, 105]
North Slope	Sagavanirktok Fm	[32]
Kiritachi	Sakasagawa Fm	[59]
Tanami	Shimotsuyu Fm	[55]
Columbia River, UWBM loc. B-7446	Siltstone of Shoalwater Bay	[60]
West Fork of Grays River	Siltstone of Unit B	[59]
Lomitos	Talara Fm	[95]
Wagonwheel seep CSUN loc. 1580	Wagonwheel Fm	[57]
LATE CRETACEOUS
Awanui GS 688, Waipiro I, Waipiro III	East Coast Allochthon	[69]
Guenoc Ranch	Great Valley Group	[64]
Maeshima	Himenoura Group	[59]
Seymour Island	Lopez de Bertodano Fm	[63]
Romero Creek	Moreno Fm	[64]
Sada Limestone	Nakamura Fm	[106]
Omagari lens, Yasukawa seep	Omagari Fm	[107, 108]
Tepee Buttes	Pierre Shale	[109]
Snow Hill Island	Snow Hill Island Fm	[63]
Alton Sink, North & South Cottonwood Wash	Tropic Shale	[110]
Obira-cho	Yezo Supergroup	[61]
EARLY CRETACEOUS
Sassenfjorden carbonates	Agardhfjellet Fm	[111]
near Freiberg	Beskidy Range	[112]
Eagle Creek	Budden Canyon Fm	[65]
Yongzhu bridge	Chebo Fm	[113]
Bonanza Creek	Chisana Fm	[114]
Prince Patric & Ellef Ringnes isl&s	Christopher Fm	[115]
Bear Creek, Foley Canyon, Rocky Creek	Crack Canyon Fm	[64]
Awanui I & II	East Coast Allochthon	[69]
Novaya Zemlya III sandy limestone	float	[116]
Little Indian Valley	Fransiscan Complex	[64]
Gravelly Flat	Gravely Flat Fm	[64]
East Berryessa, Knoxville, Rice Valley, West Berryessa, Wilbur Springs	Great Valley Group	[64]
Baska	Hradiště Fm	[117]
Cold Fork of Cottonwood Creek	Lodoga Fm	[118]
Musenalp	Musenalp	[119]
Ispaster	Ogella unit	[120]
W. Kuban	Oubine Valley	[121]
Planerskoje	Planerskoje section	[122]
East of Lhasa	Sangxiu Fm	[123]
Sinaia Beds	Sinaia Fm	[124]
Koniakov, Koniakover Schloss, Raciborsko	Upper Grodziszcze beds	[29, 125]
Curnier, Rottier	Vocontien Basin	[38]
Kuhnpasset Beds	Wollaston Forland	[70]
Ponbetsu, Utagoesawa	Yezo Supergroup	[66, 126]
JURASSIC
Sassenfjorden carbonates	Agardhfjellet Fm	[111]
Gateway Pass Limestone Bed	Atoll Nunataks Fm	[127]
Novaya Zemlya I & II	float	[116]
Charlie Valley	Fransiscan Complex	[64]
NW Berryessa, Stony Creek	Great Valley Group	[64]
Copper Island	Inklin Fm	[18]
Seneca	Keller Creek Fm	[17]
Paskenta	Stony Creek Fm	[128]
Beauvoisin	Terres Noires Fm	[129]
TRIASSIC
Terziler and Dumanlı	Kasimlar shales	[21]
Graylock Buttes	Rail Cabin mudstone	[15]
CARBONIFEROUS
Tentes Mound	Calcaires de l’Iraty	[130]
Ganigobis	Ganigobis Shale Member	[131]
Iberg seep	Iberg reef	[14]
DEVONIAN
Sidi Amar	Devonian-Carboniferous mélange	[13]
Hollard Mound	Pinacites limestone	[132]

Proxies for fluid chemistry and flow intensity at ancient seeps

Criteria used to reconstruct the composition of seep fluids and seepage intensity are based on the mineralogy and microfabric of authigenic carbonate and sulfide minerals, stable isotope signatures of authigenic minerals, and lipid biomarkers [133-140]. This set of methods, however, does not allow to reliably discern methane-seep and oil-seep deposits. The use of lipid biomarkers seems an obvious approach for such discrimination, but is hampered by the facts that (i) sulfate-driven anaerobic oxidation of methane occurs at oil seeps too [141] and (ii) the prokaryotes responsible for anaerobic degradation of oil components in marine settings (i.e. sulfate-reducing bacteria; [142]) may yield similar biomarkers like the sulfate-reducing bacteria involved in anaerobic oxidation of methane. Even more problematic, the great abundance of oil components in some seep deposits tends to mask the lipid biomarkers reflecting local biogeochemical processes [143]. Such masking by oil-derived components is a particular problem for the recognition of possible ancient oil-seep deposits, since the timing of oil ingress (syngenetic vs. epigenetic) is commonly difficult to constrain [13]. The sheer presence of pyrobitumen (i.e. metamorphosed oil) in ancient seep limestones is consequently not sufficient proof for oil seepage. These problems prompted the development of an inorganic geochemical proxy for oil seepage. Molybdenum to uranium ratios in conjunction with rare earth element contents of seep limestones have been shown to allow oil-seep and methane-seep deposits to be discriminated [144]. The application of this proxy resulted in the confirmation that Late Devonian limestones from Morocco with the dimerelloid brachiopod Dzieduszyckia formed at oil seeps. Future work will have to reveal if some of the other seep limestones with dimerelloids, for which the presence of pyrobitumen was documented, are oil-seep deposits as well.

Another crucial aspect for our reconstruction of the adaptation of bivalves and brachiopods to seep ecosystems concerns the mode in which methane was predominantly oxidized (i.e. anaerobic vs. aerobic methanotrophy). It seems straightforward that episodes of low seawater sulfate concentration favor the release of methane into bottom waters [9, 145], with less methane being oxidized at the sulfate-methane transition zone and more methane available for aerobic methane-oxidizing bacteria. Interestingly, also the mode of seepage (i.e. advective vs. diffusive) is likely to affect the relative proportions of anaerobic and aerobic methanotrophy. Although possibly counterintuitive at first glance, it has been shown that more methane tends to permeate the barrier at the sulfate-methane transition zone formed by sulfate-driven anaerobic oxidation of methane at diffusive seeps compared to advective seeps [146-148]. This circumstance agrees with the observation of more abundant biomarkers of aerobic methanotrophic bacteria in seep deposits reflecting diffusive seepage (Natalicchio et al., 2015) and the inferred affinity of Peregrinella to diffusive seepage and aerobic methanotrophy [38]. Likewise, seeps with advective flow will tend to be characterized by high concentrations of hydrogen sulfide–resulting from pronounced sulfate-driven anaerobic oxidation of methane at the sulfate-methane transition zone–whereas at seeps with diffusive flow more methane will be oxidized with molecular oxygen by aerobic methanotrophs.

