A nearly complete respiratory, circulatory, and excretory system preserved in small Late Cretaceous...

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Paläontologische ZeitschriftScientific Contributions toPalaeontology ISSN 0031-0220 Paläontol ZDOI 10.1007/s12542-015-0256-6

A nearly complete respiratory, circulatory,and excretory system preserved in smallLate Cretaceous octopods (Cephalopoda)from Lebanon

Dirk Fuchs, Philipp R. Wilby, Sigurdvon Boletzky, Pierre Abi-Saad, HelmutKeupp & Yasuhiro Iba

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RESEARCH PAPER

A nearly complete respiratory, circulatory, and excretory systempreserved in small Late Cretaceous octopods (Cephalopoda)from Lebanon

Dirk Fuchs • Philipp R. Wilby • Sigurd von Boletzky •

Pierre Abi-Saad • Helmut Keupp • Yasuhiro Iba

Received: 9 November 2014 / Accepted: 3 February 2015

� Palaontologische Gesellschaft 2015

Abstract Although they are rare, fossilized gills are well

known in Mesozoic coleoid cephalopods. In the Late

Jurassic Solnhofen (South Germany) and Late Cretaceous

Hakel and Hadjoula (Lebanon) plattenkalks, the feather-like

gill remains are usually preserved as a yellowish staining.

Small coleoids from Hakel—tentatively determined as oc-

topods—attracted our attention because these stains occur

throughout the entire mantle sac in an unusual symmetrical

pattern. Actualistic comparisons point to a compound of

diverse vascular structures that most likely reflect central

parts of the venous blood system (afferent branchial vessels,

branchial hearts, vena pallialis, blood sinus) as well as the

nephridial sacs. The nephridial sacs are clearly separated,

which confirms the octopod nature of the fossils. A

reticulated staining pattern in the rear of the mantle, which

may reflect the gonad capillary system, suggests the pres-

ence of mature small-sized octopods. Based on its colour, its

amorphous habit, and energy-dispersive X-ray spectroscopy

(EDX) elemental analyses, the major components of the

coelomic cavities have been replicated by an iron-rich phase

(presumably goethite; copper was not detected). The goe-

thite does not replace the tissues; rather, it traces their gross

form as a well-defined ‘‘stain’’. It is assumed the goethite is

secondary after pyrite, which precipitated as a consequence

of the oxygen-binding capacity of the copper-bearing

haemocyanin and its ability to locally regulate redox po-

tentials immediately postmortem.

Keywords Octopoda � Coleoidea � Cenomanian � Soft

tissue preservation � Respiratory � Circulatory � Excretory

system

Kurzfassung Fossilisierte Kiemen bei mesozoischen

coleoiden Cephalopoden sind trotz allgemeiner Seltenheit

gut bekannt. Die federformigen Kiemenreste sind in den

spatjurassischen und spatkretazischen Plattenkalken von

Solnhofen (Suddeutschland) und Hakel und Hadjoula

(Lebanon) ublicherweise als gelblich verfarbte Strukturen

erhalten. Kleine Coleoiden aus Hakel—provisorisch als

Octopoden bestimmt—erweckten unser Interesse, weil die

Verfarbungen auf ungewohnliche Weise symmetrisch uber

den ganzen Mantelsack verteilt sind. Aktualistische

Vergleiche deuten darauf hin, dass es sich hierbei um einen

Verbund aus diversen vaskularen Strukturen handelt, die

sehr wahrscheinlich zentrale Teile des venosen Blutsystems

(afferente Kiemengefaße, Kiemenherze, Vena pallialis,

Blutsinus) und der Nephridialsacke widerspiegeln. Die klar

voneinander getrennten Nephridialsacke bestatigen, dass es

sich tatsachlich um Octopoden handelt. Ein retikulares

D. Fuchs (&) � Y. Iba

Earth and Planetary System Science, Department of Natural

History Sciences, Hokkaido University, Sapporo, Japan

e-mail: [email protected]

