Coralline Algae at the Paleocene/ Eocene Thermal Maximum in the Southern Pyrenees (N Spain)

Co alline Algae a he Paleocene/
Eocene The mal Maximum in he
Sou he n Py enees (N Spain)
Julio Agui e
1
*
†
, Juan I. Bace a
2†
and Juan C. B aga
1†
1
Dp o. Es a ig a ı
´a y Paleon ologı
´a, Facul ad de Ciencias, Uni e sidad de G anada, G anada, Spain,
2
Depa amen o de
Geologı
´a, Facul ad de Ciencia y Tecnologı
´a, Uni e sidad del Paı
´s Vasco, Bilbao, Spain
Du ing he Paleocene/Eocene The mal Maximum, ~55.6 Ma, he Ea h expe ienced he
wa mes e en o he las 66 Ma due o a massi e elease o CO
2
. This e en las ed o ~100
housands o yea s wi h he consequen ocean acidifica ion (es ima ed pH = 7.8-7.6). In his
pape , we analyze he e ec s o his global en i onmen al shi on co alline algal
assemblages in he Campo and Se aduy sec ions, in he sou h-cen al Py enees
(Huesca, N Spain), whe e he PETM is eco ded wi hin coas al- o-shallow ma ine
ca bona e and siliciclas ic deposi s. In bo h sec ions, co alline algae occu mos ly as
agmen s, al hough hodoli hs and c us s coa ing o he o ganisms a e also equen .
Rhodoli hs occu ei he dispe sed o locally o ming dense concen a ions ( hodoli h beds).
Dis ichoplax bise ialis and genicula e o ms (mos ly Jania nummuli ica) o he o de
Co allinales domina ed he algal assemblages ollowed by Spo oli hales and Hapalidiales.
O he ep esen a i es o Co allinales, namely Spongi es,Li hopo ella as well as
Neogonioli hon,Ka pa hia, and Hyd oli hon, a e less abundan . Species composi ion
does no change h oughou he Paleocene/Eocene bounda y bu he ela i e abundance
o co alline algae as componen s o he ca bona e sedimen s unde wen a educ ion. They
we e abundan du ing he la e Thane ian bu became a e du ing he ea ly Yp esian. This
abundance dec ease is due o a d as ic change in he local paleoen i onmen al condi ions
immedia ely a e he bounda y. A ha dg ound a he op o he Thane ian ca bona es was
ollowed by con inen al sedimen a ion. A e ha , ma ine sedimen a ion esumed in shallow,
e y es ic ed lagoon and pe i idal se ings, whe e muddy ca bona es ich in ben hic
o amini e a, e.g., milioliids (wi h abundan Al eolina) and so i ids, and e en ually
s oma oli es we e deposi ed. These ini ial es ic ed condi ions we e un a o able o
co alline algae. Ad e se condi ions con inued o he end o he s udy sec ions al hough
co alline algae eappea ed and we e locally equen in some beds, whe e hey occu ed
associa ed wi h co als. In Se aduy, he ma ine eflooding was also accompanied by
significan e igenous supply, p ecluding algal de elopmen . The e o e, he obse ed
changes in co alline algal assemblages du ing he PETM in he Py enees we e mos likely
ela ed o local paleoen i onmen al shi s a he han o global oceanic o
a mosphe ic al e a ions.
Keywo ds: hodoli h beds, he mal maximum, paleocene/eocene bounda y, ocean acidifica ion, py enean basin
F on ie s in Ma ine Science | www. on ie sin.o g July 2022 | Volume 9 | A icle 8998771
Edi ed by:
Gang Li,
Sou h China Sea Ins i u e o
Oceanology, Chinese Academy o
Sciences, China
Re iewed by:
Ami K. Ghosh,
Bi bal Sahni Ins i u e o
Palaeosciences (BSIP), India
She i Fa ouk,
Egyp ian Pe oleum Resea ch
Ins i u e, Egyp
*Co espondence:
Julio Agui e
[email p o ec ed]
†
These au ho s ha e con ibu ed
equally o his wo k
Special y sec ion:
This a icle was submi ed o
Ma ine Ecosys em Ecology,
a sec ion o he jou nal
F on ie s in Ma ine Science
Recei ed: 19 Ma ch 2022
Accep ed: 23 May 2022
Published: 04 July 2022
Ci a ion:
Agui e J, Bace a JI and B aga JC
(2022) Co alline Algae a he
Paleocene/Eocene The mal Maximum
in he Sou he n Py enees (N Spain).
F on . Ma . Sci. 9:899877.
doi: 10.3389/ ma s.2022.899877
ORIGINAL RESEARCH
published: 04 July 2022
doi: 10.3389/ ma s.2022.899877
INTRODUCTION
Recen s udies on he p esen -day global change, pa icula ly
inc easing empe a u e and ocean acidifica ion linked o he
massi e elease o g eenhouse gasses o he a mosphe e due o
an h opogenic ac i i ies, a e p og essi ely demanding de ailed
analyses o e en s o simila magni ude h oughou he Ea h
his o y (Ridgwell and Schmid , 2010;Ga uso and Hansson,
2011;Hönisch e al., 2012;Hansen e al., 2013;Lun e al.,
2013;Zeebe and Zachos, 2013;Bu ke e al., 2018;Haynes and
Hönisch, 2020). One o he a ge s is o analyze he e ec s o
hese global p ocesses on ma ine calcified bio a in he geological
eco d o model and compa e wi h he p edic ed biological
changes o he u u e. The Paleocene/Eocene he mal
maximum (PETM) is a spike-like he mal e en (Kenne and
S o , 1991;Thomas and Shackle on, 1996), a which esea che s
a e looking as an ancien analogue o unde s and he ongoing
bio ic changes (Zeebe and Wes b oek, 2003;Sluijs e al., 2007;
Ridgwell and Schmid , 2010;McIne ney and Wing, 2011;Zeebe
and Ridgwell, 2011;Hönisch e al., 2012;Zeebe, 2012;No is
e al., 2013;Zeebe and Zachos, 2013;Mudelsee e al., 2014;
Haynes and Hönisch, 2020).
Du ing he Paleocene/Eocene bounda y ~55.6 million yea s
ago (Ma), he Ea h wi nessed he wa mes e en o he las 66
Ma due o a huge deli e y o CO
2
o he a mosphe e mos ly
linked o olcanism (Haynes and Hönisch, 2020). This e en is
eco ded by an ab up nega i e ca bon s able iso ope (d
13
C)
excu sion (CIE) (Koch e al., 1992). I is es ima ed ha abou
1,500 ppm o CO
2
we e eleased o he a mosphe e du ing a
sho ime in e al o 120-220 housands o yea s (ky ) (e.g.,
Sluijs e al., 2007;McIne ney and Wing, 2011) o e en less
(Kenne and S o , 1991;Zachos e al., 2005). The mos ecen
ime model sugges s ha he e was a fi s pulse o CO
2
elease 5-6
ky a e he CIE ha was ollowed by sus ained high alues o
ca. 40 ky and ended ~100 ky (Haynes and Hönisch, 2020). As a
consequence, ocean pH dec eased o 7.8-7.6 and global ocean
su ace empe a u e inc eased 5-9°C (Zachos e al., 2005;Zachos
e al., 2008;McIne ney and Wing, 2011;Zeebe and Ridgwell,
2011;Zeebe, 2012;No is e al., 2013;Zeebe and Zachos, 2013;
Mudelsee e al., 2014;Haynes and Hönisch, 2020).