Assumptions on chemosymbiosis in fossil bivalves

For the sake of our hypothesis, we assume that all bivalve clades that dominated seep deposits before the Cenozoic era were hosting thiotrophic (i.e. sulfide-oxidizing) symbionts only. For most clades, including the Solemyidae, Nucinellidae, Thyasiridae, and Lucinidae, this is a fair assumption based on the actualistic principle: members of these families host thiotrophic symbionts only [149]. The only bivalve clade known to harbor methanotrophic symbionts is the Bathymodiolinae [150, 151]. A detailed study on their evolutionary history [152] showed that the path to methanotrophic symbiosis is difficult: first, only 13 out of 52 investigated species harbor methanotrophs; second, intracellular rather than extracellular symbiont location seems to be required to host methanotrophs; and third, methanotrophic symbiosis was acquired fairly recently in the evolutionary history of the bathymodiolins (in the early Miocene), while the original thiotrophic symbiosis goes much further back in time [152]. Remarkable in this context is that other bivalve families with intracellular symbionts have apparently not developed methanotrophic symbiosis, despite having a similarly long (Vesicomyidae; cf. [153] Kiel, 2010) or much longer evolutionary history (Solemyidae, Lucinidae; cf. [20] Hryniewicz et al., 2017; [154] Taylor et al., 2011).

Inferring chemosymbiosis or even symbiotic types is much harder in extinct taxa such as the modiomorphids–a clade commonly found at ancient vents and seep [20, 155]–because there is presently no way to proof chemosymbiosis in the fossil record. However, some clues may be drawn from the geologic history of the modiomorphid/kalenterid genus Caspiconcha, which is found in many Late Jurassic to Late Cretaceous seep deposits around the world [66, 70, 122]. Caspiconcha was common during most of the Early Cretaceous but declined in abundance and eventually disappeared after marine sulfate concentrations–and hence sulfide availability at seeps–dropped in the Aptian [9, 66, 145]. If Caspiconcha had had methanotrophic symbionts, it should not have been affected by the low sulfate concentrations; on the contrary, it should have thrived due to the higher availability of methane at seeps (see above). But Caspiconcha responded to the mid- to Late Cretaceous low sulfate concentrations in a way expected for a taxon with thiotrophic symbionts. Based on this observation, we assume that Caspiconcha, and seep-inhabiting modiomorphids/kalenterids during the Phanerozoic in general, had thiotrophic rather than methanotrophic symbionts. Furthermore, because virtually all extant bivalves taking up geofuels for their symbionts from pore water have thiotrophic symbionts [11, 149], the infaunal and semi-infaunal lifestyle of the inferred chemosymbiotic bivalves at pre-Cenozoic seeps suggests that they relied on thiotrophy rather than methanotrophy.

The resource partitioning hypothesis: Outline and arguments

Diversity pattern

The bivalve genera at seeps are of low diversity during the Paleozoic followed by a continuous increase in diversity since the Triassic (Fig 1). Prior to the Cenozoic, this increase in diversity is mostly among infaunal genera, plus a few semi-infaunal ones; epifaunal bivalves appeared only in the Cenozoic (Fig 1). The continuous rise in bivalve diversity at seeps, at least since the Mesozoic, appears to mirror the general Phanerozoic increase in bivalve diversity [2]. But the low diversity of semi-infaunal and epifaunal bivalves at seeps and their rapid diversification in the Cenozoic are unlike the general Phanerozoic pattern of bivalve ecospace occupation with its similar proportions of infaunal, semi-infaunal, and epifaunal taxa in the Mesozoic and Cenozoic [156]. This bias toward infaunal taxa might result from our focus on chemosymbiotic bivalves. Indeed, the bivalve diversification pattern at seeps is quite similar to that of the most diverse clade of shallow-water chemosymbiotic bivalves–the Lucinidae [157]–which also shows low diversity during the Paleozoic and a continuous increase starting in the Mesozoic [158]. One may thus argue that bivalve diversity at seeps follows the diversity of chemosymbiotic bivalves in shallow water. Epifaunal and semi-infaunal chemosymbiotic bivalves such as bathymodiolins and vesicomyids are virtually absent from shallow water [149] and appear to be a unique feature of vent and seep environments.

Fig 1

Phanerozoic generic diversity of chemosymbiotic bivalves and dimerelloid brachiopods at hydrocarbon seeps, and the number of seep-bearing rock units.

Note break in scale and that the Permian was omitted because no confirmed seep deposits have been reported from this period to date. E. = Early, L. = Late.

Although this trend in increasing generic diversity among bivalves is roughly mirrored by an increase in the number of seep-bearing rock units (Fig 1), this pattern does not hold when seen in detail: (i) there is an increase in bivalve diversity from the Early to the Late Cretaceous despite a >50% decrease in the number of seep-bearing rock units; (ii) there are roughly identical numbers of seep-bearing rock units in the Early Cretaceous and in the Paleogene, but almost twice as many bivalve genera in the Paleogene; (iii) the number of seep-bearing rock units doubles from the Paleogene to the Neogene, accompanied by only a minor increase in bivalve diversity. Thus, we are confident that the observed pattern in bivalve diversity at seeps represents a real phenomenon, rather than being a sampling bias, although it is clear that the Paleozoic and early Mesozoic are still undersampled and likely contained higher numbers of bivalves at seeps.

Seep-dwelling dimerelloids are of low diversity during the Paleozoic, show a slight increase during the Jurassic and disappear after the Early Cretaceous (Fig 1). This pattern does not mirror the general Phanerozoic brachiopod diversity pattern of Paleozoic dominance, end-Permian decline, and low post-Paleozoic diversity [2]. Two observations indicate that this pattern is not significantly affected by sampling biases: first, despite the large number of seep-bearing rock units in the Early Cretaceous, there is only a single dimerelloid genus at seeps in this epoch. Second, since the first review of dimerelloid genera as potential seep-inhabiting brachiopods in 1995 [23], only a single new dimerelloid genus has been described: the Carboniferous Ibergirhynchia [72]. During the same time interval, 18 new genera of seep-inhabiting bivalves have been described, including nine from the Mesozoic and Paleozoic (indicated by asterisks in Table 1). This indicates that despite being undersampled, the relative proportions of brachiopod and bivalve genera at Paleozoic and early Mesozoic seeps shown in Fig 1 are fairly robust. The diversity pattern also does not confirm the paradigm that vents and seeps were dominated by brachiopods during the Paleozoic and most of the Mesozoic and that chemosymbiotic bivalves took over only in the Late Cretaceous [4]. Instead, dimerelloid brachiopods and chemosymbiotic bivalves have coexisted at seeps for nearly half of the Phanerozoic (Late Devonian to Late Cretaceous, ~240 million years [19]). This raises the question whether chemosymbiotic bivalves have indeed “exploited these habitats better than brachiopods” ([4] Campbell and Bottjer, 1995, p. 323).