Y. Iba


P. R. Wilby

British Geological Survey, Nottingham, UK


S. von Boletzky

CNRS, Laboratoire Arago, 66650 Banyul-sur-Mer, France


P. Abi-Saad

Memoire de Temps, Citadel Area, Byblos (Jbeil), Lebanon


H. Keupp

Institute of Geological Sciences, Freie Universitat Berlin,

Berlin, Germany


123

Palaontol Z

DOI 10.1007/s12542-015-0256-6

Author's personal copy

Farbmuster im hinteren Mantelsackbereich konnte das

Kapillarsystem der Gonaden darstellen, was darauf hindeuten

wurde, dass es sich hierbei um geschlechtsreife,

kleinwuchsige Octopoden handelt. In Anbetracht von

Farbe, amorphem Habitus und EDX-Analysen wurden

die Hauptkomponenten der Coelomhohlen durch eine

eisenreiche Phase (vermutlich Goethit; Kupfer wurde nicht

nachgewiesen) repliziert. Der Goethit ersetzte dabei nicht

die Gewebe, sondern zeichnet vielmehr ihre Formen als

klar umrissene Farbungen grob nach. Es wird vermutet,

dass primar die Ausfallung von Pyrit eine Folge der

Sauerstoffbindungskapazitat von kupferbasierten Hamcyanin

und dessen Fahigkeit ist, sofort nach dem Tod lokale

Redoxpotentiale zu regulieren.

Schlusselworter Octopoda � Coleoidea � Cenomanium �Weichteilerhaltung � Atmungs � Zirkulations � Exkretions

system

Introduction

Among invertebrates, cephalopods are unique in having a

closed high-pressure blood system (Wells 1983, 2011;

Nesis 1987; Nixon 2010). In coleoid cephalopods, one

median systemic heart and two branchial hearts drive this

highly effective circulatory system, which can be consid-

ered a remarkable convergence with vertebrates. Normally,

anterior and posterior aortas starting from the systematic

heart supply the body with oxygenated blood, and venous

vessels bring the deoxygenated blood from the periphery

back to the paired gills via the branchial hearts (Nautilus

possesses two pairs of gills with branchial heart-like pul-

sating vessels). In addition to the main veins, venous blood

also returns in large blood spaces, so-called blood sinuses.

The copper-based blood pigment haemocyanin is produced

(in coleoids) in the branchial glands (Budelmann et al.

1997). The excretory system generally includes the

nephridial (renal) sacs, branchial heart appendages, and

nephridial appendages of the vena cava.

Although the preservation of muscular tissues is widely

known in the endocochleate coleoids (e.g. Naef 1922;

Briggs et al. 1993; Kear et al. 1995; Wilby et al. 1996,

2004, 2008; Fuchs 2006), fossil conservation of thin-walled

epithelia such as those of a vascular system is surprising.

However, fossil evidence of the respiratory, circulatory,

and reproductive system is not new in coleoids. Sper-

matophores were recently observed by Keupp et al. (2010),

and fossil evidence of coleoid gills has been known since

Klinghardt (1932). Today, numerous records of preserved

gills from various subgroups and stratigraphic levels have

been created (Table 1). From the study presented by

Bandel and Leich (1986), we know that Late Jurassic

coleoids were dibranchiates. Reitner and Mehl (1989) de-

scribed a single pair of gills in a belemnoid from the Early

Jurassic (Toarcian) Posidonia Shales of South Germany

(reviewed by Mehl 1990; Reitner 2009). Klinghardt (1932:

pl. 6, Fig. 7), Bandel and Leich (1986) and Mehl (1990)

found gills in the octobrachian Plesioteuthis from the Late

Jurassic (Tithonian) Solnhofen plattenkalks in South Ger-

many (reviewed by Haas 2002). Fuchs et al. (2009) and

Fuchs and Larson (2011a, b) studied gills in gladius-bear-

ing and gladius-less octobrachians from the Late Creta-

ceous (Cenomanian–Santonian) plattenkalks of Lebanon,

which for coleoids represent the most significant Creta-

ceous Konservat-Lagerstatten (e.g., Dalla Vecchia 2004;

Fuchs 2007, and references therein).