Despi e he d as ic a mosphe ic, empe a u e, and oceanic
al e a ions aking place du ing he PETM, only deep-sea ben hic
o amini e a we e significan ly a ec ed, and 35-50% o he
species became ex inc (Thomas, 1990;Thomas, 2007;Aleg e
e al., 2009a;Aleg e e al., 2009b), whe eas he e en had a lesse
impac on ma ginal pla o m inhabi an s (Thomas, 2003;Aleg e
e al., 2005). Co al ee ecosys ems also showed conside able
educ ion in co al species di e si y, numbe o ee si es, ee size,
and ee ca bona e p oduc ion du ing he Paleocene/Eocene
bounda y (Flügel and Kiessling, 2002;Schneibne and Speije ,
2008;Kiessling, 2010;Pe in and Kiessling, 2010). No is e al.
(2013) called his ee collapse as he ea ly Eocene ee gap.
La ge ben hic and plank onic o amini e a, calca eous
nannoplank on and deep-sea os acods expe ienced di e si y
u no e s du ing he PETM (Schaub, 1951;Ho inge , 1960;
Canudo and Molina, 1992;Canudo e al., 1995;Kelly e al., 1998;
Speije and Mo si, 2002;Scheibne e al., 2005;Gibbs e al.,
2006a;Gibbs e al., 2006b;Speije e al., 2012). In addi ion,
abe an o ms ( e a ologies) o calca eous nannoplank on (Ra fi
and De Be na di, 2008), as well as dwa fism in deep-sea
os acods (Yamaguchi e al., 2012), ha e been eco ded.
Co allinealgae, ullycalcifiedma ineau o ophico ganisms,a e
one o he mos endange ed algal g oups due o global empe a u e
inc ease and ocean acidifica ion (e.g., Ma in and Hall-Spence ,
2017;Co nwall e al., 2021). Labo a o y s udies and field
obse a ions indica e ha co alline algae migh be nega i ely
a ec ed due o ocean acidifica ion de i ed om he g eenhouse
gasses elease (An hony e al., 2008;Hall-Spence e al., 2008;
Ma in and Ga uso, 2009;Büdenbende e al., 2011;Diaz-Pulido
e al.,2012;Kamenose al.,2013;Guy-Haime al.,2016;Ma inand
Hall-Spence , 2017;Peña e al., 2020a;Co nwall e al., 2021).
None heless, con adic o y o non-conclusi e esul s ha e also
been ob ained (Ma in and Hall-Spence , 2017;Peña e al., 2020a;
Co nwall e al., 2021; and e e ences he ein) due o acclima ion o
co alline algae o acidifica ion, physiological ad an ages (p e-
adap a ions) o in e ac ion wi h o he non-calcified epiphy es
g owing on co allines (Ma in and Hall-Spence , 2017;Guy-
Haim e al., 2020;Peña e al., 2020a;Co nwall e al., 2021).
In o de o explo e he long- e m e ec s o he global change
on co alline algae and hei biological/e olu iona y esponses o
hese en i onmen al al e a ions, he e we analyzed co alline algal
assemblages ac oss he Paleocene/Eocene bounda y and he
PETM. The main aim was o assess how beha ed/ esponded
co alline algae o his majo empe a u e change and ocean
acidifica ion e en . We s udied he classical sec ions o Campo
and Se aduy, in he sou h-cen al Py enees (Huesca p o ince, N
Spain), which eco d uppe Thane ian and lowe Yp esian
shallow-wa e ca bona es as well as he PETM. These sec ions
ha e been la gely s udied mos ly ocusing on he s a ig aphy,
sedimen ology, bios a ig aphy, and geochemis y ac oss he
Paleocene/Eocene in e al (Eichensee and Lu e bache , 1992;
Pay os e al., 2000;Pujal e e al., 2000a;Pujal e e al., 2000b;
O ue-E xeba ia e al., 2001;Molina e al., 2003;Pujal e e al.,
2003;Schmi z and Pujal e, 2003;Schmi z and Pujal e, 2007;
Scheibne e al., 2007;Domingo e al., 2009;Pujal e e al., 2009a;
Pujal e e al., 2009b;Robado e al., 2009;A os egi e al., 2011;
Bace a e al., 2011;Manne s e al., 2013;Pujal e e al., 2014;
Hamon e al., 2016;Dulle e al., 2019;Li e al., 2020;Se a-Kiel
e al., 2020;Pujal e e al., 2022). Rega ding he ossil con en ,
s udies ha e ocused mos ly on plank onic and ben hic
o amini e a (bo h la ge and small o ms) as well as co als
(Se a-Kiel e al., 1994;O ue-E xeba ia e al., 2001;Molina e al.,
2003;Scheibne e al., 2007;Li e al., 2020;Se a-Kiel e al., 2020).
None heless, no de ailed analysis o he co alline algae
h oughou he Paleocene-Eocene ansi ion has been ca ied
ou . We analyze he ype o occu ence, species di e si y and
ela i e abundance o co alline algae wi h espec o o he ossils
h oughou he la e Thane ian (la e Paleocene)-ea ly Yp esian
(ea ly Eocene) in e al o check how global al e a ions du ing he
PETM a ec ed co alline algae. In he case o hodoli hs, we also
examine he co alline algal g ow h o ms, as well as he inne
algal a angemen s and ex e nal mo phology.
Agui e e al. Co alline Paleocene/Eocene The mal Maximum
F on ie s in Ma ine Science | www. on ie sin.o g July 2022 | Volume 9 | A icle 8998772
GEOLOGICAL SETTING
The Py enees is a e e ence a ea in Wes e n Eu ope o he
s udy o Paleogene shallow o deep-ma ine deposi s and he
se ies o dis inc bio ic and physical e en s ha punc ua ed
he beginning o he Cenozoic. Du ing he Paleocene and ea ly
Eocene, he Py enean basin was a la ge ma ine embaymen
opening o heBayo Biscay, o heWNW,wi hacen al
(hemi)pelagic ough flanked on he no h, sou h and eas by
ex ensi e shallow ma ine ca bona e pla o ms (Bace a e al.,
2004;Bace a e al., 2011)(Figu e 1A). The pla o m sys ems
e ol ed wi h gene al amp p ofiles and mos sec o s exhibi a
wide ange o ca bona e acies ep esen a i e o beaches, idal
fla s, lagoons, seag ass banks, shoals, idal ba s and a a ie y o
ee al cons uc ions. Mos inne o mid amp li ho acies a e
ela i ely ich in pho ic-dependen o ganisms (calca eous ed
algae, co als, la ge ben hic o amini e a –LBF–)andalso
comp ise a a ied he e ozoan bio a, ep esen ed by mollusks,
b yozoans, echinode ms (Eichensee , 1988;Se a-Kiel e al.,
1994;Bace a, 1996;Bace a e al., 2004;Robado , 2008;Bace a
e al., 2011). Landwa ds, he pla o m successions in e finge
wi h siliciclas ic and mixed sedimen s wi h subo dina e
e apo i es and discon inuous paleosols, known as he
Ga umnian acies, which ep esen allu ial o coas al plain
deposi ional en i onmen s (Figu e 1A).
Sedimen a ion du ing he Paleocene and ea ly Eocene in he
Py enean basin ma gins e ol ed unde gene al ansg essi e
condi ions, punc ua ed by a numbe o hi d o de ela i e sea-
le el alls o a iable magni ude and egional ex en . These sea
le el d ops a e eco ded by ab up acies shi s and mo e o less
p ominen e osional discon inui ies, commonly associa ed o
enhanced subae ial exposu e. Based on mapping and egional
co ela ion, up o fi e deposi ional sequences eco ding shallow
ma ine se ings ha e been dis inguished wi hin he uppe
Thane ian-lowe Yp esian succession (Eichensee and
Lu e bache , 1992;Bace a, 1996;Bace a e al., 2004;Bace a
e al., 2011).