Ecology of seep-inhabiting brachiopods

At modern seeps, coexisting taxa tend to be spatially separated because different organisms require different types and amounts of geofuels, and the distribution of these geofuels is in turn controlled by flow rates and the resulting geochemical gradients [31, 159]. For example, among two species of vesicomyid clams at seeps in Monterey Canyon, Archivesica kilmeri requires 10 times higher ambient sulfide concentrations than Calyptogena pacifica, and consequently C. pacifica occupies the periphery of the seep where sulfide flux is low, whereas A. kilmeri lives in the sulfide-rich center of the seep [160]. Analogous faunal distribution patterns in relation to geochemical gradients can be traced into the fossil record: mollusks at Cretaceous seeps show similar zonation as their modern analogs [108, 109], and predation scar frequencies in Oligocene chemosymbiotic bivalves are inversely related to the different, assumed sulfide requirements of these species, most likely because the more sulfidic areas were avoided by predators and hence the bivalves with the highest sulfide requirements were spared from predation [161].

The Cretaceous seep-inhabiting dimerelloid brachiopod Peregrinella provides a particularly intriguing case of a geochemically controlled distribution pattern: Peregrinella was shown to have grown to much larger size at seeps with slow, diffusive fluid flow compared to sites with strong, advective fluid flow [38]. Because advective fluid flow releases more sulfide to the seabed than diffusive flow [146, 159], this pattern was interpreted as evidence that sulfide-rich seep sites were not ideal for Peregrinella and that bacterial, aerobic methane oxidation might have played a more prominent role in its nutrition [38]. That study used the abundance of early diagenetic fibrous cement in the seep limestone as a proxy for seepage intensity–with cement abundance positively correlated with seepage intensity [135]–and the authors pointed out that various other dimerelloids, including the very large Dzieduszyckia, lived at sites with very abundant seep cement (Anarhynchia even at an ancient hydrothermal vent site), and concluded that different dimerelloids might have had different feeding strategies [38].

Contrary to this claim, here we argue that seep-inhabiting dimerelloids in general relied on hydrocarbon-oxidizing bacteria for nutrition, rather than on sulfide oxidation. The presence of methane and oil in the water column results in rapid growth of bacterioplankton that takes advantage of these energy sources [162, 163]. We put forward the hypothesis that dimerelloids thrived by feeding on the abundant bacterioplankton at seeps where high amounts of hydrocarbon geofuels effused into bottom waters. To the best of our knowledge, there is no present-day example of a species at seeps with this feeding strategy. The closest modern analogs are probably certain species of stalked barnacles (Cirripedia) living at vents in the West Pacific Ocean [164] and near the Antarctic Peninsula [165], which are adapted to feeding on very fine particles such as bacteria and fine debris [164]. In the following, we go through all pre-Cretaceous (that is: pre-Peregrinella) instances of dimerelloids at hydrocarbon seeps to outline our arguments for (i) fluid composition and flow intensity at each site, and (ii) their implications for the dimerelloids’ preference for hydrocarbons over sulfide.

Cooperrhynchia

The Late Jurassic dimerelloid Cooperrhynchia is known from a single deposit only, were it is not superabundant but instead occurs in patches ([71] Sandy and Campbell, 1994; SK, own observation). The most common chemosymbiotic bivalve at this site is a solemyid [67], a group known to tolerate only low sulfide concentrations [159]. Similarly, the scarcity of 13C-depleted crocetane and the presence of 13C-depleted biphytane in the deposit with Cooperrhynchia [166] is typical of seep limestones that resulted from diffusive seepage [135], which would have come along with low sulfide concentrations close to the seabed.

Anarhynchia

This is the only dimerelloid genus yet known from both seeps and vents. An Early Jurassic seep deposit in northern British Columbia is dominated by Anarhynchia smithi and contains virtually no other fossils [18]. Despite the presence of early diagenetic fibrous cement, Anarhynchia smithi probably lived in a low-sulfide environment. It occurred during a geologic time interval known for its particularly low seawater sulfate concentration [167], which most likely resulted in reduced sulfide availability at seeps (cf. [9] Kiel, 2015; [145] Wortmann and Paytan, 2012) and hence also increased methane availability. Also of Early Jurassic age is a hydrothermal vent deposit in the Franciscan Complex in California, USA, at which Anarhynchia cf. gabbi is quite common [16, 168]. This occurrence at a hydrothermal vent site undoubtedly indicates that Anarhynchia was able to live at or near a strong sulfide source. But this does not necessarily contradict our hypothesis: hydrothermal vents are known to emit considerable amounts of methane, to the extent that for example the Rainbow, Snake Pit, and Logatchev vent sites on the Mid-Atlantic Ridge are inhabited by Bathymodiolus species hosting both thiotrophic and methanotrophic symbionts [169, 170].

Sulcirostra

Also of Early Jurassic age are seep deposits with Sulcirostra in eastern Oregon, USA; these are monospecific mass occurrences of Sulcirostra paronai that apparently lack bivalves and other fossils [17]. Analogously to the reasoning for the seep-inhabiting Anarhynchia above that lived in a low-sulfate ocean, we consider these occurrences low-sulfide environments. The great abundance of early diagenetic fibrous cement on the other hand is in accord with advective seepage, which is in favor of high sulfide production; but such production was necessarily still limited by the sulfate concentration of pore waters. Maybe even more interestingly, the Sulcirostra deposit contains pyrobitumen and its authigenic carbonate phases are only moderately 13C-depleted (δ13C values as low as –23.5‰), both agreeing with oil seepage [17].

Halorella

An argument for a preference for low-sulfide, diffusive seeps with abundant hydrocarbons in the bottom water analogous to that for Peregrinella can be made for the Triassic dimerelloid Halorella. In seep deposits in Oregon, Halorella occurs in rock-forming quantities, reaches almost 10 cm in size, and chemosymbiotic bivalves are rare or absent [15]. In contrast, in seep deposits in Turkey, Halorella is rare to common but never abundant, it never exceeds 45 mm in size, and it co-occurs with abundant inferred chemosymbiotic bivalves, including two species of Kalenteridae and one anomalodesmatan [21, 22]. Assuming that the abundant inferred chemosymbiotic bivalves relied on thiotrophy rather than methanotrophy, this indicates a stronger sulfide flux at the seeps with abundant bivalves compared to those without. Consequently, also Halorella appears to have preferred seeps with less sulfide and more methane or other hydrocarbons.

Ibergirhynchia

Early Carboniferous limestones with a mass occurrence of the dimerelloid Ibergirhynchia on top of a drowned atoll reef probably represent the most unusual Phanerozoic seep deposit reported to date [14]. Oil–as indicated by the presence of abundant pyrobitumen in the reef and seep limestones–passed through fissures of the Devonian atoll reef and fueled a chemosynthesis-based community on top of the reef. Migration of abundant oil through the Iberg reef apparently occurred in the latest early Carboniferous when the potential source rock, the Middle Devonian Wissenbach black shale, was in the oil window [171]. Due to the lack of a sedimentary cover, a large amount of the emitted geofuels necessarily entered the bottom water and consequently favored bacterioplankton growth, which, in turn, would have been suitable for the filter-feeding brachiopods.