In plattenkalks, the shape of gills is mostly conserved as

a yellowish staining (Fuchs et al. 2009; Fuchs and Larson

2011a, b), in contrast to those of the belemnoid gills from

the Early Jurassic Posidonia Shales, which are preserved in

apatite (Mehl 1990, p. 78; Reitner 2009). In common with

Mehl (1990), Reitner (2009), Fuchs and Larson (2011a, b)

presumed that the feather-like remains represent the carti-

laginous gill skeleton. Yellow-stained structures are also

known to occur in close association with the eye capsules

(Fuchs and Larson 2011a), where they are strongly bran-

ched and likely represent networks of capillaries. Previ-

ously, Riegraf (1987, p. 266) reported imprints of blood

vessels on petrified ink of Jurassic coleoids.

Table 1 Records of gill remains in Mesozoic coleoids

Taxon Affiliation Stratigraphic age References

Glyphiteuthis libanotica Teudopseina (Octobrachia) Cenomanian Fuchs and Larson (2011a)

Glyphiteuthis abisaadiorum Teudopseina (Octobrachia) Cenomanian Fuchs and Larson (2011a)

Rachiteuthis donovani Teudopseina (Octobrachia) Cenomanian Fuchs and Larson (2011a)

Keuppia levante Octopoda (Octobrachia) Cenomanian Fuchs et al. (2009)

Dorateuthis syriaca Prototeuthina (Octobrachia) Cenomanian Fuchs and Larson (2011b)

Plesioteuthis prisca Prototeuthina (Octobrachia) Tithonian Klinghardt (1932), Bandel and Leich (1986),

Mehl (1990) and Haas (2002)

Clarkeiteuthis conocauda Diplobelida (‘‘Belemnoidea’’) Toarcian Reitner and Mehl (1989, 2009)

D. Fuchs et al.

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New specimens from the Late Cretaceous plattenkalks

of Hadjoula (Lebanon) that are dominated by yellowish-

stained areas have confirmed the potential preservation of

vascular systems. It is the aim of the present paper to de-

scribe and to discuss this staining pattern.

Material

Nine specimens were available for our study. All of them

came from the early Late Cenomanian plattenkalks of

Hadjoula (Metoicoceras geslinianum zone). Specimens

BSPG MC138a?b, 139a?b, 140a?b, 147a?b, 148, 149,

and 150 are deposited at Bayerische Staatssammlung

Munchen (collection H. Keupp), whereas the remaining

two specimens belong to the collection of Ru Smith

(Houston, Texas, USA). Access to the latter two specimens

has been guaranteed; nevertheless, high-quality photo-

graphic documentation will be deposited at Bayerische

Staatssammlung Munchen.

Specimen MC-140a has been used for EDX analyses

(Oxford Instruments EDX system, INCA software).

The dorsoventrally embedded specimens are determined

as Octopoda incertae sedis, since there is no evidence of a

gladius (Fig. 1). Given their small size (mantle length max.

20 mm), these specimens may represent juveniles. How-

ever, in light of the small-sized forms in extant octopods

(and other coleoids), we cannot exclude the possibility that

we are dealing with small adults.

Description

Although all specimens show a similar bilaterally sym-

metrical staining pattern, it is most clearly demonstrated

in a specimen from the Smith collection (Figs. 1a, 2a, b).

This specimen shows the mantle sac (mantle length

20 mm) and eight outspread arms. The ink sac, as well as

its duct, is situated in the centre of the stained structures.

On either side of the ink sac, there is a longitudinal axis

with a series of faint inner and outer branches (lengths

max. 1 mm). Outer branches are more distinct than inner

branches. Posterior to the ink sac, a pair of triangular

structures (basis length 5 mm) is present. Both triangles

are flanked on either side by circular stained structures

(diameter 1.5–2 mm). The left of this pair is laterally

adjoining a 3.3 mm-long structure that runs in an ante-

rior–posterior direction along the lateral mantle outline.

Anterior to the ink sac, a comparatively wide medial

stain (max. width 1.2 mm) runs from anterior to poste-

rior. The posteriormost area of yellow staining is circular

in outline (diameter 2.2 mm) and appears to be

reticulated (Fig. 2a).