Ou s udy ocuses on he Paleocene o lowe Eocene co alline
ed algae eco ded in he Campo and Se aduy sec ions, which
o m pa o con inuous ou c ops along he Fe e a and Mo illo-
Me li idges, on he no he n flank o he T emp-Ainsa a ea
(Figu e 1B). P e ious s udies in hese wo sec ions and on coe al
ou c ops in he whole T emp-Ainsa a ea ha e p o ided a well-
cons ained s a ig aphic amewo k o he allu ial-coas al o
FIGURE 1 |(A) Gene al paleogeog aphy o he Py enean a ea du ing he ea lies Eocene, a he ime o he so-called Ile dian ansg ession (adap ed om Bace a
e al., 2004). (B) Enla ged geog aphic map o pa o he Ainsa-T emp sec o o he Py enean basin wi h loca ion o he Campo and Se aduy sec ions (yellow s a s).
(C) In eg a ed s a ig aphy o he uppe Paleocene-lowe mos Eocene s a a o he Ainsa-T emp a ea (adap ed om Bace a e al., 2011;Pujal e e al., 2014). The
ec angles indica e he posi ion o he wo s udy s a ig aphic sec ions wi hin he gene al s a ig aphic amewo k.
Agui e e al. Co alline Paleocene/Eocene The mal Maximum
F on ie s in Ma ine Science | www. on ie sin.o g July 2022 | Volume 9 | A icle 8998773
shallow ma ine successions embedding he PETM e en (e.g.,
Eichensee , 1988;Pay os e al., 2000;Bace a e al., 2004;Bace a
e al., 2011). A de ailed bios a ig aphic scheme has been
p oposed based on LBF biozona ion calib a ed wi h s anda d
calca eous plank on zona ions and magne os a ig aphy (e.g.,
Ho inge and Schaub, 1960;Schaub, 1973;Se a-Kiel e al., 1994;
Se a-Kiel e al., 1998;O ue-E xeba ia e al., 2001;Pujal e e al.,
2009b;Se a-Kiel e al., 2020)(Figu e 1C).
The uppe Paleocene o lowe Eocene s a a o he a ea
in ol es he in e bedding o ou li hos a ig aphic o ma ions
(Figu e 1C). The Espluga eda and Cla e Fo ma ions a e made
up o siliciclas ic deposi s o med in allu ial o coas al se ings.
The Na a i and Se aduy Fo ma ions a e domina ed by
ca bona e li ho acies ep esen ing coas al, lagoonal and shallow
ma ine en i onmen s. In e ms o sequence s a ig aphy, he
uppe Paleocene Espluga eda and Na a i Fo ma ions emb ace
wo hi d-o de deposi ional sequences ( he Th-1 and Th-2) and
he lowe Yp esian Cla e and Se aduy Fo ma ions comp ise
h ee deposi ional sequences (IL-1, IL-2 and IL-3) (Figu e 1C).
The PETM, as de e mined om de ailed geochemical and
iso opic s udies (Pujal e e al., 2014;Pujal e e al., 2022) lies
wi hin he lowe mos Yp esian IL-1 sequence, encompassing
mos o he allu ial Cla e Fm. and he lowe mos ma ine
deposi s o he Se aduy Fo ma ion (Figu e 1C).
Acco ding o paleogeog aphic econs uc ions o he a ea
(Pujal e e al., 2014), he Se aduy sec ion ep esen s a
shallowe posi ion ela i e o he Campo sec ion. This is clea ly
e idenced by he a chi ec u e o he uppe Paleocene succession,
which a Campo sec ion mainly consis s o shallow ma ine
ca bona es, whe eas a Se aduy sec ion i is mos ly made up
o con inen al Ga umnian acies. In bo h sec ions, he ea ly
Eocene comp ises coas al and shallow-ma ine ca bona es
defining a deepening succession ha culmina es wi h middle o
ou e amp deposi s. In mos ou c ops o he T emp-Ainsa a ea,
he PETM e en lies wi hin con inen al siliciclas ic deposi s. In
he Campo sec ion, i is eco ded wi hin an in e al o
con inen al clas ics wi h discon inuous palus ine ca bona es
passing e ically o inne amp and es ic ed idal fla
ca bona es (Figu e 1C). The e ical acies succession o he
Paleocene-lowe Eocene deposi s exposed a Campo and
Se aduy is syn he ized in Figu e 2.
STRATIGRAPHIC SECTIONS
Campo Sec ion
This sec ion is loca ed along he banks o he Ese a Ri e , 1 km
sou h om he illage o Campo (Figu e 1B). Th ee main
ou c ops (along he old oad o Ainsa, he local oad o
Na a i, and he oad om Campo o G aus) allow he bed-
by-bed analysis o 173 m o he uppe Paleocene o lowe Eocene
deposi s (Figu e 2A). Sampling was ocused in wo in e als. The
lowe one comp ises he uppe mos 38 m o he Thane ian Th-2
sequence, which is made up o middle amp bioclas ic ca bona es
FIGURE 2 | S a ig aphic logs o he Campo (A) and Se aduy (B) sec ions, wi h indica ion o acies, main in e als, s a ig aphic sequences (Th and IL),
bios a ig aphy, and he loca ion o he samples s udied o co alline algae (a e Eichensee , 1988;Se a-Kiel e al., 1994;Robado , 2008;Bace a e al., 2011;Se a-
Kiel e al., 2020). Wck, Wackes one; Pck, Packs one; G s , G ains one; Ruds , Ruds one; Fls , Floas one; SB, Sequence bounda y.
Agui e e al. Co alline Paleocene/Eocene The mal Maximum
F on ie s in Ma ine Science | www. on ie sin.o g July 2022 | Volume 9 | A icle 8998774
wi h decime e - o me e - hick sigmoidal c oss bedded idal ba s
ending owa ds he eas and sou heas . This in e al culmina es
wi h a massi e muddy limes one ich in co als, ed algae and
mollusks, jus below he p ominen discon inui y a he op o
he Th-2 sequence ha ma ks he Paleocene-Eocene bounda y.
Acco ding o Se a-Kiel e al. (1994;2020), he LBF assemblage
o his uppe pa o he Th-2 sequence comp ises Glomal eolina
le is,Assilina y e ae,A. azilensis, and Da iesina ga umnensis, all
cha ac e is ic o he SBZ4 biozone o Se a-Kiel e al.
(1998) (Figu e 2A).
The uppe in e al, up o 41 m hick, belongs o he lowe
Eocene and comp ises he uppe pa o he IL-1 and mos o he
IL-2 deposi ional sequences (Figu e 2A). This in e al mainly
consis s o shallow, inne - amp ca bona es ich in al eolinids,
small milioliids, and so i ids, associa ed wi h subo dina e
gas opods and bi al es (oys e s and lucinids). A 2.5 m hick
massi e co al- ich limes one bed defining he base o sequence
IL-2 was he only p o iding significan amoun s o co alline
algae. The e o e, his bed was sampled in wo di e en ou c ops:
1) samples CPE-14 and 15 on he new oad o G aus, and, 2)
samples CPN-1 o 3 on he old oad o Ainsa. Acco ding o
Se a-Kiel e al. (1994;2020), his in e al encompasses LBF
associa ion cha ac e is ic o he SBZ5 (Al eolina edenbu gi,A.
a amea,A. a ians) and he lowe pa o SBZ6 (A. ellipsoidalis,
A. pas icilla a,A. a . a agonensis)(Figu e 2A).
Se aduy Sec ion
The Se aduy sec ion is loca ed 0.5 km no h o Se aduy del
Pon , on he Isabena alley, ~12 km o he SE o Campo
(Figu e 1B). Co ela ion h ough mapping o he ou c ops on
bo h i e banks, he Se aduy Eas and Se aduy Wes , allowed
analyzing in de ail a 130 m hick sec ion o uppe Paleocene
(66 m) and lowe Eocene (64 m) deposi s (Figu e 2B).