Dzieduszyckia

The Moroccan deposit with Dzieduszyckia contains abundant early diagenetic fibrous cement [13]. If the seepage fluids had been dominated by methane, such a pattern would suggest a sulfide-rich environment; a context similar to that of the Sulcirostra deposits of eastern Oregon. However, the presence of pyrobitumen and trace metal patterns reveal that the Upper Devonian limestone with Dzieduszyckia represents an oil-seep deposit [13, 144]. At oil seeps, where both oil and accessory methane escape the seabed, these geofuels facilitate bacterioplankton growth [162, 163], resulting in conditions favorable for the colonization by dimerelloid brachiopods. The Middle Devonian Hollard Mound seep deposit is also typified by abundant early diagenetic fibrous cement [132], but contains a mass occurrence of modiomorphid bivalves (Ataviaconcha) instead of dimerelloids [19]. Unlike the Dzieduszyckia oil-seep deposit, thermogenic or abiogenic methane, deriving from the underlying volcaniclastics, have been inferred as dominant geofuels of the Hollard Mound seep [172, 173]. The patterns found for the Devonian seep deposits consequently agree with the hypothesized resource partitioning between hydrocarbon-dependent brachiopods and sulfide-dependent bivalves.

In summary, there are several lines of evidence suggesting that, unlike most bivalves, dimerelloid brachiopods at Paleozoic and Mesozoic seeps were dependent on hydrocarbon rather than sulfide oxidation. Although we have made a strong case for filter-feeding on bacterioplankton for dimerelloid brachiopods, we cannot exclude the possibility that dimerelloids hosted episymbiotic bacteria on the surface of the lophophor instead of feeding on bacterioplankton. However, we do not consider this further because (i) such adaptation is unknown from living brachiopods, (ii) it would be very difficult to proof based on fossil evidence, and (iii) it does not change or add much to our hypothesis. Like episymbiosis, endosymbiosis cannot be fully excluded either. A few animals with symbionts oxidizing short-chain alkanes are known [174]. Yet, because of the lack of features in the brachiopod bauplan that are essential for endosymbiosis in other groups of animals, we consider it unlikely that the seep-dwelling dimerelloids harbored chemosymbiotic bacteria in their soft tissue.

Perhaps contrary to the scenario proposed here might be the lack of brachiopod-dominated seeps during the mid-Cretaceous to early Eocene period of low marine sulfate concentrations [9, 145]. If our scenario is correct, this time interval should have been favorable for dimerelloid brachiopods at seeps. The only explanation we can offer is that dimerelloids went extinct in the Barremian with the disappearance of Peregrinella [38], so that simply no suitable brachiopods were around to take advantage of the methane-rich seeps. This hypothesis is based on the following lines of evidence:

the inclusion of the Cretaceous to present-day Cryptoporidae in the dimerelloids is questionable, so that Peregrinella is probably indeed the geologically youngest dimerelloid [175];

save for the Silurian Septatrypa, only dimerelloids have been able to dominate fossil seep sites, indicating that they possessed some pre-adaptation to successfully invade this habitat;

although other brachiopods, namely various terebratulids, have been found at fossil seeps [28, 33, 34, 37], they never formed mass occurrences like dimerelloids, and hence did not fill the same ecologic niche as dimerelloids;

the stratigraphic ranges of seep-inhabiting dimerelloids rarely overlap; this is particularly obvious for the three very large-sized genera Dzieduszyckia, Halorella, and Peregrinella, which are considered phylogenetically closely related ([28] Sandy, 2010, fig 9.6 therein) but are separated stratigraphically by 80 to 130 million years. This suggests that the genera discussed above represent repeated and temporarily very successful radiations into seep environments, which must be derived from as-yet unknown ‘ghost dimerelloids’ that may have been small and may have lived in cryptic or erosional settings (as suggested earlier for dimerelloids, cf. [176] Ager 1965).

Thus, the apparently only brachiopod lineage with the ability (or a trait) to colonize and to become a dominant member of vent and seep communities became extinct during the Early Cretaceous. This could explain why no brachiopod mass occurrences have been found at seeps during the theoretically favorable ‘low sulfate interval’ in the mid-Cretaceous to early Eocene. Furthermore, this also argues against the possibility that in the Cenozoic brachiopods were outcompeted at seeps by epifaunal bivalves or by bivalves with methanotrophic symbionts.

An analogous case of partitioning of resources instead of competition for them was recently made for Phanerozoic shallow-water brachiopods and bivalves in general [3]. This allows us to put forward the following scenario: resource partitioning controlled the evolutionary relationship between brachiopods and bivalves both in shallow marine habitats as well as at deep-water hydrocarbon seeps. But in seep environments, the animals were partitioning resources whose availability was controlled by fluid composition and flow intensity rather than by photosynthetic primary production, and hence the Phanerozoic diversity pattern of seep-dwelling animals differs from that of their shallow water relatives.

Conclusions

The diversity patterns of brachiopods and chemosymbiotic bivalves at seeps through the Phanerozoic indicate an interesting combination of evolutionary trajectories. The diversity of infaunal chemosymbiotic bivalves at seeps mirrors their diversity in shallow-marine environments, whereas epifaunal and semi-infaunal chemosymbiotic bivalves are unique to vent and seep ecosystems and are not found in shallow water. Brachiopod diversity at seeps is unlike the global shallow-marine trend, is unrelated to the diversity of seep-dwelling bivalves, and instead indicates long-term coexistence of the two clades. Therefore, bivalves and brachiopods have probably not been competing for the same resources but instead partitioned the food sources resulting from the two most common categories of geofuels in seepage fluids: (i) hydrogen sulfide and (ii) methane and oil-derived components. Chemosymbiotic bivalves mostly relied on sulfide-oxidizing symbionts for nutrition, for the brachiopods bacterial aerobic oxidation of methane and of other hydrocarbons played a more prominent role. The distribution and availability of hydrogen sulfide and methane at seeps is governed by geochemical gradients and ocean chemistry, which in turn should ultimately have controlled whether bivalves or brachiopods dominated hydrocarbon seeps, both in space and through geologic time.

7 Aug 2019

PONE-D-19-16788

Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: a hypothesis

PLOS ONE

Dear Prof. Peckmann,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

We would appreciate receiving your revised manuscript by Sep 21 2019 11:59PM. When you are ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter.

To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). This letter should be uploaded as separate file and labeled 'Response to Reviewers'.

A marked-up copy of your manuscript that highlights changes made to the original version. This file should be uploaded as separate file and labeled 'Revised Manuscript with Track Changes'.

An unmarked version of your revised paper without tracked changes. This file should be uploaded as separate file and labeled 'Manuscript'.

Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out.

We look forward to receiving your revised manuscript.

Kind regards,

Jürgen Kriwet

Academic Editor

PLOS ONE

Journal Requirements:

When submitting your revision, we need you to address these additional requirements.

Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at

http://www.journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and http://www.journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

Additional Editor Comments (if provided):

Dear authors,

This manuscript represents a very interesting study that has a lot of merits. Nevertheless, I would like to ask you to carefully address alll comments of the two reviewers.