Discussion

The repeated occurrence of paired structures in the studied

specimens suggests that these structures are not preserva-

tional artefacts. The assumption of preserved internal or-

gans is therefore preferable. Paired feather-like structures

in the lateral mantle occurs often in coleoids from the

Lebanon plattenkalks and have regularly been interpreted

as gills (Fuchs et al. 2009; Fuchs and Larson 2011a, b). The

remaining stained structures described above are hitherto

unknown. Their preservation and relative positions to the

respiratory gills point to the circulatory and excretory

system. They do not resemble the digestive system, which

in coleoids is mainly muscular, with a cuticular lining, and

is typically preserved differently (see Roger 1946; Fuchs

et al. 2009; Fuchs and Larson 2011a, b).

Based on the interpretation of paired gills in the lateral

mantle, the following conclusions can be drawn: The cir-

cular stains on either side of the gill bases likely represent

the branchial hearts. The anterior and posterior stained

structures branching off from the left branchial heart can

then be tentatively determined as the ramus stellaris and

ramus superior of the vena pallialis in which the blood

flows back to the branchial heart on either side (Boletzky

1968). The medial broad staining running in an anterior–

posterior direction corresponds to the position of venous

blood sinuses, which are known to surround the gut in

incirrate octopods (Wells 1983, p. 244, Fig. 5). The pos-

terior reticulated stains may represent the gonad capillary

system. If this is true, it clearly pleads against the idea that

we are looking at premature juveniles. Many parts of the

latter tissues appear to be overlain by comparatively large

triangles whose positions are suggestive of the paired

nephridial sacs. According to Young and Vecchione (1996,

p. 99), the voluminous nephridial sacs are separated in

octobrachians, whereas they are fused (unpaired) in de-

cabrachians. In our material, the presence of the large

blood sinus around the gut as well as the separated

nephridial sacs supports our tentative identification as oc-

topods. The fact that the nephridial sacs in Recent octo-

brachians are situated ventrally to the branchial hearts and

vena cava further suggests that the specimen from the

Smith collection represents a ventral view (see Young and

Vecchione 1996, Figs. 8–9).

The yellow staining pattern is thus likely to represent

major components of the true body cavities (Budelmann

et al. 1997). The venous vessels are structurally similar to

the blood sinuses, which also developed from embryonic

blood spaces. The nephridial sacs, in contrast, represent

parts of the coelomic cavities.

Our interpretation also sheds new light on the nature of

that part of the cephalopod gill that has been preserved.

Mehl (1990), Reitner (2009), and Fuchs and Larson

A nearly complete respiratory, circulatory, and excretory system

123


D. Fuchs et al.

123


(2011a) interpreted the feather-like structures in gladius-

bearing octobrachians as cartilaginous gill skeleton,

whereas Fuchs et al. (2009) considered them to be the ef-

ferent branchial vessels themselves. Our present observa-

tions suggest that the yellowish staining marks venous

vessels rather than cartilaginous structures. This assump-

tion may explain why the staining is not visible under UV

light, while cartilaginous tissues such as eye capsules or fin

supports that are preserved in apatite are strongly fluores-

cent (Fuchs et al. 2009; Fuchs and Larson 2011a, b). Ac-

cordingly, the yellowish ‘‘feathers’’ most likely represent

the primary (first-order) and secondary (second-order) af-

ferent branchial vessels carrying the deoxygenated blood.

Hence, Fuchs and Larson (2011b, p. 831, Figs. 16.1–5)

were in error when they detected gill skeletal elements

supporting septa characteristics for octobrachians (see

Young and Vecchione 2002). In light of our new insights,

these very short side branches of the gill lamellae likely

correspond to the third-order afferent branchial vessels.

Determination of the yellowish staining as venous blood

vessels finally confirms the assumption of Fuchs and Lar-

son (2011b, p. 239, Figs. 4.1–6), who first linked the

reticulated staining pattern adjacent to eye capsules with

the eyes’ capillary system.

What happened taphonomically?

The taphonomy of the above described specimens is aty-

pical of fossil coleoids, both in terms of the tissues pre-

served and the replicating mineral phase. Unlike most

fossil coleoids, where the ink sac is usually the only in-

ternal organ preserved (e.g., Glass et al. 2012) and the body

is replaced by apatite (e.g., Wilby et al. 2004), these spe-

cimens retain much of their internal anatomy, and it is

replicated by an iron-rich phase. This is presumed to be

goethite (iron oxyhydroxide), based on its colour, its

amorphous habit, and EDX analysis: elemental maps

indicate elevated Fe and O relative to the background

CaCO3 sediment, making siderite (FeCO3) a less likely

prospect (Fig. 3). The goethite does not replace the tissues;

it rather preserves their gross form as a ‘stain’ (or ‘sil-

houette’) on the abutting sediment. This most likely com-

prises a thin coating rather than a replacement of the

b Fig. 1 Octopoda incertae sedis, early Late Cenomanian plattenkalks

of Hadjoula (Metoicoceras geslinianum zone), overviews.

a Specimen 1, coll. Ru Smith (Houston, Texas). b Specimen 2, coll.