The uppe Paleocene is mos ly siliciclas ic and consis s o ed
o b ownish calca eous lu i es wi h in e cala ions o medium o
coa se-g ained li hic sands ones o ming lenses, shee s and
disc e e channel fills (allu ial floodplain deposi s), and
discon inuous de elopmen o calc e e paleosols. Two disc e e
in e als o shallow ma ine ca bona es, espec i ely up o 4 and
8 m hick, define he maximum flooding s ages wi hin he
uppe Paleocene deposi ional sequences Th-1 and Th-2
(Figu es 1C,2B). We sampled he uppe one (Th-2 sequence)
(Figu e 2B). The lowe beds o his uppe limes one uni a e
sandy co algal limes ones, which a e he only ones in he
Thane ian o Se aduy sec ion con aining significan amoun o
ed algae (samples SEW-0 o 2). Acco ding o Se a-Kiel e al.
(1994;2020), he lowe limes one in e al (Th-1 sequence)
comp ises a LBF assemblage o Glomal eolina p imae a,
Idalina sinja ica,andMiscellanea y e ae, indica i e o he
SBZ3, whe eas he uppe limes one in e al (Th-2 sequence)
includes Glomal eolina le is and Da iesina ga umnensis, wo
cha ac e is ic axa o he SBZ4 (Figu e 2B).
The lowe Eocene deposi s belong o deposi ional sequences
IL-1 o IL-3 (Figu e 2B). The IL-1 is en i ely made up o
con inen al deposi s, including he cha ac e is ic Cla e
conglome a e membe o heCla e Fo ma ion,which
acco ding o Pujal e e al. (2014;2022) ma ks he beginning o
he PETM e en in he whole T emp-Ainsa a ea.
The IL-2 consis s o shallow ma ine ca bona es. The bulk
deposi s co espond o bedded packs one-g ains ones ich in
al eolinids and so i ids wi h a LBF assemblage o Al eolina
edenb igi,A. a amea and Ope o bi oli es g acilis (SBZ5) in
he lowe beds, and A. ellipsoidalis,A. dolioli o mis and
Ope o bi oli es (lowe pa o SBZ6) in he uppe beds
(Figu e 2B). On he Se aduy Wes ou c op, a bed wi h
sca e ed co als 13 m abo e he base o he sequence is he
only one wi h significan ed algal con en (samples SEW-3). On
he eas ou c ops o he alley, a dis inc massi e bed package o
co algal limes ones, up o 17 m hick, in e finge s wi h he
dominan Al eolina- ich deposi s and comp ises he main
in e al sampled o ed algae (samples SEE-1 o 10)
(Figu e 2B). Eichensee and Lu e bache (1992) in e p e ed
hese massi e limes ones as a low- elie co al bios ome.
The o e lying IL-3 sequence es s uncon o mably on o he
IL-2 sequence and consis s mainly o bio u ba ed sands ones,
sil y ma ls, and sandy limes ones ha e en ually o m me e -
hick idal ba s wi h sigmoidal c oss bedding ending owa ds
he no heas and sou heas . The ossil con en in he mixed
deposi s is a mix u e o small nummuli ids, milioliids, a e
Al eolina, g een algae (dasyclads), bi al es, echinoids and
gas opods. Ve ically, he basal mixed deposi s o he IL-3
pass g adually in o Al eolina- ich packs one-g ains ones,
simila o hose defining he bulk o sequence IL-2. The LBF
assemblage o hese uppe mos limes ones comp ises Al eolina
ellipsoidalis,A. dolioli o mis,Glomal eolina lepidula,
Ope o bi oli es,andNummuli es bigu densis,defining he
uppe pa o he SBZ6 (Se a-Kiel e al., 1998).
METHODS
Co alline algae occu mos ly as agmen s, which do no p ese e
enough axonomic ea u es o be iden ified a any p ecise
axonomic le el. In hese cases, we es ima e he ela i e
abundance o co alline algal agmen s using he cha s o
Baccelle and Bosellini (1956).
In he uppe Thane ian ca bona es, co alline algae occu
o ming hodoli hs concen a ed in pa icula beds. He e,
p ese a ion o he co alline algae is be e allowing mo e
p ecise axonomic iden ifica ions. In hese cases, he ela i e
abundance o species was quan ified by poin -coun ing he
a ea occupied by each axon (Pe in e al., 1995). We iden ified
he co alline algae a he lowes possible axonomic le el, in mos
cases a species le el. When he specimens could no be
confiden ly assigned o a desc ibed species, we used an open
specific nomencla u e. The axonomic schemes o o de s,
amilies, sub amilies and gene a ollow ecen molecula
phylogenies (Peña e al., 2020b;Jeong e al., 2021).
The ex e nal hodoli h mo phology was examined in di e en
2-D sec ions a he ou c ops, as ex ac ion o comple e and
isola ed hodoli hs was impossible due o cemen a ion o
limes ones. The in e nal a angemen , algal g ow h o m, and
Agui e e al. Co alline Paleocene/Eocene The mal Maximum
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algal composi ion o hodoli hs we e analyzed in hin sec ions.
We use he e minology p oposed by Woelke ling e al. (1993),as
well as he ecen e minology upda ed by Agui e e al. (2017).
All da a a e compiled in Table 1, and a discussion o some o
he iden ified axa is p o ided in he Taxonomic Appendix.
RESULTS
Co alline Algal Occu ences
Mos o he co alline algae occu as agmen s in uds one,
g ains one and packs one li ho acies. They occu wi h o he
bioclas s, mos ly, la ge and small ben hic o amini e s, co als,
mollusks, b yozoans, echinoids, se pulids, and ba nacles, as well
as addi ional hodophy es, such as Ma inella lugeoni P ende
1939 and he peyssonneliacean Polys a a alba,(P ende )
Denizo 1968 and chlo ophy es o he o de s Dasycladales and
B yopsidales (Halimeda spp) (Figu e 3).
Co alline algal agmen s a e small (up o 2 mm; e y
excep ionally la ge ) and ab aded due o ewo king
(Figu es 4A, B). In bo h sec ions, co alline algae ep esen up
o 30% o he ock olume in he uppe Thane ian sedimen s.
The p opo ion dec eases subs an ially in he lowe Yp esian
deposi s, wi h alues anging om 1 o 5% (excep ionally, up o
10% in sample CPE-15).
Due o high agmen a ion and ab asion in hese li ho acies,
mos co alline algal emains do no show diagnos ic
cha ac e is ics o be p ope ly iden ified, e en a amily and
o de le els. None heless, in some agmen s ep oduc i e
s uc u es a e p ese ed allowing hei iden ifica ion. In he
case o Dis ichoplax bise ialis, he cha ac e is ic lamina g ow h
o ms and he isobila e al cell a angemen s acili a e
i s iden ifica ion.