Best wishes,

Jürgen

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: This is a review of manuscript „Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: a hypothesis” by Steffen Kiel and Joern Peckmann. The manuscript tackles and interesting topic of seemingly contrasting brachiopod and bivalve evolutionary histories at seeps throughout the Phanerozoic. The authors present an interesting hypothesis that bivalves and brachiopods utilized different resources, and that the contrasting evolutionary pathways are apparent rather than real. Authors present evidence to support this hypothesis, which makes the manuscript a quality work eligible for publication after a minor revision.

I have reviewed the previous version of this manuscript, where I have pointed several drawbacks in the reasoning, which were improved since then. The manuscript is properly referenced, although there are several important references missing, as I outline below. There are some minor drawbacks left to be corrected, outlined below.:

Line 40: please don’t get overly enthusiastic, it is difficult to judge what is most, and what is least extreme environment, it all depends on for whom; “…a similar pattern was also seen at deep-sea hydrothermal vents and hydrocarbon seeps” is enough

Line 182: we are unable to say whether they indeed have never developed methanotrophic symbioses, or they developed them only to have those symbioses extinct; better to write: Remarkable in this context is that other bivalve families with intracellular symbionts have not developed methanotrophic symbioses, or have not developed methanotrophic symbioses that would survive to the present day

Line 261-263: Phreagena kilmeri, rather than Archivesica kilmeri (check out vesicomyid taxonomy update paper by Krylova and Sahling (2010), PLoS one; line 262: C. pacifica, rather than P. pacifica

Line 308-309: Remove the sentence “Despite the presence of early diagenetic fibrous cement, Anarhynchia smithi probably lived in a low sulfide environment.” It doesn’t bring anything into the discussion, later you give some reasons why this might have been a low sulfide seep.

Line 332-333: There are two Greylock Butte seep deposits; one contains micrite, mass accumulations of Halorella up to 10 cm along longer axis, and no other fossils; the second Greylock Butte deposit contains somewhat rare Halorella up to 3-4 cm along longer axis, and some molluscs (anomalodesmatan and modiomorphid bivalves, among others); it is not true that both seep deposits in Oregon contain mass accumulations of Halorella, both are different, with second one being somewhat similar to Turkish deposit; please rewrite accordingly.

Line 350-351: remove “which, in turn, was suitable for the filter-feeding brachiopods”. Unnecessary.

Line 385-386: Eucalathis methanophila at Omagari occurs in some sort of monospecific brachiopod accumulations, although it doesn’t for such mass accumulations as dimerelloids did, please consider that; please add citation of Hryniewicz et al. (2019), describing another non-dimerelloid brachiopod from seep, Neoliothyrina nakremi

Another figure, with two schematic subfigures illustrating geochemical gradients and fauna at low-sulfide seeps with dimerelloids, and high sulfide seeps with bivalves, respectively, would be useful in this manuscript.

Table 1: clarify why you asterisk fossil genera erected after 1995 (presumably because after Campbell and Bottjer paper); you should asterisk also extant genera with fossil record erected after 1995 (they were unknown for Campbell and Bottjer, just as the fossil genera were)

Neogene:

Cubatea, rather than Cubathea, consider asterisking Elliptiolucina, Meganodontia according to my previous comments

Adulomya vs. Pleurophopsis: in your (SK) recent paper on Japanese Neogene vesis you consider Adulomya and Pleurophopsis as synonyms, with Pleurophopsis having priority. These seems to be true at least for Neogene species. Please be consistent here.

Samiolus from your 2017 paper (SK) paper on Miocene chemosymbiotic seep bivalves from Italy is missing – why? Also “Anodontia” from Ca’Fornace is missing (citation: Kiel et al. 2018), and Megaxinus from Stirone river (citation: Kiel and Taviani 2018), please complement the reference list and adjust fig. 1 according to missing genera

Paleogene:

Cubatea, not Cubathea

add Rhacothyas (citation: Hryniewicz et al. 2019), also Solemya species recorded there; adjust figure 1

Adulomya/Pleurophopsis problem again

Jurassic: Please note that there were 15 seep carbonates in Sassenfjorden area, with 3 of them Jurassic in age and the 8 Cretaceous (remainder not dated; details of stratigraphy in Wierzbowski et al. 2011, available from me on request). Therefore, putting all Sassenfjorden seep carbonates into Early Cretaceous category is an error. The significance of that is Solemya from one of the Jurassic seeps from Sassenfjorden, which is missing from your list and should be added (cite Hryniewicz et al. 2014, Zootaxa)

Table 2

be consistent and use “Fm” or “fm”; some of the terms used later are not lithostratigraphic in any way, but geographic (e.g. Beskidy Range, Musenalp, Wollaston Forland), therefore

Neogene: Ca’Fornace seep deposit missing (citation: Kiel et al. 2018)

Paleogene

Paleocene seep sites from Spitsbergen from Spitsbergen missing (citation: Hryniewicz et al. 2016, Palaeo3x, describing site, not fauna; do not cite 2019 paper here as it discusses the fauna)

Satsop Weatherwax seep deposit missing (citation: Hybertsen and Kiel, 2018, APP)

Late Cretaceous: separate Omagari lens and Yasukawa seep, these are two very different deposits

There are two Late Cretaceous seep deposits on Antarctic Peninsula; one on Seymour Island (Lopez de Bertodano Fm), one on Snow Hill Island (Snow Hill Island Formation), both are lumped into one here which is a mistake; worse, the deposit from Seymour Island is referred to as belonging to Snow Hill Island Formation, the seep-bearing lithologies of which do not even cropp out on Seymour Island; please correct that

Devonian

Regarding Sidi-Amar: in your 2007 paper you write about a limestone layer yielding Dzieduszyckia which was sampled, please include that next to “erratic limestone”; and “Devonian erratic limestones” does not look good as it suggest glacial erratics to most people, perhaps write “Devono-Carboniferous melange” or something like that

Despite numerous studies, I have seen the host lithological unit of Hollard Mound named just once, and that would be Pinacites limestone indeed (Peckmann et al. 1999); this is an informal unit, so small “l” and italics for Pinacites

Missing references:

Hryniewicz, K., Little, C.T.S., and Nakrem, H.A. 2014. Bivalves from the latest Jurassic–earliest Cretaceous hydrocarbon seep carbonates from Spitsbergen, Svalbard. Zootaxa 3859: 1–66.

Hryniewicz, K., Bitner, M.A., Durska, E., Hagström, J., Hjálmársdottir H.R., Jenkins, R.G., Little, C.T.S., Miyajima, Y., Nakrem, H.A., and Kaim, A. 2016. Paleocene methane seep and wood-fall marine environments from Spitsbergen, Svalbard. Palaeogeography, Palaeoclimatology,Palaeoecology 462: 41–56.

Hryniewicz, K., Amano, A., Bitner, M.A., Hagström, J., Kiel, S., Klompmaker, A.A., Mörs, T., Robins, C.M., and Kaim, A. 2019. A late Paleocene fauna from shallow-water chemosynthesis-based ecosystems, Spitsbergen, Svalbard. Acta Palaeontologica Polonica 64 (1): 101–141.