Ru Smith; c MC-139a; d MC-140a (the rectangle indicates the

position of EDX elemental mapping). Scale bars 10 mm

Fig. 2 Interpretation of the yellow staining. a Detail of specimen 1, coll. Ru Smith. b Corresponding sketch. Scale bar 3 mm


123


sediment, as it affects both the constituent CaCO3 and

(rare) quartz grains. In contrast, the sediment’s interstitial

quartz cement remains unstained, and may itself overprint

the goethite, suggesting that it postdates fossilization.

The goethite stains have well-defined (i.e., discrete)

margins and even colour density, retain fine morphological

details (e.g., secondary lamellae), and are symmetrical

across the midline of the fossil. These features suggest that

they each represent the preserved remains of an individual

organ and/or tissue rather than the compounded outlines of

multiple superimposed ones. The goethite is conspicuously

localised in blood-rich organs, including the circulatory

system (hearts and gills), a major sinus, the nephridia, and

the gonad. This strongly implies a causal relationship.

Comparable preferential preservation of well-vascularized

organs (as iron-rich stains) has been reported in fossil

vertebrates (e.g., Dal Sasso and Signore 1998; Ruben et al.

1999; Davidson and Trewin 2005; Lindgren et al. 2010),

where it has been linked to the in vivo presence of iron in

their hemoglobin (see also Greenwalt et al. 2013). How-

ever, this cannot explain the preservation of the viscera in

the Lebanese coleoids, as cephalopods use a copper-bear-

ing protein (haemocyanin) to transport oxygen throughout

their body tissues. It is significant that Cu was not detected

in these specimens, though we cannot discount the possi-

bility that it may have been lost during weathering or that it

was present in trace amounts (e.g., Pushie et al. 2014).

Instead, we propose that soft tissue mineralization was

more likely a consequence of the oxygen-binding capacity

of the haemocyanin (a metalloprotein) and its ability to lo-

cally regulate redox conditions immediately after death.

Support for this contention is evidenced in the preferential

preservation of the venous (i.e., deoxygenated) components

of the circulatory system, which would theoretically have

had the greatest potential for sequestering oxygen and for

reducing the Eh in the immediate vicinity. Worthy of note is

the apparent non-preservation of the systemic heart and

other components of the arterial (i.e., oxygenated) system.

Analogous microenvironments, defined by steep geo-

chemical gradients (Eh, pH, saturation), are widely impli-

cated in the fossilization of soft tissues (see Briggs 2003),

although they are typically thought to be generated by mi-

crobial decay rather than body fluid chemistry. Whatever the

cause, they have the effect of triggering the local pre-

cipitation of particular minerals in, on, or around a tissue.

Because anaerobic conditions are rapidly established in de-

caying carcasses (see Sagemann et al. 1999), it seems un-

likely that the goethite (an oxyhydroxide) is a primary phase.

In common with several other lagerstatten (e.g., see Gabbott

et al. 2004; Williams et al. 2008; Van Roy et al. 2010), it is

more likely a weathering product of pyrite, which is

favoured in reducing marine conditions such as those en-

visaged here. Regardless of nature of the initial phase, it is

clear that early mineralization was a key factor in stabilizing

the otherwise decay-prone viscera (see Kear et al. 1995).

This ensured that even delicate structures such as secondary

lamellae maintained their integrity whilst being transposed

onto the sediment by the decay of the intervening mantle.

Acknowledgments We are particularly grateful to Ru Smith

(Houston, Texas), who kindly provided his specimens for morpho-

logical studies. Thanks also go to Monika Bulang-Lorcher (Freie

Universitat Berlin), who drew the sketch in Fig. 2.

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