In he small co al buildups ound bo h in he uppe Thane ian
and lowe Yp esian deposi s, co alline algae occu as agmen s in
he ma ix and as hin lamina c us s a ached o co als (Figu es 4C,
D). Mo e a ely, hey o m small hodoli hs wi h bioclas ic nuclei,
mos ly co als o o he algal agmen s (Figu e 4E).
Co alline algae also occu loosely o densely packed in
hodoli h beds (Agui e e al., 2017), such as hose ound in
he uppe pa o he Na a i Fo ma ion in he Campo sec ion
(samples CPE-8 and CPE-10) (Figu es 5A–E). The loosely
packed beds consis o ellipsoidal hodoli hs, om 1 o 3 cm in
la ges diame e , made up o enc us ing o wa y co allines
(Figu es 5A, C). They a e embedded in a fine-g ained
packs one-wackes one ma ix wi h accompanying o ganisms
such as echinoids, ben hic o amini e s, and b yozoans.
Densely packed hodoli h beds con ain sphe oidal o ellipsoidal
hodoli hs, up o 7 cm in la ges diame e , consis ing o
enc us ing, u icose and wa y co allines (Figu es 5B, D, E).
In his case, hodoli hs a e included in a packs one ( a ely
g ains one) ma ix.
In e nally, hodoli hs a e ei he mul ispecific o monospecific
(Figu e 6). They a e buil up by co alline algae in e g own wi h
enc us ing o amini e a (mainly Solenome is), se pulids,
b yozoans, and Polys a a alba (Figu es 3A,6). The nuclei o
hodoli hs consis o li hoclas s o bioclas s, such as co als
(Figu es 5F,6). In e nal oids a e filled wi h he ma ix
sedimen o a e open and la e filled up wi h cemen . In some
cases, hodoli hs a e asymme ical and geope al s uc u es
indica e ha he p e e en ial algal g ow h coincided wi h he
up igh posi ion o he hodoli h. This sugges s ha hodoli hs
a e p ese ed in hei o iginal g ow h posi ion, wi hou
subs an ial ewo king.
Co alline Algal Di e si y
The o de s Co allinales, Hapalidiales, and Spo oli hales a e
ep esen ed h oughou he la e Thane ian-ea ly Yp esian
in e al in he s udy sec ions, being he wo o me g oups he
mos di e sified (Table 1;Figu e 7). In he la e Thane ian,
co alline assemblages include up o 16 species. Maximum
co alline di e sifica ion is ound in he co al floa s one acies
sampled a Se aduy sec ion (samples SEW-0 and SEW-1)
(Figu es 2B,7). The h ee algal o de s unde wen a d as ic
educ ion in he numbe o species in he ea lies Yp esian, wi h a
i ual disappea ance wi hin he fi s ma ine beds encompassing
and immedia ely abo e he PETM a he Campo sec ion. He e,
he limes ones we e almos exclusi ely domina ed by LBF
packs ones-g ains ones, wi h al eolinids and subo dina e
so i ids. A e his in e al, he species ichness o co allines
inc eases in he ea ly Yp esian. This di e si y eco e y is
associa ed wi h he de elopmen o co al buildups a he base
o IL-2 in bo h Campo and Se aduy sec ions.
The es ima ion o he ela i e abundance o species is
hampe ed by p ese a ion. Among he easily iden ifiable ones,
he bes ep esen ed is Dis ichoplax bise ialis, which occu s in all
samples, ollowed by genicula e species. The abundance o D.
bise ialis embedded in a packs one-wackes one ma ix ound in
he uppe mos Thane ian ca bona es in he Campo sec ion
(samples CPE-9 and CPE-10) is ema kable, as i anges om
73% o 95% o he co alline assemblages (Figu e 8).
In con as , p ese a ion o co alline algae in he uppe
Thane ian hodoli h beds o Campo allows es ima ing species
abundance. He e, membe s o he o de Spo oli hales we e he
mos abundan (up o 75%), being Spo oli hon lugeoni he bes -
ep esen ed species, ollowed by Spongi es sp.1,a ew
Hapalidiales, and anecdo al p esence o lamina c us s o
Li hopo ella spp.
The hin lamina algae enc us ing co als, bo h in he
Thane ian and in he Yp esian, a e mos ly Li hopo ella spp,
and Li ho hamnion c ispi hallus and Li ho hamnion sp 5.
DISCUSSION
Paleoen i onmen al E olu ion
High agmen a ion and ounding o co alline algae and o he
bioclas s, in he c oss-bedded deposi s defining he lowe pa o
he uppe Thane ian Na a i Fo ma ion indica e high-ene gy
condi ions in an open inne amp se ing. Dominance o
Co allinales is consis en wi h hese shallow wa e condi ions
(B aga and Ma ı
n, 1988;B aga and Agui e, 2001;B aga and
Agui e e al. Co alline Paleocene/Eocene The mal Maximum
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TABLE 1 | Co alline algal species dis ibu ion in he wo s udy sec ions, indica ing p esence (X) o each axon in he samples.
HAPALIDIALES SPOROLITHALES CORALLINALES OTHER
Age Sample
N° o hin sec ions
Mic o acies
CCA in ma ix
Rhodoli hs
Li ho hamnion conc e um Howe
L:cama asae P ende
L:c :co allinae o me Lemoine
L:c :exube ans Mas o illi
L:c ispi hallus Johnson
L: aughani Howe
Li ho hamnion sp:1
Li ho hamnion sp:2
Li ho hamnion sp:3
Li ho hamnion sp:4
Li ho hamnion sp:5
Undi e en ia ed Hapalidiales
Melobesia sp:
Spo oli hon lugeonii P ende
S:c :ouliano ii P ende
S:b e ium=ai oldii
Spo oli hon sp:1
Undi e en ia ed Spo oli hales
Jania nummuli ica Lemoine
Genicula e sp:1c :Co allina p isca Johnson
Genicula e sp:2
Genicula e sp:3
Undi e en ia ed ganicula es
Li hopo ella minus Johnson
Li hopo ellamelobesioides ðFoslieÞFoslie
Dis ichoplax bise ialis Die ich
Spongi es sp:1
Spomgi es sp:2
Spongi es sp:3
Hyd oli hon lemoinei ðMi andaÞAgui e e al:
Ka pa hia sphae ocellulosa Maslo
Undi e en ia ed Co allinales
Polys a a alba ðP ende ÞDenizo
Ma inella lugeonii P ende
Dasycladales
Halimedales
Campo sec ion
ea ly Yp esian CPE-20 1 Wck.-Pck. Milioliids+Nummuli ids 0%
CPE-19 1 Pck.-G n. Al eolina+Milioliids 0%
CPE-18 1 G n. Al eolina+Milioliids 0%
CPE-17 1 Sands one Milioliids+Al eolina 0%
CPE-16 1 Pck-G n. Al eolinas 0%
CPE-15 4 Fls .(F m.) Co als+CCA c us s+Milioliids 5-10% Dispe sed hodos. CPN-3 x x x x x x x x x x x x x x
CPE-14 1 Pck.-Wck. Milioliids+oys e s 1% CPN; CPN-1; CPN-2 x xx
CPE-13 1 Pck.-G n. Al eolina 0%
CPE-12 1 Pck. Al eolina 0%
CPE-11 1 Pck. Al eolina 0%
la e Thane ian CPE-10 5 Wck.-Pck. BF+Co als+B yos+Dis ichoplax 10-20% Dispe sed hodos. x x x x x x x x x x x x
CPE-9 1 Wck. Solenome is+Dis ichoplax 10-20% xxxx
CPE-8 5 Fls . Rhodos. 20-25% Rhodoli h bed x x ? x x x x x x x x x x x x x
CPE-7 2 Rud. BF+CCA 20-25% x x x x x x x x x x x x x
CPE-6 1 Pck. LBF+CCA 35-40% x x x x x x x x x
CPE-5 7 Rud. BF+CCA+Mollusks+Co als 10-30% x x x x x x x x x x x x x
CPE-4 3 Rud. BF+CCA 5-15% xxx xx x x x
CPE-3 1 Pck. LBF+SBF+CCA 3-5% x x x x
CPE-2 1 Pck. LBF+SBF+se pulids+gas opods 3-5% xx
CPE-1 2 G n.-Pack. LBF+se pulids < 1% xx x
Se aduy sec ion
ea ly Yp esian SEE-10 2 Calca eous sands one 0%
SEE-9 2 Pck. Co als+Milioliids+CCA 1-3% xx x x x
SEE-8 3 Fls .(F m.) Co als+CCA c us s+Milioliids 1-5% xxx xx xxx
SEE-7 2 Fls .(F m.) Co als+CCA c us s+Milioliids 3-5% x x x x x x x x x
SEE-6 2 Pck. Co als+BF+CCA 5% x x x x x x x x x x x x x x
SEE-5 4 Pck. Co als+BF+CCA (c us s) 1-5% x x x x x x x x x x
SEE-4 2 Pck. Bioclas ic 1-5% xxxxxx
SEE-3 3 G n. Bioclas ic < 1% xx x
SEE-2 1 G n. Al eolina+Co als+BF 1-3% x x xx
SEE-1 2 G n. Al eolina+Milioliids < 1% xxxx
SEW-3 4 Fls .(F m.) Co als+CCA+Milioliids 1-3% x x x x x x x x x x x
la e Thane ian SEW-2
SEW-1 8 G n.-Pck. Co als+BF+CCA 20-50% x x x x x x x x x x x x x x x x x x
SEW-0 2 Fls .(F ame.) Co als+Fo ams 1-3% x x x x x
Wck, Wackes one; Pck, Packs one; G n, G ains one; Rud, Ruds one; Fls , Floas one; F, F ames one; CCA, C us ose co alline algae; B yos, B yozoans; LBF, La ge ben hic o amini e a; BF, Ben hic o amini e a; Rhodos, Rhodoli hs.