Hybertsen, F. and Kiel, S. 2018. A middle Eocene seep deposit with silicified fauna from the Humptulips Formation in western Washington State, USA. Acta Palaeontologica Polonica 63 (4): 751–768.

Kiel, S., Taviani, M. 2017. Chemosymbiotic bivalves from Miocene methane seep carbonates in Italy. Journal of Paleontology 91, 444–466.

Kiel, S. and Taviani, M. 2018. Chemosymbiotic bivalves from the late Pliocene Stirone River hydrocarbon seep complex in northern Italy. Acta Palaeontologica Polonica 63 (3): 557–568.

Kiel, S., Sami, M., and Taviani, M. 2018. A serpulid-Anodontia-dominated methane-seep deposit from the Miocene ofnorthern Italy. Acta Palaeontologica Polonica 63 (3): 569–577.

Krzysztof Hryniewicz

Reviewer #2: To authors

It is challenging paper which try to answer to one of the most interesting issue on faunal change in seep environment through the Phanerozoic; brachiopods vs bivalves in seeps.

Although your hypothesis, seep obligate dimerelloid brachiopods had mainly consumed methanotrophic and/or hydrocarbon-consuming bacteria, is seemed to established upon many assumptions, I think the idea based on you detailed review on the current our knowledge is fair. The paper would be a starting point to make better understanding of on brachiopods vs bivalves in seeps. Followings are minor point to be revised.

Minor points:

l. 72-76: Although I know authors stated in the discussion parts, it would be better to mention about non-dimerelloid brachiopod, e.g. terebratulide Eucalathis, occurrences in seep.

l. 238-240: Authors mentioned that the seep dwelling brachiopods disappeared after the Early Cretaceous, however, there are several occurrences of terebratulide brachiopods in Late Cretaceous and Cenozoic seeps. May be authors think those terebratulide brachiopods are not seep obligate group, author should state their thinking with reasonable reason before this sentence.

l. 262: not P. pacifica, C. pacifica

l. 287-290: So, do you think the dimerelloid brachiopods fed on free living hydrocarbon-consuming microbes only? Don’t you think they have epi-symbiotic bacteria on the surface of lophophor? Why you can exclude this possibility? Please state.

It is also better to argue or state the internal morphology of dimerelloid compared to other brachiopods. If they have special features, please state.

Table 1: I couldn’t understand why author put Conchocele bivalves as “semi-infauna.” I know they sometimes lived on the sea floor, like in Sea of Okhotsk, but in most cases they lived within sediments, beneath the sea floor. So, it shout be categorized into “infauna”.

l. 374-379: It is just comment. As authors already noted, it is big contrary that the dimerelloids couldn’t flourished in low sulfate concentration period, L. Cretaceous.

l. 778: delete “pdf ed.”

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Krzysztof Hryniewicz

Reviewer #2: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email us at figures@plos.org. Please note that Supporting Information files do not need this step.

Submitted filename: Kiel_Peckmann_2019_review.docx

Click here for additional data file.

14 Aug 2019

Note that the color code of the response letter will not show in this box.

PONE-D-19-16788

Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: a hypothesis

Comments to the Author

Reviewer #1: This is a review of manuscript „Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: a hypothesis” by Steffen Kiel and Joern Peckmann. The manuscript tackles and interesting topic of seemingly contrasting brachiopod and bivalve evolutionary histories at seeps throughout the Phanerozoic. The authors present an interesting hypothesis that bivalves and brachiopods utilized different resources, and that the contrasting evolutionary pathways are apparent rather than real. Authors present evidence to support this hypothesis, which makes the manuscript a quality work eligible for publication after a minor revision.

I have reviewed the previous version of this manuscript, where I have pointed several drawbacks in the reasoning, which were improved since then. The manuscript is properly referenced, although there are several important references missing, as I outline below. There are some minor drawbacks left to be corrected, outlined below.:

Line 40: please don’t get overly enthusiastic, it is difficult to judge what is most, and what is least extreme environment, it all depends on for whom; “…a similar pattern was also seen at deep-sea hydrothermal vents and hydrocarbon seeps” is enough

Reply: Point taken; we have changed wording accordingly.

Line 182: we are unable to say whether they indeed have never developed methanotrophic symbioses, or they developed them only to have those symbioses extinct; better to write: Remarkable in this context is that other bivalve families with intracellular symbionts have not developed methanotrophic symbioses, or have not developed methanotrophic symbioses that would survive to the present day

Reply: A fair comment, but also a bit of a nit-picking comment. Since there is no point in discussing this is detail, we have changed “other families with intracellular symbionts have never developed methanotrophic symbiosis” to “other families with intracellular symbionts have apparently not developed methanotrophic symbiosis “.

Line 261-263: Phreagena kilmeri, rather than Archivesica kilmeri (check out vesicomyid taxonomy update paper by Krylova and Sahling (2010), PLoS one; line 262: C. pacifica, rather than P. pacifica

Reply: The species assigned by Krylova and co-workers to Phreagena have not been retrieved as a monophyletic group in any molecular analysis of the vesicomyids; Archivesica is used here in the sense of Kiel (2016, Proc. Royal Society B 283: 2016233). Corrected ‘P. pacifica’

Line 308-309: Remove the sentence “Despite the presence of early diagenetic fibrous cement, Anarhynchia smithi probably lived in a low sulfide environment.” It doesn’t bring anything into the discussion, later you give some reasons why this might have been a low sulfide seep.

Reply: We disagree. Omitting this information may come along with the impression that we have ignored evidence that is not in favor of our interpretation. Although the evidence detailed here (abundant fibrous cement) may argue for a high sulfide environment, there is other evidence – and we think this is stronger evidence – in favor of a low sulfide environment, which is detailed in the main text. For the sake of good scientific practice, we prefer to keep on mentioning evidence not in favor of our overall interpretation.

Line 332-333: There are two Greylock Butte seep deposits; one contains micrite, mass accumulations of Halorella up to 10 cm along longer axis, and no other fossils; the second Greylock Butte deposit contains somewhat rare Halorella up to 3-4 cm along longer axis, and some molluscs (anomalodesmatan and modiomorphid bivalves, among others); it is not true that both seep deposits in Oregon contain mass accumulations of Halorella, both are different, with second one being somewhat similar to Turkish deposit; please rewrite accordingly.

Reply: The differences between the two Graylock Butte outcrops as outlined by the reviewer may indeed exists, however, based on our own field experience we cannot exclude that the Graylock Butte 1 and 2 deposits are only one deposit in reality. The large deposits are only approx. 200 m apart in outcrop, but may be connected in the subsurface. Bivalves were only found in the Graylock Butte 2 deposit by us, but only at one meter-scale spot at its margin (Peckmann et al. 2011). We cannot exclude that similar accessory fossil assemblages occur within the large Graylock Butte 1 deposit (70 m in width) that are not exposed in outcrop. It is certainly NOT correct, however, that the second Graylock Butte deposit is more similar to some of the Turkish deposits (described in Kiel et al. 2017) than to the first Graylock Butte deposit. Therefore, we prefer not to make a case for facies differentiation among the Graylock Butte deposits. Anyway, even if we would make such a case, it would be in favor of our hypothesis: large brachiopods and lack of bivalves coincides with high methane/low sulfide for Graylock Butte 1, whereas somewhat smaller (?) but certainly fewer brachiopods and the very few bivalves coincide with less methane/higher sulfide flux for Graylock Butte 2.

Line 350-351: remove “which, in turn, was suitable for the filter-feeding brachiopods”. Unnecessary.

Reply: We feel that this clarification is of use. The reviewer is a leading expert of the research topic, but not every reader will be equally familiar with the topic. Anyway, we toned down wording to avoid the impression that we use this statement as an argument and not for clarification. This, indeed, would be circular reasoning. We have changed “was suitable” to “would have been suitable”.

Line 385-386: Eucalathis methanophila at Omagari occurs in some sort of monospecific brachiopod accumulations, although it doesn’t for such mass accumulations as dimerelloids did, please consider that; please add citation of Hryniewicz et al. (2019), describing another non-dimerelloid brachiopod from seep, Neoliothyrina nakremi

Reply: Eucalathis methanophila occurs in small numbers among a mass accumulation of small and diverse gastropods at the Omagari site. This does not resemble in any way the mass accumulations of dimerelloids – and should never have been called a ‘monospecific assemblage’ in the title of that paper in the first place. The citation was added.

Another figure, with two schematic subfigures illustrating geochemical gradients and fauna at low-sulfide seeps with dimerelloids, and high sulfide seeps with bivalves, respectively, would be useful in this manuscript.

Reply: We see the point and had thought about such a figure ourselves. In the end, we had opted against such schematic figure because there are not two simple end-member systems; too many factors impact the modes of seepage at the different sites discussed in the manuscript. We are afraid that we are not yet at a point, where we are able to include all steering mechanisms in a simple sketch.

Table 1: clarify why you asterisk fossil genera erected after 1995 (presumably because after Campbell and Bottjer paper); you should asterisk also extant genera with fossil record erected after 1995 (they were unknown for Campbell and Bottjer, just as the fossil genera were)

Reply: This was indeed insufficiently explained. In the discussion section we compare the number of newly described seep brachiopods genera since Mike Sandy’s (1995) review to the number of new seep-inhabiting bivalve genera described since the same year. We made this clearer in the discussion (lines 244 to 247 in the revised ms) and in the table caption. Per suggestion of the reviewer, we now also mark the new genera based on living species (Elliptiolucina, Meganodontia etc.), as well as the one new dimerelloid genus since 1995 (Ibergirhynchia). We have also adjusted the numbers in the text (line 246 in the revised ms).

Neogene:

Cubatea, rather than Cubathea, consider asterisking Elliptiolucina, Meganodontia according to my previous comments

Reply: Thanks for spotting the typo in Cubatea; see also previous comment.

Adulomya vs. Pleurophopsis: in your (SK) recent paper on Japanese Neogene vesis you consider Adulomya and Pleurophopsis as synonyms, with Pleurophopsis having priority. These seems to be true at least for Neogene species. Please be consistent here.

Reply: Thanks for spotting this; we removed Adulomya from the list.

Samiolus from your 2017 paper (SK) paper on Miocene chemosymbiotic seep bivalves from Italy is missing – why? Also “Anodontia” from Ca’Fornace is missing (citation: Kiel et al. 2018), and Megaxinus from Stirone river (citation: Kiel and Taviani 2018), please complement the reference list and adjust fig. 1 according to missing genera

Reply: Samiolus was not considered as a bathymodiolin by Kiel & Taviani, just as a mytilid. Hence it does not qualify as ‘chemosymbiotic bivalve’ and is consequently not included in this list. Anodontia and Megaxinus were added to the list.

Paleogene:

Cubatea, not Cubathea

add Rhacothyas (citation: Hryniewicz et al. 2019), also Solemya species recorded there; adjust figure 1

Reply: Rhacothyas was added to the list; Solemya was already in the list

Adulomya/Pleurophopsis problem again

Reply: Adulomya was removed.

Jurassic: Please note that there were 15 seep carbonates in Sassenfjorden area, with 3 of them Jurassic in age and the 8 Cretaceous (remainder not dated; details of stratigraphy in Wierzbowski et al. 2011, available from me on request). Therefore, putting all Sassenfjorden seep carbonates into Early Cretaceous category is an error. The significance of that is Solemya from one of the Jurassic seeps from Sassenfjorden, which is missing from your list and should be added (cite Hryniewicz et al. 2014, Zootaxa)

Reply: Sassenfjorden was added to the list of Jurassic sites/rock units and Solemya was added to the list of Jurassic infaunal bivalves. Thanks for correcting this.

Table 2

be consistent and use “Fm” or “fm”; some of the terms used later are not lithostratigraphic in any way, but geographic (e.g. Beskidy Range, Musenalp, Wollaston Forland), therefore

Reply: We replaced the one instance of “fm” by “Fm”.

Neogene: Ca’Fornace seep deposit missing (citation: Kiel et al. 2018)

Reply: It is not the intention of this table to list all seep deposits, but just the seep-bearing rock units. This is clearly stated in the table caption. Furthermore, the Ca’Fornace limestone was found float and its exact provenance is unclear (Kiel et al. 2018).

Paleogene

Paleocene seep sites from Spitsbergen from Spitsbergen missing (citation: Hryniewicz et al. 2016, Palaeo3x, describing site, not fauna; do not cite 2019 paper here as it discusses the fauna)

Reply: added

Satsop Weatherwax seep deposit missing (citation: Hybertsen and Kiel, 2018, APP)

Reply: As above, the seep-bearing rock unit (Humptulips Fm.) is already in the list.

Late Cretaceous: separate Omagari lens and Yasukawa seep, these are two very different deposits

Reply: They are from the same rock unit; no point in separating them here.

There are two Late Cretaceous seep deposits on Antarctic Peninsula; one on Seymour Island (Lopez de Bertodano Fm), one on Snow Hill Island (Snow Hill Island Formation), both are lumped into one here which is a mistake; worse, the deposit from Seymour Island is referred to as belonging to Snow Hill Island Formation, the seep-bearing lithologies of which do not even cropp out on Seymour Island; please correct that

Reply: corrected and number on figure 1 adjusted; note that we also changed the word ‘Formations’ in both the legend and the caption of the X-axis to ‘rock units’.

Devonian

Regarding Sidi-Amar: in your 2007 paper you write about a limestone layer yielding Dzieduszyckia which was sampled, please include that next to “erratic limestone”; and “Devonian erratic limestones” does not look good as it suggest glacial erratics to most people, perhaps write “Devono-Carboniferous melange” or something like that

Reply: changed to ‘Devonian-Carboniferous mélange’

Despite numerous studies, I have seen the host lithological unit of Hollard Mound named just once, and that would be Pinacites limestone indeed (Peckmann et al. 1999); this is an informal unit, so small “l” and italics for Pinacites

Reply: accepted

Missing references:

Hryniewicz, K., Little, C.T.S., and Nakrem, H.A. 2014. Bivalves from the latest Jurassic–earliest Cretaceous hydrocarbon seep carbonates from Spitsbergen, Svalbard. Zootaxa 3859: 1–66.