Agui e e al. Co alline Paleocene/Eocene The mal Maximum
F on ie s in Ma ine Science | www. on ie sin.o g July 2022 | Volume 9 | A icle 8998777
Agui e, 2004;Agui e e al., 2017). Pa icula ly in e es ing is he
ela i e abundance o genicula e co alline algae, which domina e
in high-ene gy in e idal, shallow-sub idal se ings, bo h in he
p esen day (Ga ba y and Johansen, 1982;Canals and
Balles e os, 1997;Cou o e al., 2014) and in he ossil eco d
(Scheibne e al., 2007;Qua an a e al., 2012;B andano, 2017). In
hese se ings, hey a e p one o disa icula ion and b eakage
a e dea h, hus, educing hei ossiliza ion po en ial (Agui e
e al., 2000a;Agui e e al., 2010;Basso, 2012). Du ing he la e
Thane ian, co alline algae di e sified in small co al buildups,
such as hose ound in he Se aduy sec ion (samples SEW-0 and
SEW-1) (Figu es 2B,7).
In addi ion o co alline algal agmen s, loosely and densely
packed hodoli h beds de eloped a he uppe pa o he Na a i
Fo ma ion.Al hough hodoli hshapeandalgalg ow h o msin he
ou e pa so he hodoli hscanbe wa e -dep handhyd odynamic
indica o s (B acchi e al., 2022), labo a o y expe imen s and field
obse a ions ha e shown ha in mos cases he e is no co ela ion
be ween hose ac o s (Agui e e al., 2017;B aga, 2017;O’Connell
e al., 2020; and e e ences he ein). In he Campo sec ion, se e al
e idences sugges ha hodoli h beds o med in ela i ely deep,
calm ma ine se ings, mos likely in a middle amp: 1) he ma ix
su ounding he hodoli hs is fine g ained-muddy ca bona e; 2)
Spo oli honspp.a emajo componen so he hodoli hs,indica ing
g ow hin ela i edeepwa e s(se e al enso me e s),asabundance
o Spo oli hales inc eases wi h wa e dep h (Adey and Macin y e,
1973;Adey, 1979;Minne y e al., 1985;Adey, 1986;F a ega e al.,
1989;Minne y,1990;Agui ee al.,2000a;B agaandAgui e,2001;
B aga and Agui e, 2004;B aga and Bassi, 2007;B aga e al., 2009);
and, 3) geope al fillings poin o a no mal pola i y o hodoli hs and
p ese a ion in g ow h posi ion wi hou significan ewo king.
The uppe mos ca bona e beds o he uppe Thane ian
Na a i Fo ma ion, immedia ely below he ka s su ace, a e
o e whelmingly domina ed by la ge lamina halli o D. bise ialis
dispe sed in a muddy (packs one-wackes one) ma ix (Figu e 8).
Loose lamina g ow h o ms o his co alline alga in fine-g ained
sedimen s sugges low ene gy condi ions. These sedimen s a he
op o he Na a i Fo ma ion a e in e p e ed as middle amp
deposi s as well (Scheibne e al, 2007;Li e al., 2020).
In he Campo sec ion, he Paleocene-Eocene bounda y is
ep esen ed by a subae ial e osional su ace ha eflec s a
p o ound paleoen i onmen al change in he s udy egion.
O e lying he uncon o mi y, con inen al clays, sands, and
discon inuous palus ine limes ones o he Cla e Fo ma ion
o med. Con inen al sedimen a ion was coe al wi h a sea le el
lowe ing du ing he ca bon iso ope excu sion (CIE) eco ded a
he Paleocene/Eocene ansi ion (e.g., Pujal e e al., 2014;Pujal e
e al., 2022). In he Campo sec ion, he con inen al in e al is
o e lain by packs one-wackes one beds o al eolinids, which a e
opped, in u n, by lamina ed mic obial ca bona es (uppe
deposi s o IL-1 sequence). The almos exclusi e dominance o
Al eolina indica es ha hey o med in a e y es ic ed lagoon
wi h p obable fluc ua ions in salini y (BouDaghe -Fadel, 2018).
The p o use de elopmen o mic obial lamini es, wi h e apo i e
mine als, e eals ma ginal/ e y es ic ed o e en ually
hype saline en i onmen al condi ions. Co alline algae we e
absen in all hese se ings. S a al geome y o hese fi s
ma ine beds shows an onlap indica ing ela i e sea-le el ise,
which inc eased accommoda ion.
Highe up in o he s udy sec ions, milioliids and locally
oys e s (sample CPE-14), oge he wi h Al eolina, domina e
he ossil assemblages. Milioliids a e small ben hic o amini e s
p e e en ially inhabi ing lagoons (Mu ay, 1991;Mu ay, 2006).
Dasyclads a e also abundan in he lowe Yp esian ca bona es,
pa icula ly in he Se aduy sec ion (Table 1). They p e e en ially
inhabi low la i ude, shallow bays and lagoons (Flügel, 1985;
Flügel, 1991;Be ge and Kae e , 1992;Agui e and Riding, 2005;
Be ge , 2006).
FIGURE 3 |(A) Supe imposed halli o Polys a a alba (nucleus o he hodoli h) and co alline algae (sample SEW-15). (B) Ma inella lugeoni (sample CPE-7).
(C) Longi udinal sec ion o a Halimeda pla e (sample CPE-5). (D) Oblique sec ion o a dasycladalean g een alga (sample SEE-6i).
Agui e e al. Co alline Paleocene/Eocene The mal Maximum
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Locally, small co al pa ches, co esponding o samples CPE-
15 and CPN-3 o he Campo sec ion, as well as samples SEW-3
and SEE-5—SEE-9 o he Se aduy sec ion, g ew in hese
shallow-wa e en i onmen s domina ed by al eolinids. Co als
a e embedded in a wackes one-packs one ma ix, e y ich in
milioliids, and sugges ela i ely no mal ma ine condi ions,
p obably in lagoonal a eas wi h connec ion wi h open ma ine
wa e s. The only eco ds o co allines in he lowe Yp esian
deposi s o he Campo sec ion a e ound in he co al pa ches a
he base o sequence IL-2. In he Se aduy sec ion, co alline algae
a e p esen bu sca ce in all samples om he lowe Yp esian IL-2
sequence, being mo e abundan in he co al buildups (Table 1).
In he Campo sec ion, he lowe Yp esian ca bona es abo e he co al
buildups ep esen a p og essi e deepening end, as in e ed by he
p og essi e di e sifica ion o he la ge ben hic o amini e assemblages
(pa icula ly, nummuli ids) as well as o he in e eb a es (bi al es,
gas opods, and echinode ms). In he uppe mos pa o he sec ion, a
monospecific bed o lucinids p ese ed in li e posi ion (below sample
CPE-19) is ound. The amily Lucinidae is one o he mos di e sified
g oups o bi al es in chemosyn he ic communi ies associa ed wi h
hyd o he mal en s and cold seeps, disoxic bo om condi ions and/o
eu ophic se ings (Taylo and Glo e , 2006). This sugges s he
p e alence o ha sh condi ions o co alline algae du ing he ea ly
Yp esian deepening in he Campo sec ion.
FIGURE 4 |(A, B) G ains one- uds ones o bioclas s including genicula e co alline algae (gen), D. bise ialis (Db), la ge ben hic o amini e a (LBF), echinoids (ech),
small ben hic o amini e a (sb ), and M. lugeoni (Ml) (A: sample CPE-4; B: sample CPE-7). (C, D) Thin lamina enc us ing co alline algae coa ing co als (Co)
embedded in a wackes one ma ix (C: sample SEW-2ii; D: sample SEE-6). (E) Spo oli hon sp. engulfing genicula e co alline algae (sample SEW-1ii).
Agui e e al. Co alline Paleocene/Eocene The mal Maximum
F on ie s in Ma ine Science | www. on ie sin.o g July 2022 | Volume 9 | A icle 8998779
species epi he show g ow h o m, hallus cons uc ion,
ege a i e ana omy and ep oduc i e s uc u es compa able
wi h he ype ma e ial o L. co allinae o me Lemoine, 1924 as
eassessed by Agui e e al. (2012).Li ho hamnion ma ianae
Johnson, 1957 p esen s simila i ies wi h Lemoine’s species.
The g ow h o ms (slende , long b anches), as well as he cell
size and shape ( ec angula o polygonal wi h a hickened cell
wall) a e ana omical ea u es highligh ed bo h by Johnson
(1957) and by Agui e e al. (2012) in he desc ip ion o he
wo species.
4. Li ho hamnion c . exube ans Mas o illi 1967 (Figu e 10D).
This species occu s as agmen ed b anches. Cell filamen s in
he cen e o he b anch o m egula g ow h zones.
Spo angial concep acles sligh ly p o ude abo e he hallus
FIGURE 11 |(A) Li ho hamnion sp. 3 (sample CPE-15). (B) Li ho hamnion sp. 4 (sample SEE-5i). (C) Li ho hamnion sp. 5 (sample SEW-3ii). (D) Jania nummuli ica
(sample CPE-4i). (E) Genicula e sp. 1 (c . Co allina p isca) (sample CPE-4). (F) Genicula e sp. 2 [sample (CPE-4ii)]. (G) Genicula e sp. 2 (sample SEE-5i).
(H) Genicula e sp. 3 (sample SEE-6i). (I) Ka pa hia sphae ocellulosa (sample CPE-5iii). (J) Hyd oli hon lemoineii (sample SEE-6i). (K) Li hopo ella minus (sample SEW-
1i). (L) L. minus showing a unipo a e spo angial concep acle pa ially p ese ed (sample CPE-8iii). (M) Li hopo ella melobesioides (sample CPE-10iii).
Agui e e al. Co alline Paleocene/Eocene The mal Maximum
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su ace and measu e abou 200 mm in diame e and 100-130
mm in heigh . They a e sligh ly apezoidal bu i egula in
shape and possess conspicuous po e canals in he oo . The
specimens showing hese ea u es can be assigned o he
species Li ho hamnion exube ans Mas o illi, 1967,who
highligh ed he i egula shape o he spo angial
concep acles, which is a ypical cha ac e o he s udy
ma e ial. Simila co alline algae we e desc ibed as
Li ho hamnion sp. 4 by Agui e e al. (2020) om he
middle Eocene ca bona es o Subbe ic Zones, Be ic
Co dille a (S Spain), Colombia, and Dominican Republic.
5. Li ho hamnion c ispi hallus Johnson 1957 (Figu e 10H).
Thin hallus wi h a well-de eloped plumose en al co e
and a hin pe iphe al egion, which hickens subs an ially
su ounding concep acles. Spo angial concep acles, which
a e c owded in po ions o he hallus, p o ude on he
hallus su ace gene a ing a wa -like s uc u e. They a e
ec angula o dome-like in shape anging om 190 mm o
250 mm in diame e and om 100 mm o 140 mm in heigh .
This alga occu s a ached o ha d skele ons o as c us s
isola ed in he sedimen . Johnson (1957) highligh ed he
c owding o he concep acles as cha ac e is ic o he species.
Li ho hamnion cha ollaisi Segonzac and Cha ollais 1974
shows simila i ies wi h L. c ispi hallus. None heless, he
desc ip ion o he species is e y limi ed p ecluding easible
compa isons.
6. Li ho hamnion aughani Howe 1919b (Figu e 10E). In he
p o ologue o his species, Howe (1919b) indica ed “p ima y
hypo hallia somewha educed, …. a he i egula ly a anged
(i.e., no dis inc ly “coaxial”)”(Howe, 1919b;p.6).
FIGURE 12 |(A) Li hopo ella melobesioides (sample SEW-3ii). (B) Lamina halli o Dis ichoplax bise ialis in a wackes one ma ix (sample CPE-9). A ows ma k cell
usions. (C) D. dbise ialis showing a unipo a e spo angial concep acle (sample SEE-9). A ow ma ks cell usions. (D) Oblique sec ion o a lamina o D.bise ialis
(sample CPE-9). A ows ma k cell usions. (E) Spongi es sp. 3 (sample CPN-3). (F) Spongi es sp. 2 (sample CPN-5ii). (G) Spongi es sp. 1 (sample CPE-7).
Agui e e al. Co alline Paleocene/Eocene The mal Maximum
F on ie s in Ma ine Science | www. on ie sin.o g July 2022 | Volume 9 | A icle 89987717
La e , Lemoine (1928; see also Lemoine, 1939) ans e ed he
species o he new genus Mesophyllum ha she desc ibed: “Les
espèces ossiles qui me pa aissen ai e pa ie du gen e
Mesophylllum son : …M. aughani Howe”(Lemoine, 1928;
p. 253). This new genus a ibu ion has been ollowed by la e
au ho s. None heless, aking in o conside a ion he clea
e e ence o he plumose en al co e we keep he o iginal
genus a ibu ion by Howe (1919b).