Hryniewicz, K., Bitner, M.A., Durska, E., Hagström, J., Hjálmársdottir H.R., Jenkins, R.G., Little, C.T.S., Miyajima, Y., Nakrem, H.A., and Kaim, A. 2016. Paleocene methane seep and wood-fall marine environments from Spitsbergen, Svalbard. Palaeogeography, Palaeoclimatology,Palaeoecology 462: 41–56.

Hryniewicz, K., Amano, A., Bitner, M.A., Hagström, J., Kiel, S., Klompmaker, A.A., Mörs, T., Robins, C.M., and Kaim, A. 2019. A late Paleocene fauna from shallow-water chemosynthesis-based ecosystems, Spitsbergen, Svalbard. Acta Palaeontologica Polonica 64 (1): 101–141.

Hybertsen, F. and Kiel, S. 2018. A middle Eocene seep deposit with silicified fauna from the Humptulips Formation in western Washington State, USA. Acta Palaeontologica Polonica 63 (4): 751–768.

Kiel, S., Taviani, M. 2017. Chemosymbiotic bivalves from Miocene methane seep carbonates in Italy. Journal of Paleontology 91, 444–466.

Kiel, S. and Taviani, M. 2018. Chemosymbiotic bivalves from the late Pliocene Stirone River hydrocarbon seep complex in northern Italy. Acta Palaeontologica Polonica 63 (3): 557–568.

Kiel, S., Sami, M., and Taviani, M. 2018. A serpulid-Anodontia-dominated methane-seep deposit from the Miocene ofnorthern Italy. Acta Palaeontologica Polonica 63 (3): 569–577.

Reply: all appropriate references were added

Krzysztof Hryniewicz

Reviewer #2: It is challenging paper which try to answer to one of the most interesting issue on faunal change in seep environment through the Phanerozoic; brachiopods vs bivalves in seeps. Although your hypothesis, seep obligate dimerelloid brachiopods had mainly consumed methanotrophic and/or hydrocarbon-consuming bacteria, is seemed to established upon many assumptions, I think the idea based on you detailed review on the current our knowledge is fair. The paper would be a starting point to make better understanding of on brachiopods vs bivalves in seeps. Followings are minor point to be revised.

Minor points:

l. 72-76: Although I know authors stated in the discussion parts, it would be better to mention about non-dimerelloid brachiopod, e.g. terebratulide Eucalathis, occurrences in seep.

Reply: Point taken. We now refer to the publications on terebratulides at seeps. The following addition (bold letters) was made to the text:

Among brachiopods, only dimerelloid genera reported from geochemically confirmed seep deposits are included because (i) with a single exception (see below), only dimerelloids occurred at ancient seeps in rock-forming quantities; all other brachiopods reported from ancient seeps (including various terebratulids, i.e. [33-36]) represent minor faunal elements that most likely took advantage of exposed hard substrate [28], …

l. 238-240: Authors mentioned that the seep dwelling brachiopods disappeared after the Early Cretaceous, however, there are several occurrences of terebratulide brachiopods in Late Cretaceous and Cenozoic seeps. May be authors think those terebratulide brachiopods are not seep obligate group, author should state their thinking with reasonable reason before this sentence.

Reply: We have replaced “Seep-dwelling brachiopods” by “Seep-dwelling dimerelloids”.

l. 262: not P. pacifica, C. pacifica

Reply: corrected

l. 287-290: So, do you think the dimerelloid brachiopods fed on free living hydrocarbon-consuming microbes only? Don’t you think they have epi-symbiotic bacteria on the surface of lophophor? Why you can exclude this possibility? Please state.

Reply: A fair comment that is consistent with our hypothesis. We have added the following statement (lines 368 to 372): “ … we cannot exclude the possibility that dimerelloids hosted episymbiotic bacteria on the surface of the lophophor instead of feeding on bacterioplankton. However, we do not consider this further because (i) such adaptation is unknown from living brachiopods, (ii) it would be very difficult to proof based on fossil evidence, and (iii) it does not change or add much to our hypothesis.”

It is also better to argue or state the internal morphology of dimerelloid compared to other brachiopods. If they have special features, please state.

Reply: The first author (SK) has discussed this matter with several brachiopod specialists. Their view is that although many dimerelloids have rather long crurae (lophophor support structures), the length of the crurae does not allow any conclusions on the length of the lophophor itself. Hence we refrain from speculating about this matter.

Table 1: I couldn’t understand why author put Conchocele bivalves as “semi-infauna.” I know they sometimes lived on the sea floor, like in Sea of Okhotsk, but in most cases they lived within sediments, beneath the sea floor. So, it shout be categorized into “infauna”.

Reply: To our knowledge, the only actual observations on the mode of life of Conchocele come from the Sea of Okhotsk, where they were semi-infaunal. Hence we follow this view (as done in a previous assessment of epifaunal/infaunal trends among seep bivalves by Kiel 2015, Proc. Roy. Soc. B, 282: 20142908).

l. 374-379: It is just comment. As authors already noted, it is big contrary that the dimerelloids couldn’t flourished in low sulfate concentration period, L. Cretaceous.

Reply: This is correct. We do discuss this relationship in detail in the lines below (lines 380 to 394, submitted version; lines 383 to 397, revised version).

l. 778: delete “pdf ed.”

Reply: We thank the reviewer for spotting this typo. It has been corrected.

Submitted filename: Response to reviewers.docx

Click here for additional data file.

19 Aug 2019

Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: a hypothesis

PONE-D-19-16788R1

Dear Dr. Peckmann,

We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements.

Within one week, you will receive an e-mail containing information on the amendments required prior to publication. When all required modifications have been addressed, you will receive a formal acceptance letter and your manuscript will proceed to our production department and be scheduled for publication.

Shortly after the formal acceptance letter is sent, an invoice for payment will follow. To ensure an efficient production and billing process, please log into Editorial Manager at https://www.editorialmanager.com/pone/, click the "Update My Information" link at the top of the page, and update your user information. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, you must inform our press team as soon as possible and no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

With kind regards,

Jürgen Kriwet

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Dear authors,

Thank you for considering all comments and suggestions by the reviewers and also to provide apmple arguments where you did not follow the reviewer's suggestions. I agreen with all your comments and arguments and thus consider your manuscript acceptal for publication in Plos One in its current form.

Kind regards,

Jürgen Kriwet

Reviewers' comments:

27 Aug 2019

PONE-D-19-16788R1

Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: a hypothesis

Dear Dr. Peckmann:

I am pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please notify them about your upcoming paper at this point, to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

For any other questions or concerns, please email plosone@plos.org.

Thank you for submitting your work to PLOS ONE.

With kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Jürgen Kriwet

Academic Editor

PLOS ONE