7. Li ho hamnion sp. 2 (Figu e 10G). This species occu s as
u icoseo enc us ingplan swi hb anchesshowing
i egula in e nal zones. The mos cha ac e is ic ea u e is
ha nume ous mul ipo a e spo angial concep acles a e
g ouped in he ips o b anches o wa s. They a e mos ly
seconda ily filled by ad en i ious cells. Thallus mo phology,
in e nal o ganiza ion, concep acle shapes and sizes, and hei
dis ibu ion allow compa ing his species wi h Mesophyllum
schenckii Howe, 1934,Li ho hamnion wallisium Johnson and
Ta u , 1952, la e figu ed by Johnson and S ewa (1953), and
Li ho hamnion sp. S ocka (2000). I also shows ce ain
esemblance wi h Mesophyllum gale oi Mas o illi, 1967.
Membe s o he genus Mesophyllum p esen a
p edominan ly coaxial hypo hallus. None heless, in he
p o ologue o M. schenckii and M. gale oi,bo hHowe
(1934) and Mas o illi (1967), espec i ely, indica e he
p esence o a plumose en al co e. The specimens we ha e
s udied show plumose en al co e, so, we assign hem o
Li ho hamnion.
One specimen in sample SEW-1 shows a la ge iangula
concep acle wi h a long single po e in he oo . The po e
canal p o udes abo e he hallus su ace gene a ing a wa -
like p o ube ance. This alga shows he same g ow h
mo phology and hallus o ganiza ion as ha o
Li ho hamnion sp. 2, hus, we in e p e i as a game angial
plan o he species.
8. Undi e en ia ed Hapalidiales. Unde his ca ego y, we
include small uniden ifiable agmen s o enc us ing halli
wi h well-de eloped plumose hypo hallus and a hin
pe i hallus, which hickens a ound spo angial mul ipo a e
concep acles.
O de Co allinales (Figu es 11D–M,12)
1. Genicula e sp. 1 (Figu e 11E). I occu s as calcified
disa icula ed po ions o in e genicula wi h cell usions.
One po ion p esen s a unipo a e concep acle loca ed in a
e minal posi ion o he in e geniculum (Figu e 11E).
F agmen a ion p ecludes genus iden ifica ion; howe e ,
p ese ed ea u es emind hose o Co allina p isca
Johnson, 1957 om he la e Eocene o Saipan (Ma iana
Islands).
2. Genicula e sp. 2 (Figu es 11F, G). Dispe sed agmen s o
po ions o calcified in e genicula wi h cell usions. Two o
hese in e genicula p ese e unipo a e concep acles in he
e minal posi ion ha a e su ounded by la e al b anches.
One o he specimens show a small concep acle wi h a high
po e canal(Figu e 11F)and heo he is bigge wi ha sho po e
canal (Figu e 11G). The o me is en a i ely in e p e ed as a
possible game angial concep acle o he same axon.
3. Genicula e sp. 3 (Figu e 11H). A single hallus showing cell
usions and a big unipo a e spo angial concep acle de i ed
om co ical cells in a la e al posi ion o he in e geniculum.
4. Dis ichoplax bise ialis Die ich 1927 (Figu es 12B–D). This is
a widely known species, al hough i s a ibu ion has been
deba ed. In he s udy ma e ial, we ha e ound lamina halli
o D. bise ialis showing bo h concep acle p imo dia and oid
unipo a e spo angial concep acles (Figu e 12C), enabling he
assignmen o his species o he o de Co allinales. Simila
ep oduc i e s uc u es ha e been figu ed by Kiej (1963;
1964)andDieni e al. (1979). Recen ly, Sa ka (2018)
included his species wi hin he sub amily Li hophylloideae,
based on he absence o cell usions, an in e p e a ion also
e oneously made by Agui e e al. (2010). This species shows
e iden cell usions, al hough hey a e some imes nea ly
absen in some po ions o he hallus (Figu es 12C, D).
The e o e, i canno be conside ed a li hophylloid any longe
(Rösle e al., 2017;Peña e al., 2020b). A hanasiadis (1995)
al eady ques ioned he a ibu ion o Dis ichoplax o
Li hophylloideae and p oposed i s a fini y wi h Mas opho a
o Li hopo ella.
5. Spongi es sp. 1 (Figu e 12G). This species is ela i ely
equen in he s udy ma e ial. I occu s as c us s o
b oken b anches and is cha ac e ized by unipo a e
spo angial concep acles ha show sligh ly eccen ic po e
canals in he concep acle oo . (Figu e 12G). The eccen ic
po e canal is highligh ed by S ocka (1997) while desc ibing
wha he iden ified as Li hophyllum a um Con i 1945.
None heless, Con i (1945) did no men ion his ea u e in
he o iginal desc ip ion o he species. Fu he mo e,
spo angial concep acles o L. a um a e much bigge han
hose ound in he p esen s udy. Based on he ege a i e
ana omy and he ep oduc i e s uc u es, addi ional names
ha fi wi h ou ma e ial a e hose o iginally desc ibed as
Li hophyllum ice inum Mas o illi, 1973 o Li hophyllum
ligus icum Ai oldi, 1932.Vannucci (1970) figu ed a
specimen iden ified as Li hophyllum ligus icum showing a
unipo a e spo angial concep acle wi h an eccen ic po e
canal. The eassessmen o he Ai oldi’s ypema e ialby
Vannucci e al. (2008) led hem o synonymize L.
ligus icum and Li hophyllum pe andoi, Ai oldi 1932
a o ing he la e as he alid species name. Ai oldi
(1932) desc ibed a coaxial en al co e, he same hallus
o ganiza ion ha can be obse ed in Figu e (1A and
Figu e 4)o Vannucci e al. (2008). None heless, hese
au ho s desc ibed he ype ma e ial as ha ing a plumose
en al co e ( hei Figu e 2).
6. Spongi es sp. 2 (Figu e 12F). F agmen o a u icose plan
obliquely cu showing nume ous cell usions. A he ip o he
b anch, a unipo a e concep acle, 270 mm in diame e and 110
mm in heigh , is obse ed. The po e canal is pa ially isible.
7. Spongi es sp. 3 (Figu e 12E). Thin enc us ing monome ous
plan wi h hin en al co e and pe iphe al egion. The la e
hickens a ound a p o uding unipo a e concep acle 310 mm
in diame e and 115 mm in heigh (Figu e 12E). Concep acle
shape and size emembe Li hophyllum bassanense
Mas o illi, 1973.
Agui e e al. Co alline Paleocene/Eocene The mal Maximum
F on ie s in Ma ine Science | www. on ie sin.o g July 2022 | Volume 9 | A icle 89987718
8. Undi e en ia ed Co allinales. F agmen s o co alline algae
ha show cell usions and unipo a e spo angial concep acles
bu ha do no show enough ea u es o assign hem o any
species.
DATA AVAILABILITY STATEMENT
The o iginal con ibu ions p esen ed in he s udy a e included in
he a icle/supplemen a y ma e ial. Fu he inqui ies can be
di ec ed o he co esponding au ho .
AUTHOR CONTRIBUTIONS
All au ho s con ibu ed o he a icle and app o ed he
submi ed e sion.
FUNDING
JA and JCB we e unded by he esea ch p ojec PGC2018-
099391-B-100 o he Spanish Minis e io de Ciencia e Inno acion
and by he Resea ch G oup RNM-190 o he Jun a de Andalucı
a.
JIB acknowledges unding h ough he Resea ch G oup IT930-16
o he Basque Go e nmen Resea ch P og amme.
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